Rebecca A. Berman, Laura M. Heiser, Richard C. Saunders and...

Rebecca A. Berman, Laura M. Heiser, Richard C. Saunders and...
Rebecca A. Berman, Laura M. Heiser, Richard C. Saunders and Carol L. Colby
J Neurophysiol 94:3228-3248, 2005. First published May 11, 2005; doi:10.1152/jn.00028.2005
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Dynamic Circuitry for Updating Spatial Representations. III. From Neurons to Behavior
R. A. Berman, L. M. Heiser, C. A. Dunn, R. C. Saunders and C. L. Colby
J Neurophysiol, July 1, 2007; 98 (1): 105-121.
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J Neurophysiol 94: 3228 –3248, 2005.
First published May 11, 2005; doi:10.1152/jn.00028.2005.
Dynamic Circuitry for Updating Spatial Representations. I. Behavioral
Evidence for Interhemispheric Transfer in the Split-Brain Macaque
Rebecca A. Berman,1 Laura M. Heiser,1 Richard C. Saunders,2 and Carol L. Colby1
1
2
Department of Neuroscience and Center for the Neural Basis of Cognition, University of Pittsburgh, Pittsburgh, Pennsylvania; and
Laboratory of Neuropsychology, National Institute of Mental Health, Bethesda, Maryland
Submitted 10 January 2005; accepted in final form 4 May 2005
INTRODUCTION
We explore the visual world by directing our gaze to
locations of interest. The simple act of moving our eyes,
however, introduces a complex problem. With each eye movement, the brain receives a new snapshot of the world around us.
We nevertheless perceive the visual world as stable and can
effortlessly localize objects despite intervening eye movements. How does the brain achieve this spatial constancy?
Many mechanisms must contribute to the construction of a
dynamic representation of space that can take self-generated
movements into account. Of particular interest is the finding
that neurons can update or “remap” stimulus traces in conjunction with saccades (Duhamel et al. 1992a; Goldberg and Bruce
1990; Mays and Sparks 1980; Nakamura and Colby 2002;
Umeno and Goldberg 1997, 2001; Walker et al. 1995). Remapping involves a transfer of visual information from neurons that
Address for reprint requests and other correspondence: C. L. Colby, 115 Mellon
Institute, 4400 5th Ave, Pittsburgh, PA 15213 (E-mail: [email protected]).
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represent a stimulus location before the eyes move, to those
that represent the location after the eye movement. The result
is an internal representation of space that is in register with
incoming retinal information—a representation that can contribute to spatial constancy. Relatively little is known about the
pathways that underlie the communication of visuospatial
signals necessary for updating.
The overarching aim of this research is to elucidate the
neural pathways necessary for updating spatial representations
when the eyes move. In this first study, we used behavioral
methods to assess the necessity of direct cortico-cortical links
in spatial updating. We used a simple behavioral task, the
double-step saccade task, which reveals the brain’s capacity to
construct a dynamic map of space that takes eye movements
into account. In this task, subjects make consecutive saccades
to two briefly appearing targets (Hallett and Lightstone 1976).
The crucial feature of this task is that the second target is
visible only when the eyes are at the initial fixation point.
Consequently, there is a disparity between the initial retinal
coordinates of the second target and the ultimate motor coordinates required to make a saccade to the location of this
remembered target. Accurate double-step performance requires
that the stimulus trace of the second target be updated in
conjunction with the first saccade. Both humans and monkeys
can accurately perform the double-step task (Gnadt and
Andersen 1988; Goldberg and Bruce 1990; Hallett and Lightstone 1976; Mays and Sparks 1980). Furthermore, performance
of the double-step task is accurate even when the second target
must be updated from one visual hemifield to the other (Baizer
and Bender 1989; Becker and Jurgens 1979; Dassonville et al.
1995; Goldberg et al. 1990; Jeffries et al. 2003; Li and
Andersen 2001; Zivotofsky et al. 2003). This across-hemifield
updating presumably requires a transfer of information between neurons in opposite hemispheres, given that the representation of visual stimuli is highly lateralized (Trevarthen
1990). We took advantage of this lateralization to investigate
the role of direct cortico-cortical pathways in spatial updating.
We hypothesized that the forebrain commissures—the corpus callosum and anterior commissure—serve as the primary
path for updating the representations of visual stimuli from one
hemifield to the other. The corpus callosum, with roughly half
a billion fibers, constitutes the most prominent route for interhemispheric communication (Houzel et al. 2002; Lamantia and
Rakic 1990). The corpus callosum and anterior commissure
provide extensive links between visuospatial and oculomotor
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Berman, Rebecca A., Laura M. Heiser, Richard C. Saunders,
and Carol L. Colby. Dynamic circuitry for updating spatial
representations. I. Behavioral evidence for interhemispheric transfer
in the split-brain macaque. J Neurophysiol 94: 3228 –3248, 2005. First
published May 11, 2005; doi:10.1152/jn.00028.2005. Internal representations of the sensory world must be constantly adjusted to take
movements into account. In the visual system, spatial updating provides a mechanism for maintaining a coherent map of salient locations
as the eyes move. Little is known, however, about the pathways that
produce updated spatial representations. In the present study, we
asked whether direct cortico-cortical links are required for spatial
updating. We addressed this question by investigating whether the
forebrain commissures—the direct path between the two cortical
hemispheres—are necessary for updating visual representations from
one hemifield to the other. We assessed spatial updating in two
split-brain monkeys using the double-step task, which involves saccades to two sequentially appearing targets. Accurate performance
requires that the representation of the second target be updated to take
the first saccade into account. We made two central discoveries
regarding the pathways that underlie spatial updating. First, we found
that split-brain monkeys exhibited a selective initial impairment on
double-step sequences that required updating across visual hemifields.
Second, and most surprisingly, these impairments were neither universal nor permanent: the monkeys were ultimately able to perform
the across-hemifield sequences and, in some cases, this ability
emerged rapidly. These findings indicate that direct cortical links
provide the main substrate for updating visual representations, but
they are not the sole substrate. Rather, a unified and stable representation of visual space is supported by a redundant cortico-subcortical
network with a striking capacity for reorganization.
BEHAVIOR OF SPATIAL UPDATING IN THE SPLIT-BRAIN MONKEY
FIG. 1. Comparison of double-step saccade conditions that require the
second target representation to be updated across or within visual hemifields.
In each condition, the monkey’s task is to make a visually guided saccade to
T1, followed by a memory-guided saccade to T2. In the across-hemifield
condition (A), T2 appears in the right visual field when the eyes are at the
central fixation point (FP), and therefore is initially represented by neurons in
the left hemisphere (black T2). When the eyes reach T1, however, the memory
trace of T2 is now located in the left visual field. This location is encoded by
neurons in the right hemisphere (gray T2⬘). Consequently, updating in this
condition must involve an interhemispheric transfer of visual information. In
the within-hemifield condition (B), T2 appears in the right visual field when the
eyes are at FP; the memory trace of T2 is still in the right visual field when the
eyes reach T1. Updating therefore involves communication between sets of
neurons within the same cortical hemisphere. We expected that, in the absence
of the forebrain commissures, performance of the across-hemifield condition
would be selectively impaired.
J Neurophysiol • VOL
tially. We carried out five sets of experiments to characterize
the initial deficits and unexpected recovery of the behavior
associated with across-hemifield updating in the split-brain
monkey.
METHODS
Subjects
Subjects were three adult rhesus macaques, two male and one
female, weighing 6.5–7.5 kg. Two monkeys, designated EM and CH,
underwent a commissurotomy to remove the corpus callosum and
anterior commissure. In the third monkey, FF, these commissures
were intact. All experimental protocols were approved by the University of Pittsburgh Institutional Animal Care and Use Committee and
were certified to be in compliance with guidelines set forth in the
Public Health Service Guide for the Care and Use of Laboratory Animals.
The commissurotomy was performed at the outset of the experiment. This surgery is extremely invasive, requiring exposure of the
cranial cavity, which leaves the brain vulnerable to infection. The
surgery is riskier still because it requires transection of a deep
structure, the anterior commissure. For these reasons, it was critical
for us to take every precaution to minimize the risk of infection. Had
we installed even a small cranial implant before the commissurotomy,
this would have resulted in a less than sterile surgical field and
compromised the chances for recovery. Accordingly, we installed an
implant for behavioral testing only after the commissurotomy, when
healing was complete. Details of the surgical procedure can be found
in Vogels et al. (1994). The monkeys were prepared for this surgery
with dexamethasone, and anesthesia was induced with ketamine and
maintained with isoflurane. Mannitol was administered throughout the
surgery to minimize tissue swelling. Under sterile conditions, a bone
flap was made and the underlying dura turned to allow access to the
corpus callosum with gentle retraction of the right hemisphere. The
callosum was transected along its full length using a small glass
pipette with suction. The anterior commissure was viewed through the
third ventricle and then transected. After completing the transection of
the forebrain commissures, the dura was returned and the bone flap
sewn back into position. In the 2 wk after the surgery, analgesics were
given to control postsurgical pain and antibiotics were administered
daily to prevent infection.
The complete transection of the anterior commissure and corpus
callosum was verified by direct vision at the time of surgery. Several
months after the surgery, we used magnetic resonance (MR) imaging
to confirm the absence of the commissures in coronal images spanning
the entire anterior–posterior extent of cortex. Structural MR images
were acquired using the 4.7-T magnet at the Pittsburgh NMR Center.
Images from a normal monkey and from the split-brain monkeys are
shown in Fig. 2, A–C.
After recovery, the animals were prepared for behavioral training.
Under general anesthesia (induced with ketamine and maintained with
isoflurane), scleral search coils were implanted for monitoring eye
position (Judge et al. 1980), and head restraint bars were affixed for
the purpose of holding the head stable during testing sessions (Nakamura and Colby 2000). This procedure could not be conducted until
the skull was fully healed. The time between the commissurotomy and
the beginning of behavioral training was 2 mo for monkey CH and 7
mo for monkey EM.
Stimuli
During behavioral sessions, the monkey sat with its head fixed in a
primate chair, in a darkened room. The monkey faced a tangent
screen, which subtended about 100° horizontally and 75° vertically.
Visual stimuli were back-projected onto the screen using an LCD
projector. Stimulus presentation was under the control of two computers running a C-based program, CORTEX, made available by R.
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areas in each hemisphere (Demeter et al. 1990; Hedreen and
Yin 1981; Jouandet and Gazzaniga 1979; Pandya and Vignolo
1969; Schwartz and Goldman-Rakic 1984; Seltzer and Pandya
1983). The absence of these commissures has important functional consequences, both for neural processing and for behavior. The corpus callosum and anterior commissure contribute
critically to the receptive field properties of individual neurons
in striate cortex and in the ventral stream (Berlucchi and
Rizzolatti 1968; Desimone et al. 1993; Gross et al. 1977).
Furthermore, the commissures are necessary for integrating
visual stimuli across hemifields, especially form and color
information (Corballis 1995; Eacott and Gaffan 1989; Gazzaniga 1987; Gazzaniga et al. 1962; Land et al. 1983; Trevarthen
1990). Behavioral evidence from split-brain and acallosal humans indicates that information about spatial locations can be
transferred between hemispheres in the absence of the corpus
callosum, but only in limited circumstances and with coarse
spatial resolution (Corballis 1995; Hines et al. 2002; Holtzman
et al., 1981, Holtzman 1984; Reuter-Lorenz and Fendrich
1990). We asked whether stimulus traces can be accurately and
precisely updated from one hemisphere to the other, when all
direct links between the cortical hemispheres are severed. Our
expectation at the outset of these experiments was that acrosshemifield spatial updating would be abolished in the absence of
the forebrain commissures.
We tested this prediction by measuring the performance of
split-brain monkeys on two conditions of the double-step task.
In the across-hemifield condition (Fig. 1A), updating requires a
transfer of visual information between neurons in opposite
hemispheres. In the within-hemifield condition (Fig. 1B), updating involves a transfer of visual information between sets of
neurons within the same hemisphere. We expected that splitbrain monkeys would exhibit selective impairment on the
across-hemifield but not the within-hemifield condition. We
found that across-hemifield updating could be profoundly impaired after transection of the commissures. Nevertheless,
performance in these double-step sequences recovered substan-
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R. A. BERMAN, L. M. HEISER, R. C. SAUNDERS, AND C. L. COLBY
second target (T2) appeared 100 ms later and was extinguished after
50 ms. FP was extinguished simultaneously with T2 offset, cueing the
monkey to initiate the double-step sequence. T1 was extinguished
once the monkey attained it. If the monkey successfully reached the
T2 location, this target reappeared after 100 ms. The monkey was
required to refixate T2 for an additional 300 –500 ms to receive a juice
reward. In expt 5, we measured performance on a delayed version of
the double-step task, which was identical to the standard task in all
respects, except that the monkey had to maintain fixation during a
300- to 500-ms delay period before generating the sequence.
Spatial configuration of the double-step task
Desimone at the National Institutes of Mental Health. In the doublestep task, the critical feature is that the monkeys have retinal information about the second target (T2) only when the eyes are at central
fixation; once the eyes reach the first target (T1) they must rely on an
updated representation of the stimulus trace to generate the second
saccade. It was therefore important to demonstrate that the T2 stimulus had disappeared before the monkeys initiated the first saccade to
T1. To do this, we used a photodiode to measure the phosphopersistence of the briefly flashed T2 stimulus. The stimulus did not
vanish instantaneously when it was turned off, but decayed to half its
luminance with a time constant of 8 ms. We then calculated the
luminance threshold for each monkey, using a memory-guided saccade task (Hikosaka and Wurtz 1983). By gradually dimming the
flashed stimulus, we determined the luminance at which the monkey
could no longer generate saccades to the location of the flashed
stimulus. For all three monkeys, the stimulus fell below perceptual
threshold within 40 ms of its extinction. On average, the monkeys
took 152.5 ms (⫾36.4 ms SD) to initiate the first saccade (S1), and
minimum acceptable S1 latency was 50 ms. These observations
indicate that the monkeys had access to retinal information about the
T2 stimulus only when the eyes were fixated centrally; correct
performance on the double-step task thus relied on updating the
stimulus trace of T2.
Data collection and identification of saccades
Eye position was monitored using scleral search coils (Judge et al.
1980). Eye position was sampled at 250 Hz (monkeys EM and FF) or
100 Hz (monkey CH). Eye data were stored for off-line analysis,
along with CORTEX event markers, which indicated when stimuli
appeared and were extinguished.
Data processing and statistical analyses were carried using customwritten MATLAB programs and SPSS. For all experiments, saccades
were identified in MATLAB on the basis of velocity criteria. The
beginning of the saccade was defined as the timepoint when velocity
exceeded 50°/s. The end of the saccade was defined as the timepoint
when velocity fell below 20°/s. The accuracy of saccade identification
was verified on a trial-by-trial basis.
Timing of the double-step task
At the beginning of each trial, the monkey fixated a central fixation
point (FP) for 300 –500 ms. The first target (T1) then appeared. The
J Neurophysiol • VOL
Training on the double-step task
Our objective was to train the animals extensively on the doublestep task, so that they were proficient on the task and could respond
accurately even on double-step sequences they had not seen before.
This approach was important for ensuring that, if deficits were
present, we could attribute the deficits to impaired spatial updating
rather than to a general inability to adapt to new target arrangements.
It was also critical that we train the animals without using sequences
that resembled either of two critical test conditions (within-hemifield
or across-hemifield). Training took place in two stages. In the first
stage, we used a vertical version of the double-step task. In these
sequences, the first target (T1) appeared directly above or directly
below central fixation. The second target (T2) appeared either in the
left (LVF) or right visual field (RVF). For these vertical sequences,
the location of T2 was represented by the same cortical hemisphere
both when the eyes were at fixation and when the eyes reached T1.
The monkeys were trained to a criterion of 75% correct for all
sequences in the upper and lower visual fields. Both split-brain
monkeys reached criterion after about 4 mo of training; the normal
monkey reached criterion within 1 mo.
Once the animals had learned to perform the vertical double-step
sequences, we moved to the second stage of training. In this second
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FIG. 2. Verification of commissurotomy (A–C) and timing of the doublestep saccade task (D). A: coronal magnetic resonance (MR) images from a
normal monkey. B and C: comparable images from split-brain monkeys EM
and CH. Arrows point to the location of the corpus callosum (A) or its absence
(B, C). D: events of the standard double-step task (see METHODS).
For each testing session, we measured double-step performance in
three conditions (Fig. 3A). One condition, the central condition, was
always familiar to the monkeys. The other two conditions, withinhemifield and across-hemifield, were both unfamiliar. All three conditions began with a first saccade directed either to the right or to the
left. 1) In the well-trained central condition, the second saccade was
vertical. This sequence did not require interhemispheric transfer of
visual information. 2) In the within-hemifield condition, updating
required a transfer of visual signals within the same hemisphere. 3) In
the across-hemifield condition, updating required an interhemispheric
transfer of visual signals. We tested these conditions in each quadrant
of the visual field, testing upper and lower fields in separate sessions.
In each session, then, six sequences were randomly interleaved without replacement; trials did not repeat on error.
In the standard paradigm (expt 1), the first and second saccades
were 12° in amplitude. The within- and across-hemifield S2 trajectories were offset from the central S2 by 30° in angle. The location of
T2 was at an eccentricity of 12° for the central condition, 18° for the
within condition, and 6° for the across condition. Electronic eye
windows were ⫾2° at central fixation and T1 and ⫾2.7° at T2. In
expts 2–4, we tested performance on the double-step task using
different target geometries, which are described in RESULTS. For these
experiments, eye windows were adjusted such that the T1 and T2 eye
windows were equal to about 15% and about 20% of saccade amplitude, respectively. The eye windows for T2 were less stringent than
those for T1 because saccades are known to be less accurate when
directed toward a remembered target compared with a visual target
(Barash et al. 1991). The T2 eye windows were always constrained so
as to be nonoverlapping for the three targets (within, central, across)
in each quadrant.
BEHAVIOR OF SPATIAL UPDATING IN THE SPLIT-BRAIN MONKEY
stage, we used only one condition, the central condition (Fig. 3A,
black lines). On central sequences, the first saccade was a horizontal
saccade, directed 12° either to the right or to the left. The second
saccade (also 12° in amplitude) was vertical, and so did not require
across-hemifield updating of the T2 stimulus trace. The monkeys were
trained to perform the central condition in each of the four visual
quadrants. This stage of training proceeded rapidly, requiring only a
single session for monkeys CH and FF to reach criterion, and two
sessions for monkey EM. In further training sessions, we varied the
saccade amplitude of the central sequences, to reinforce the principle
of the task and ensure the monkeys’ ability to adapt to changes in
target geometry. The rapid acquisition of the central sequences indicated that the monkeys were proficient on the double-step task. After
these two stages of training were complete and the animals were very
good at the task, we began testing in expt 1.
Data analysis
RESULTS
Experiment 1: Initial impairment of
across-hemifield sequences
We began behavioral testing after the monkeys completed
both stages of training on the double-step task, described in
J Neurophysiol • VOL
METHODS.
Monkeys were able to perform an extensive set of
double-step sequences accurately, and had demonstrated an
ability to generalize when presented with sequences they had
not previously seen. It was crucial that the monkeys had not yet
encountered the two conditions of experimental interest, the
within-hemifield and across-hemifield conditions (Fig. 3A, red
and green lines). On the trained central sequences, their performance reliably exceeded 75% correct (Fig. 3A, black lines).
With this evidence that the animals understood the double-step
task, we proceeded to test the essential question: could the
split-brain monkeys perform double-step sequences that required updating from one visual hemifield to the other? We
tested the monkeys’ double-step performance in the upper
visual field in the first session, and in the lower visual field on
the subsequent day. In each session, we simultaneously introduced four test sequences, two across-hemifield and two within-hemifield conditions, in the right and left visual fields.
Across- and within-hemifield sequences were equally unfamiliar and were counterbalanced for the direction of the first and
second saccades. This design isolated the difference of interest:
accurate double-step performance required either across-hemifield or within-hemifield spatial updating. These initial testing
sessions were critical because the monkeys’ performance was
not confounded by experience with either test condition (within
or across). As such, these sessions provide unique insight into
the integrity of spatial updating in the split-brain monkey.
PERFORMANCE ON EARLY TRIALS. In each animal, first exposure
to the across- and within-hemifield conditions revealed a conspicuous and selective impairment for sequences that required
updating across visual hemifields. Eye traces from the upper
field demonstrate the initial double-step deficit (Fig. 3B).
Traces from the central condition show that the monkeys were
very accurate in the execution of these well-trained sequences.
The monkeys were also able to perform the within condition
with considerable accuracy, despite the fact that these particular sequences were unfamiliar. In contrast, both monkeys
made inaccurate movements on every trial of the first ten
across-hemifield sequences. On these trials, the trajectory of
the second saccade deviated substantially from the ideal trajectory, and resembled a straight vertical saccade. These data
are consistent with the prediction that performance on acrosshemifield sequences would be impaired in the absence of the
forebrain commissures.
Eye traces from the lower field, tested on Day 2, show a
similar pattern but also reveal some surprising dissimilarities
(Fig. 3C). As in the upper field, both monkeys performed well
on central and within conditions. Monkey EM showed a clear
impairment for the across-hemifield sequences: saccade trajectories were predominantly vertical, in keeping with observations in the upper field. Monkey CH, however, was able to
execute the lower-field across-hemifield sequences with considerable accuracy, even in the first ten trials. This successful
performance may have emerged partly as a result of the order
of testing. We tested the upper visual field first and the lower
field sequences on the subsequent day. This raises the possibility that monkey CH, having learned to perform the acrosshemifield sequence in the upper left quadrant on the first day
(see below), was able to generalize rapidly to the lower field
sequences.
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We excluded from analysis any double-step trials in which the
latency of the first saccade was ⬍50 or ⬎500 ms. In addition, we
excluded trials in which the monkey attained T1 but directed the
second saccade into the wrong vertical visual field. Trials in which the
first saccade went to neither T1 nor T2 were also excluded from
further analysis. Having removed anticipatory or otherwise erratic
trials from analysis, we classified the trials according to error type,
defined as follows. Correct trials were those in which the first saccade
reached T1 and the second saccade reached T2. S2 error trials were
those in which the first saccade reached T1 but the second saccade
failed to reach T2. T2-first trials were those in which the first saccade
was directed to T2, rather than to T1. The criteria for a saccade to
reach a target location were implemented in off-line analysis, by
measuring angular error (angular offset between the saccade trajectory
and the ideal trajectory) and distance error (distance between the
saccade endpoint and the target). For the first saccade, angular error
had to be ⬍10° and distance error had to be ⬍15% of the target’s
amplitude (i.e., a gain of 0.85). For the second saccade, angular error
had to be ⬍12° and distance error had to be ⬍20%.
We assessed accuracy and latency by conducting a univariate ANOVA
to determine the significance of three independent factors: updating
condition (central, within, or across), direction of the first saccade (“S1
direction, ” right or left), and vertical visual field (upper or lower). This
analysis included only those trials where the monkey accurately reached
T1 (i.e., correct trials and S2 error trials). ANOVAs were conducted
separately for each monkey. We used post hoc analyses to determine
whether specific across-hemifield sequences were significantly impaired.
We corrected for all possible pairwise comparisons between the sequences (Tukey’s HSD [Honestly Significantly Different], calculated at
␣ ⫽ 0.05 for 66 pairs), but focused on the comparison of each of the
across-hemifield sequences to three matched sequences that controlled
for saccade metrics and unfamiliarity. The well-trained central sequence
in the same hemifield was matched for direction of the first saccade. The
within-hemifield sequence in the same hemifield was matched for unfamiliarity and for direction of the first saccade. The within-hemifield
sequence in the opposite hemifield was matched for unfamiliarity and the
direction of the second saccade. If all three pairwise comparisons were
significant, we concluded that there was an impairment in spatial updating, rather than an impairment related to saccade metrics or to encountering unfamiliar sequences. Throughout the results, we refer to individual across-hemifield sequences as being significantly impaired only if
they met these criteria.
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R. A. BERMAN, L. M. HEISER, R. C. SAUNDERS, AND C. L. COLBY
DOUBLE-STEP SACCADE ENDPOINTS FROM THE FIRST SESSION. Are
the eye traces from these early trials representative of the
monkeys’ performance throughout the entire first session of
testing? For monkey EM, the impairment of the across-hemifield sequences was clearly present throughout the first session
(Fig. 3D). In both the upper and lower visual fields, the
endpoints for the across-hemifield sequences (red) were clustered far from the correct endpoint. By comparison, endpoints
for the central sequences (black) and within sequences (green)
were clustered near the correct T2 locations. For monkey CH,
the endpoint data were more variable (Fig. 3E). In the upper
right field, impairment on the across-hemifield sequence continued throughout the session. Endpoints for this sequence
resembled those for monkey EM. In the upper left quadrant,
however, many endpoints for the across-hemifield sequence
were clustered near the correct T2 location. This reflects the
fact that performance improved as the monkey gained experience in the first session (about 200 trials of this sequence). In
the lower field, monkey CH performed both across-hemifield
J Neurophysiol • VOL
sequences with considerable accuracy throughout the session
(Day 2 of testing).
The data in Fig. 3 show two contrasting results: in the
absence of the forebrain commissures, the performance on
across-hemifield sequences was impaired in most cases, but
was surprisingly accurate in a few cases. These results are
borne out in quantitative analysis, described below. We characterized the monkeys’ initial performance using three analytic
approaches. First, we classified the trials according to error
type. Second, we quantified saccadic accuracy and latency and
subjected these measures to statistical analyses. Finally, we
investigated the precision of the monkeys’ across-hemifield
performance.
FEWER CORRECT TRIALS FOR ACROSS-HEMIFIELD UPDATING IN THE
FIRST SESSION. In the first analysis, we determined the per-
centage of trials belonging to each of three categories: 1)
correct; 2) S2 errors, in which the monkey made an accurate
saccade to T1 but not to T2; and 3) T2-first errors, in which the
monkey’s first saccade went directly to T2 (Fig. 4). For both
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FIG. 3. Initial double-step performance of split-brain monkeys for across-hemifield compared with within-hemifield
updating. A: standard test configuration: testing was conducted first in the upper field (shown) and then in the lower
field. Horizontal arrows represent the first saccade from FP to
the first target, T1. In each quadrant, the second target (T2)
appeared at one of 3 locations. Central sequences (black)
served as the training condition; within-hemifield (green) and
across-hemifield (red) conditions were introduced simultaneously. B and C: traces show the eye path for the first 10
trials of each sequence. Dots indicate the locations of FP, T1,
and T2. Brackets represent 10°. D and E: saccade endpoints
from the first session of across-hemifield testing. Lines show
ideal trajectories for the second saccade of each sequence.
Lines and endpoints are colored according to condition, as in A.
BEHAVIOR OF SPATIAL UPDATING IN THE SPLIT-BRAIN MONKEY
monkeys, percentage correct (filled columns) typically was
high for the central (black) and within-hemifield conditions
(green). The percentage correct for the across-hemifield condition (red) varied by monkey and visual quadrant. For monkey
EM, percentage correct was 0, regardless of visual quadrant.
For monkey CH, it ranged from 0% (upper RVF) to 80%
(lower RVF).
We found that the two monkeys exhibited distinct behavior,
not only in terms of the percentage correct for across-hemifield
trials, but also in terms of the kinds of errors committed. For
monkey EM, all of the error trials were S2 errors (open
columns). For monkey CH, error trials also included T2-first
errors (hatched columns). These T2-first errors occurred almost
exclusively for the across-hemifield sequences. The differences
in error types indicate that the monkeys may have used different strategies in response to the across-hemifield condition.
ACROSS-HEMIFIELD IMPAIRMENT OF SACCADE ACCURACY IN THE
FIRST SESSION. In the second analysis, we quantified saccade
field (both monkeys, P ⬍ 0.0001). Our primary interest was to
determine whether individual across-hemifield sequences were
significantly impaired, relative to central and within-hemifield
sequences that controlled for saccade metrics and unfamiliarity. Accordingly, we conducted post hoc pairwise comparisons,
focusing on the contrast between each across-hemifield sequence and three matched sequences, the central and within
sequences in the same quadrant, and the within sequence in the
opposite hemifield (see METHODS). If the across-hemifield sequence was significantly impaired relative to all three matched
sequences, we concluded that there was a deficit in updating,
rather than an impairment related to encountering an unfamiliar
sequence, or related to the metrics of the first or second saccade.
In monkey EM, accuracy was significantly impaired for all
four across-hemifield sequences (increased S2 error, Fig. 5, A
and B). In monkey CH, accuracy was impaired for two of the
across-hemifield sequences, both in the upper visual field (Fig.
5A). We conclude that double-step performance in these initial
sessions was generally, although not always, less accurate for
across-hemifield sequences compared with matched central
and within sequences.
Previous studies indicate no differences between the accuracy of across-hemifield and within-hemifield double-step performance in the normal animal (Baizer and Bender 1989;
Becker and Jurgens 1979; Dassonville et al. 1995; Goldberg et
al. 1990; Jeffries et al. 2003; Li and Andersen 2001; Zivotofsky
et al. 2003). We confirmed this using exactly the same paradigm used for the split-brain monkeys. In contrast to the
across-hemifield impairment in saccade accuracy in the splitbrain monkeys, we found no selective differences in the normal
animal (Fig. 5, A and B). This observation is consistent with
previous findings, and demonstrates that the impairments observed in the split-brain animals are indeed attributable to the
absence of the forebrain commissures.
MODERATE ACROSS-HEMIFIELD IMPAIRMENT OF SACCADE LATENCY
IN THE FIRST SESSION. We hypothesized that saccade initiation
FIG. 4. Percentage of correct and incorrect trials for double-step performance in the first session of testing, for upper (A, B) and lower field (C, D).
Each panel shows percentages from 6 sequences; icons along the x-axis. Color
coding as in Fig. 3. Solid bars represent the percentage of correct trials. Open
bars indicate incorrect trials in which the first saccade went to T1 but the
second saccade did not reach T2. Hatched bars indicate incorrect trials when
the monkey made the first saccade directly to T2 (monkey CH, acrosshemifield sequences only).
J Neurophysiol • VOL
would be slower for across-hemifield conditions for transfer of
visual information, given the absence of the most direct interhemispheric path. We anticipated that this slowing would be most
evident in the initiation of the second saccade of the double-step
task. We expected the latency of the first saccade, which was
visually guided, to be unaffected. We found, however, that
latencies of both the first and the second saccades were prolonged for the across-hemifield compared with the within and
central conditions (main effect of updating, all P ⬍ 0.0001).
The latency of both the first and second saccades depended
significantly on the interaction between updating condition, S1
direction, and vertical field (S1 latency: P ⬍ 0.0001 for
monkey EM, P ⬍ 0.05 for monkey CH; S2 latency: P ⬍
0.0001 for both monkeys; Fig. 5, C–F). As with the accuracy
data, we asked whether the latencies of individual acrosshemifield sequences were significantly increased relative to the
three matched central and within sequences. For each monkey,
latencies for the first saccade were significantly prolonged in
one of four quadrants (Fig. 5, C and D). Latencies for the
second saccade were significantly prolonged in three of four
quadrants (Fig. 5, E and F). In the normal monkey, by contrast,
first saccade latencies in the across-hemifield condition were
not prolonged in any quadrant. Second saccade latencies in the
across-hemifield condition were slowed significantly in one
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accuracy and latency to evaluate the monkeys’ performance in
the first testing sessions. We quantified accuracy of the second
saccade by measuring the distance between the endpoint of the
monkey’s saccade and the target. We found that distance error
was significantly increased for the across-hemifield condition,
in most but not all cases (Fig. 5, A and B). Analysis of variance
showed that, on average, the across-hemifield condition elicited greater error than the within-hemifield or central conditions (main effect of updating condition, both monkeys P ⬍
0.0001). The across-hemifield impairment varied by quadrant,
which was evident in a significant interaction among updating
condition, direction of the first saccade (S1), and vertical visual
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quadrant (lower right) and this trend was apparent in another
quadrant (upper left). This slowing is compatible with the
notion of longer transmission times for interhemispheric communication in the intact brain (Zaidel and Iacoboni 2003). The
slowed across-hemifield latencies are nonetheless more prominent in the split-brain monkeys, indicating that updating may
be less efficient in the absence of direct fibers linking the
cortical hemispheres. In summary, quantitative analysis
showed that performance in the split-brain monkey was significantly impaired when the double-step sequence required the
representation of T2 to be updated from one visual hemifield to
the other. The across-hemifield impairment was evident in
moderate increases in latency and in more prominent increases
in distance error.
PRECISION OF ACROSS-HEMIFIELD PERFORMANCE IN THE FIRST SESSION. What kinds of spatial representations did the split-brain
monkeys use to perform the across-hemifield sequences? This
question was particularly intriguing given the variability we
observed in across-hemifield performance, both between the
two animals and among quadrants in each individual animal.
One way to get a sense of the underlying spatial representations
is to assess the precision of saccade performance. In this last
analysis, we focused specifically on the question of how
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precisely the split-brain monkeys generated the second saccade
in across-hemifield sequences. Measures of precision capture
the consistency of the second saccade trajectory, regardless of
whether the saccade was directed toward the correct location.
For example, second saccades in the across-hemifield condition might be inaccurate but precise, suggesting that the monkey made use of a consistent (albeit wrong) representation of
T2. We measured precision on a trial-by-trial basis, taking
advantage of the slight variability in landing points of the first
saccade (Sommer and Wurtz 2004b). This approach tells us
how well the monkey adjusted the second saccade trajectory to
take the first saccade into account. In other words, if the
monkey has a precise representation of the second target
location, then the trajectory of the second saccade will vary
slightly according to the exact endpoint of the first saccade. For
each trial, we determined the direction of the ideal second
saccade, which the monkey would make if it were adjusting
precisely for the first saccade. We then compared this ideal
direction to the direction of the observed second saccade.
We were interested in two questions. First, when the
monkey was wrong, was it always wrong in the same way, i.e.,
directing the second saccade to the same inaccurate location?
Second, when the monkey was right, was it really updating the
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FIG. 5. Accuracy and latency of double-step performance in initial testing sessions for the split-brain monkeys (EM, CH) and normal monkey (FF).
In each panel, each set of 6 columns represents data (mean ⫾ SE) from one monkey (EM, CH, FF). Icons indicate the sequence; color coding as in previous
figures. A and B: distance error. C and D: latency for the first saccade (S1). E and F: latency for the second saccade (S2). Asterisks denote across-hemifield
sequences in which error or latency was significantly increased, compared with the matched central sequence and to both matched within-hemifield
sequences.
BEHAVIOR OF SPATIAL UPDATING IN THE SPLIT-BRAIN MONKEY
second target according to where the first saccade landed, or
was it inclined to use a more rote, automated strategy? We find
an answer to the first question by looking at the quadrants
where the accuracy impairment was most profound, for example, in the upper right quadrant for both monkeys (Fig. 6, B and
F). Both animals performed this across-hemifield sequence
inaccurately, but precisely: there is a highly significant relationship between the direction of the observed saccade and that
of the ideal saccade. This precision can also be appreciated in
Fig. 3D, which shows that the S2 endpoints are clustered
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closely together for these across-hemifield sequences. We
observed an exception to precision in the lower right quadrant
for monkey EM, where observed S2 direction was not significantly related to the ideal direction (Fig. 6D). This indicates a
more variable representation of T2. With regard to the second
question—what happens when the monkey is accurate—the
clearest example comes from the lower visual field of monkey
CH, where performance was relatively accurate from the start
on Day 2. Here, precision is relatively poor (Fig. 6, G and H).
The absence of a strong correlation between observed and ideal
directions may indicate that the monkey’s representation of T2
was changing over time and becoming more accurate. Alternatively, it may indicate that the monkey was performing these
across-hemifield sequences without genuinely updating the T2
representation to account for the first saccade. We later address
this second possibility more fully (expt 3). The basic points
here are that the monkeys were typically precise even when
they were inaccurate and that directional precision tended to be
worst when accuracy was best.
RULING OUT OTHER SOURCES OF ERROR. We considered the
possibility that the initial across-hemifield impairment in the
split-brain monkey resulted from inaccuracy of the first saccade. We minimized the variability in first saccade accuracy by
making that saccade visually guided. Furthermore, the accuracy and latency measures described above were computed
only from those trials where the monkey’s first saccade fell
within two degrees of T1. The ANOVA revealed main effects
of updating condition on the accuracy of S1 (P ⬍ 0.0001, both
monkeys), but the differences were exceedingly small. Average error was increased by no more than 0.17° for the acrosshemifield condition relative to the central and within conditions. This observation confirms that conditional differences in
the first saccade were slight and could not account for those
observed in the second saccade.
We also considered the possibility that the split-brain monkeys’ performance on the across-hemifield condition reflected
a sensorimotor or mnemonic impairment, rather than an impairment in spatial updating. We tested these possibilities by
having the monkeys perform single memory-guided saccades
(MGS) to the T2 locations used in the double-step task, either
directly from the central fixation point or directly from the first
target (T1) locations. These single-saccade tasks measure the
monkeys’ ability to encode and remember the T2 locations
relative to the initial position of the eyes and relative to the
position of the eyes at T1. We evaluated the accuracy and
latency of these single memory-guided saccades to determine
whether impairment in the double-step task reflected a deficit
in these sensorimotor or memory processes.
Neither split-brain monkey showed a selective impairment
for attaining the across-hemifield T2 location in the MGS task,
regardless of whether the eyes began at central fixation or at
T1. Their accurate performance is apparent in the eye traces
from the monkeys’ first ten trials of the MGS task (Fig. 7).
Analysis of variance revealed small but significant accuracy
and latency differences by updating condition. These conditional differences, however, were opposite to those observed in
the double-step task: overall error and latency values were
increased for the within compared with the across conditions
(Fig. 7). These differences likely reflect the tendency for
performance in the MGS task to decline for more peripheral
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FIG. 6. Precision of across-hemifield performance in the split-brain monkeys, for each visual quadrant. In each panel, the observed angle of the second
saccade (y-axis) is plotted against the ideal angle (x-axis) for individual trials.
Regression lines show the slope and r values give correlation coefficients.
Asterisks indicate that the strength of the relationship is significant: *P ⬍ 0.05,
**P ⬍ 0.01, and ***P ⬍ 0.001; ns, not significant.
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performance on the across-hemifield sequences improved with
experience for sequences that showed initial impairment. We
continued to test the monkeys on the standard sequences until
performance was stable, which ranged from seven sessions
(monkey CH, lower field) to 65 sessions (monkey EM). In this
section, we characterize the evolution of across-hemifield performance over multiple sessions.
targets (Barash et al. 1991; Bell et al. 2000; Gnadt et al. 1991;
Kalesnyka and Hallett 1994). We conclude that the acrosshemifield impairment in the double-step task cannot be attributed to a deficit in encoding, remembering, or generating eye
movements to the across-hemifield T2 locations.
Experiment 1: Changes in across-hemifield performance
over time
There were two exceptions to the initial impairment of the
across-hemifield sequences. First, monkey CH was effectively
unimpaired in the lower visual field. Second, we found that
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1. Number of trials to criterion for
across-hemifield sequences
TABLE
Monkey EM
Upper field
Lower field
Monkey CH
Left
Right
Left
Right
2471 (44)
2710 (49)
1667 (20)
1336 (15)
70 (1)
10 (1)
918 (27)
10 (1)
Number in parentheses indicates the session in which criterion was met. To
reach criterion, average distance error had to be ⬍3.5°, for three consecutive
groups of ten trials. For sequences that reached criterion during the first session
of testing (⬍200 trials), the listed number indicates the first of these three
groups. The listed number otherwise indicates the total number of trials
performed, up to and including the session in which criterion was met.
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FIG. 7. Accuracy measures show no across-hemifield impairment for single
memory-guided saccades (MGS) to T2 from fixation (FP; A) or from the first
target (T1; B). Conditions are arranged according to the corresponding doublestep conditions. Eye traces (between the upper and lower field panels) show
performance on the first 10 trials of testing the single MGS.
CHANGES IN ACCURACY. We found that performance in the
double-step task changed considerably over time. We first
obtained an estimate of the number of trials required to reach
criterion for correct performance in each across-hemifield sequence. As we saw in the initial testing session, improvement
in the across-hemifield sequences was heterogeneous, varying
by monkey and by quadrant (Table 1). We then plotted the
mean accuracy and latency of double-step performance in each
testing session (Figs. 8 –10). We focus on those quadrants
where across-hemifield accuracy was impaired beyond the first
testing session (monkey EM, all quadrants; monkey CH, upper
right quadrant). In these five quadrants, distance error was
greater for the across-hemifield sequences compared with the
central and within sequences (Fig. 8, A–D and F). After nearly
ten sessions, monkey EM’s performance on the across-hemifield sequences became even more inaccurate. At this stage, the
monkey often made erratic saccades into the periphery, rather
than attempting a second eye movement toward the target
location. This deterioration was especially notable in the lower
left quadrant (Fig. 8C). We found that the increased error
co-occurred with a decrease in precision on across-hemifield
sequences; the correspondence between ideal and observed
direction of the second saccade fell to nonsignificant levels.
This decline in accuracy and precision may indicate that the
animal was no longer making a reasonable effort to perform the
across-hemifield sequences. Alternatively, it could reflect a
strategic shift, whereby the monkey began to “sample” the
visual space in an effort to find sequences that were rewarded.
When improvement occurred for monkey EM, it did so in
rapid, discrete steps. This is evident in the first across-hemifield
sequence to improve (lower right quadrant; Fig. 8D). Between
sessions 14 and 15, distance error decreased suddenly from 13
to 2°. Rapid decreases in error also occurred in the other three
quadrants (Fig. 8, A–C). The onset of this improvement in
accuracy was different for the four quadrants, but was accompanied by increases in directional precision for the acrosshemifield condition (not shown). In other words, once the
monkey learned to perform the across-hemifield sequences,
performance appeared to be guided by an updated spatial
BEHAVIOR OF SPATIAL UPDATING IN THE SPLIT-BRAIN MONKEY
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FIG. 8. Accuracy for double-step performance over multiple sessions, for monkey EM (A–D) and monkey CH (E–H). Each panel shows average distance error
(y-axis) for the 3 conditions in each quadrant of the visual field, as performance evolved over testing sessions (x-axis). Testing continued until across-hemifield
performance was stable, which ranged from 7 sessions (monkey CH, lower field) to 65 (monkey EM). For monkey EM, small black arrows indicate the time
of events, described in the text, which influenced across-hemifield performance: A, consistent visual feedback; C, increase in size of electronic window; D,
beginning of expt 2.
representation. For monkey CH, accuracy of the across-hemifield condition improved or was unimpaired in three of four
quadrants during the first session of testing. In the remaining
quadrant, the accuracy of across-hemifield trials improved
slowly and discontinuously (Fig. 8F).
For
both monkeys, saccadic latencies changed over the course of
the testing sessions (Figs. 9 and 10). With few exceptions,
changes in saccade latency co-occurred with changes in accuracy. For example, when monkey EM exhibited more erratic
CHANGES IN LATENCY PARALLEL CHANGES IN ACCURACY.
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across-hemifield performance, this was evident in increased
error as well as increased latencies (lower left quadrant, C in
Figs. 8 –10). Likewise, when across-hemifield error decreased,
it did so in parallel with decreases in S1 latency (monkey CH
in Figs. 8F and 9F) and/or decreases in S2 latency (monkey
EM in Figs. 8D and 10D). We assessed the strength of these
relationships by conducting regression analyses on average
accuracy and latency for the across-hemifield sequences from
all testing sessions. We found a highly significant relationship
between distance error and both S1 latency and S2 latency, for
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FIG. 9.
Fig. 8.
Latency for the first saccade in double-step performance over multiple sessions, for monkey EM (A–D) and monkey CH (E–H). Conventions as in
all cases except the lower field sequences in monkey CH (all
significant at P ⬍ 0.001). This adds further support to the
central observation that improvement on the across-hemifield
sequences was marked by concomitant decreases in error and
latency.
FACTORS CONTRIBUTING TO IMPROVED PERFORMANCE. What
elicited the improvement in across-hemifield performance?
Two factors likely influenced performance: specific experimental manipulations and visual feedback. For monkey EM,
across-hemifield performance improved in most quadrants only
after expt 2 (below), in which the across-hemifield T2 location
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was placed closer to, and then directly onto, the vertical
midline. We began expt 2 in session 10, while we continued to
test the standard sequences from expt 1 in a separate block
during the same session. At this point, we observed an initial
increase in error on the standard sequences. Subsequently,
successful performance at the midline seemed to extend gradually to a recovery of across-hemifield performance on the
standard sequences.
Visual feedback was also likely important for improvement
on across-hemifield sequences. Whenever the monkey performed a trial correctly, the T2 target reappeared and the
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BEHAVIOR OF SPATIAL UPDATING IN THE SPLIT-BRAIN MONKEY
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FIG. 10.
in Fig. 8.
Latency for the second saccade in double-step performance over multiple sessions, for monkey EM (A–D) and monkey CH (E–H). Conventions as
monkey refixated its location. The presence of visual feedback
likely accounted for the discrete and rapid decreases in error.
Typically, the monkey spontaneously initiated a change in
behavior that allowed it to perform some trials correctly, but
there was one exception to this self-initiated improvement. In
the lower left quadrant, monkey EM was unable to perform the
across-hemifield sequences even after 40 sessions, and performance had actually deteriorated (Fig. 8C). The monkey’s
performance on this sequence was so erratic in several sessions
that no valid trials were available for analysis (breaks in line).
In session 45, we expanded the size of the electronic eye
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window at T2, to determine whether the across-hemifield
sequence could be learned under any circumstance. As a result,
the monkey received visual feedback even for very inaccurate
saccades. The monkey’s subsequent performance shows a
rapid improvement. Visual feedback therefore appears to be
sufficient to instigate accurate behavior. It is not, however,
strictly necessary. In the upper left quadrant, monkey EM did
not receive consistent visual feedback for the across-hemifield
sequence until session 49, but accuracy improved substantially
at session 15 (Fig. 8A). Accuracy improved still further after
session 49, when performance was consistently reinforced. In
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R. A. BERMAN, L. M. HEISER, R. C. SAUNDERS, AND C. L. COLBY
sum, visual feedback appears to play a central role in eliciting
accurate behavior on across-hemifield sequences.
ACROSS-HEMIFIELD
SIONS. Data from
PERFORMANCE
AFTER
MULTIPLE
SES-
the final testing sessions show appreciable
improvement in the performance of across-hemifield sequences
(Fig. 11). We were specifically interested in whether the
monkeys continued to be impaired on individual sequences of
the across-hemifield condition in this final testing session. We
used our standard post hoc procedure used in expt 1 to assess
whether each across-hemifield sequence was significantly impaired relative to the matched central and within sequences. In
initial testing, the across-hemifield accuracy was significantly
worse in six quadrants (all four in monkey EM, and two in
monkey CH; Fig. 5). In final testing, this impairment was
significant in only two quadrants (one in each monkey). Monkey EM continued to show increased across-hemifield errors in
the upper left quadrant, monkey CH in the upper right quadrant
(Fig. 11C). The magnitude of this impairment, however, is far
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FIG. 11. Performance of the split-brain monkeys on standard double-step sequences in final testing sessions. A and B: saccade endpoints for monkey EM (A)
and monkey CH (B); conventions as in Fig. 3. C–H: accuracy and latency of double-step performance; conventions as in Fig. 4.
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BEHAVIOR OF SPATIAL UPDATING IN THE SPLIT-BRAIN MONKEY
Experiment 2: Ipsilateral representation of space and
saccade reversal.
The initial impairment in across-hemifield performance
prompted us to investigate two issues, which we addressed
simultaneously in expt 2. Our main objective was to determine
whether ipsilateral representations were available for updating
in the split-brain animals. In investigating this issue, we were
also able to address and rule out an alternative explanation for
the across-hemifield impairment.
In our consideration of ipsilateral representations, we focused on the lateral intraparietal area (LIP). Area LIP is an
important site for the construction of updated spatial representations (Colby and Goldberg 1999; Duhamel et al. 1992b;
Heide et al. 1995; Quaia et al. 1998). Physiological studies of
area LIP in the normal monkey generally indicate a strong
contralateral bias in spatial representation. When ipsilateral
responses are found, they are rarely elicited by stimuli more
than a few degrees beyond the vertical meridian (Barash 1991;
Ben Hamed et al. 2001; but see Platt and Glimcher 1998). In
the standard paradigm we used in initial testing, we intentionally placed the across-hemifield T2 at a location that was
unlikely to be encompassed by receptive fields extending into
the ipsilateral field (six degrees from the midline). It was
nevertheless important for us to consider the possibility that
ipsilateral representations could contribute to performance in
the across-hemifield condition. If so, a single hemisphere
would have access to visual representations of the acrosshemifield T2 location, both before and after the first eye
movement.
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The initial impairment we observed on across-hemifield
sequences indicates that the split-brain monkeys could not
easily make use of ipsilateral representations to guide accurate
performance. This observation is compatible with several interpretations. It might simply confirm the idea that stimuli
located six degrees from the midline are not represented
bilaterally, in either the normal or the split-brain animal. Or,
these ipsilateral representations may be absent in the split-brain
animal. This possibility is consistent with evidence from ventral stream areas, where ipsilateral representations disappear
after transection of the forebrain commissures (Gross et al.
1977). We also considered, however, two alternative explanations. The first was that ipsilateral representations may be
present in the split-brain animal, but only for locations closer
than six degrees to the vertical meridian. The second was that
the across-hemifield deficit was not actually related to updating, but reflected a more general inability to perform sequences
that required a reversal in saccade direction (e.g., rightward S1,
leftward S2).
We tested these possibilities by measuring the monkeys’
performance on the double-step task in three different spatial
configurations. The first configuration was the standard acrosshemifield paradigm used in expt 1. We refer to this configuration as the six-degree paradigm to emphasize the eccentricity
of the across-hemifield T2. In the second configuration, the
across-hemifield T2 was located three degrees from the midline
(“three-degree” paradigm). In the third configuration, T2 was
located directly on the midline (“zero-degree” paradigm). This
last configuration does not require across-hemifield updating
because each cortical hemisphere contains a representation of
the vertical meridian. Even so, we use the term “acrosshemifield” to underscore the parametric comparison of the
three configurations. For each paradigm, we continued to test
all three updating conditions (central, within-hemifield, and
across-hemifield), and saccade amplitudes were equivalent for
each condition. For the three- and zero-degree paradigms, we
first trained the monkeys on the new central condition, which
differed from the original only in the location of T2 (Fig. 12A,
black lines). Then we simultaneously introduced the new
within and across conditions. We began by testing the threedegree paradigm and tested the zero-degree paradigm in the
following day’s session.
To determine whether performance improved when T2 was
placed nearer to the midline, it was critical that the monkeys
continued to show impairment in the standard six-degree paradigm. We found that performance on the standard acrosshemifield sequences remained impaired throughout this experiment (example data, Fig. 12A).
We first asked whether this across-hemifield impairment
could be mitigated by placing the second target closer to the
vertical midline. When T2 was located three degrees from the
midline, performance on the across-hemifield sequences did
not improve. On the contrary, performance worsened in all
quadrants. The deterioration in performance may reflect a
response to the unfamiliarity of this sequence, which exacerbated the existing across-hemifield impairment. This degraded
performance indicates that the monkey was unable to use
ipsilateral representations to perform the double-step task.
We next asked whether the monkeys could perform the
across-hemifield sequences if T2 were placed directly on the
midline. We expected the monkeys to perform these sequences
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less than that observed in the first session of testing (Fig. 5A,
same scale).
Finally, we investigated the monkeys’ saccade latencies for
the learned across-hemifield sequences. We considered the
possibility that accurate performance on the across-hemifield
sequence might require slow, deliberate eye movements. In the
final behavioral testing session, however, we found that latency
in the across-hemifield sequence was significantly slowed only
for the first saccade and only in one quadrant in monkey CH
(Fig. 11E, upper left quadrant). In all other cases, initiation of
the across-hemifield sequence was equivalent to, or even faster
than, the matched central and within sequences. These data
indicate that the monkeys did not have to perform the doublestep task more slowly to complete the across-hemifield sequences successfully.
In sum, we made five observations regarding the monkeys’
performance on the across-hemifield condition over time. 1)
Improvement in the across-hemifield condition took place over
a range of timescales, varying by monkey and by visual
quadrant. 2) When improvement began, errors on acrosshemifield sequences typically decreased in rapid steps. 3)
Saccade latencies changed abruptly as across-hemifield sequences were learned, often in parallel with changes in accuracy. 4) Visual feedback was sufficient, although not necessary, to elicit improved performance on across-hemifield sequences. 5) Both monkeys showed minimal impairment of
across-hemifield sequences in the final testing session, although significant inaccuracies persisted in one quadrant for
each monkey.
3241
3242
R. A. BERMAN, L. M. HEISER, R. C. SAUNDERS, AND C. L. COLBY
Experiment 3: Across-hemifield performance is under
sensory control
FIG. 12. Across-hemifield impairment persisted when T2 was located 3
degrees from the midline but was abolished when T2 was on the midline. A:
example endpoint data from the upper field, monkey EM; conventions as in
Fig. 3. B and C: average distance error, grouped by condition (within ⫽ green,
central ⫽ black, across ⫽ red). Bars show average error from all 4 quadrants
for each paradigm (6-, 3-, 0-degree).
without difficulty because each hemisphere would have access
to the updated representation of T2. If, however, the monkeys
were simply impaired in generating sequences that require a
reversal of saccade direction, performance would remain inaccurate. We found that performance on the midline sequences
was very accurate (Fig. 12A). These data indicate that the
initial across-hemifield impairment did not arise from a difficulty in reversing saccade directions.
We assessed the relationship between T2 location and
across-hemifield performance using a four-factor ANOVA
[updating condition, S1 direction, vertical visual field, and
J Neurophysiol • VOL
What kind of information do the monkeys use to perform the
across-hemifield sequences correctly? One possibility is that
the monkeys learned to apply a motor rule, such as “if the first
saccade is leftward and the second saccade is unknown, then
direct the second saccade up and to the right.” In this scenario,
the monkeys would not be using sensory information about the
actual target location. This possibility was consistent with our
precision analysis of initial across-hemifield performance. In
the precision analysis, we had observed the least precision for
the across-hemifield sequences that were performed most accurately, making it possible that successful performance (as
initially observed in monkey CH) was not genuinely based on
updating T2 in conjunction with the first saccade. We explicitly
tested this possibility in both monkeys when their performance
on the across-hemifield sequences had reached asymptote in at
least two quadrants. In this experiment, we introduced a small
shift of the T2 locations (Fig. 13A). The shift, or phi, varied
unpredictably from trial to trial and was small enough to allow
the monkeys to perform the trials correctly without taking
sensory information into account. In other words, the monkeys
would continue to receive reward if they executed the same
“learned ” saccade to the original T2, even on offset trials. If
the monkeys were using a motor rule, we expected that the
trajectory of S2 would not change systematically with the
location of T2. If, however, the monkeys used sensory information about the precise location of T2, even on acrosshemifield sequences, then the trajectory of S2 would vary
according to the position of T2.
Both monkeys generated the double-step sequences according to the actual location of the second target. This spatial
precision was observed not only for the within-hemifield condition, as expected, but also for the across-hemifield condition.
As seen in Fig. 13A, endpoints for the standard within-hemifield and across-hemifield conditions (green or red) are flanked
by endpoints for the phi conditions (pink and cyan). Likewise,
the average data from both monkeys demonstrate that the
second saccade endpoints varied according to T2 location (Fig.
13, B and C). We assessed the significance of this relationship
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paradigm (6°, 3°, or 0°)]. Of greatest interest was the significant interaction between updating condition and paradigm
(both monkeys, P ⬍ 0.0001). Post hoc analyses confirmed that
across-hemifield accuracy improved significantly for the midline configuration compared with the three- and six-degree
paradigms, for both monkeys (Fig. 12, B and C; P ⬍ 0.05,
Bonferroni correction). In contrast, the accuracy of within
sequences was either unchanged or decreased for the midline
compared with the three- and six-degree configurations. This
decline in within-hemifield performance likely occurred because the T2 locations were farther in the periphery (21° and 24°).
The data from expt 2 indicate that stimuli presented three
degrees from the midline cannot be updated across visual
hemifields in the absence of the forebrain commissures. Locations along the midline, however, are updated readily. The
monkeys’ ability to perform the midline sequence also rules
out the possibility that the across-hemifield impairment reflects
a simpler deficit in generating a second saccade in the opposite
direction opposite to that of the first saccade.
BEHAVIOR OF SPATIAL UPDATING IN THE SPLIT-BRAIN MONKEY
3243
Experiment 4: New spatial configurations disrupt
across-hemifield performance
FIG. 13. Spatial updating is under sensory control, even for the acrosshemifield condition. A: testing configuration and example data from Monkey
EM. For each standard within (green) and across (red) sequence, the T2
location was unpredictably displaced by 5 angular degrees either toward (cyan)
or away from (yellow) the vertical meridian. B and C: crosshairs show mean
endpoint (⫾SE) of the second saccade for each sequence, for each monkey;
color coding as in A. R2 values, shown either above or below each set of
sequences, indicate the strength of the relationship between the direction of the
monkey’s saccade and the ideal direction; all but one were significant at either
**P ⬍ 0.0001 or *P ⬍ 0.05.
by conducting a regression analysis, asking whether the angular trajectory of the ideal saccade was predicted by the angular
trajectory of the monkey’s saccade. Like the precision analysis
we conducted on the data from expt 1, this approach also tells
us how well the monkey took the first saccade into account on
a trial-by-trial basis. We conducted the regression separately
on the data from each standard sequence with its associated
shifted sequences. We found highly significant R2 values (P ⬍
J Neurophysiol • VOL
In expt 4 we asked whether the monkeys’ success on the
standard across-hemifield sequences would generalize to a
novel configuration of the double-step task. This possibility
was of particular interest given the variability we observed in
initial across-hemifield performance. We reasoned that the
monkeys might be least able to generalize in quadrants where
across-hemifield performance had improved most slowly. We
tested the monkeys’ ability to generalize by changing the
amplitude of both saccades and altering the angular displacement of the second saccade. In this new configuration, the
amplitudes of the first and second saccades were 8 and 15°,
respectively, and angular displacement was 45°; in the standard
sequences, saccade amplitudes were both 12°, with a displacement of 30°. Once again we simultaneously introduced the new
within- and across-hemifield sequences, after brief training to
criterion on the new central sequences. Data from the standard
configuration were obtained at the end of each session.
Both monkeys were able to perform all the new sequences,
although with more inaccuracy than that for the standard
sequences. Our specific interest was the interaction between
updating condition and novelty: did the new configuration
disrupt performance on the across-hemifield condition more
than the within-hemifield condition? We conducted a multivariate ANOVA with four factors (updating condition, S1
direction, vertical visual field, and novelty). We observed a
highly significant interaction between updating condition and
novelty (both monkeys, P ⬍ 0.0001), and indeed, the difference between old and new configurations was significant for
the across but not the within condition (P ⬍ 0.05, Tukey’s
HSD). On average, then, the monkeys were subject to reimpairment when introduced to novel spatial geometries.
We further asked whether there was evidence of generalization on the across-hemifield condition in any quadrant. When
we examined across-hemifield performance in each quadrant,
we found a variable pattern of results, not unlike the pattern
observed in initial behavioral testing. Monkey EM was consistently worse on new compared with old across-hemifield
sequences in all quadrants (Fig. 14A, all red triangles above
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0.0001) for all but two across-hemifield sequences, where
performance remained impaired: the lower left quadrant for
monkey EM (P ⬍ 0.05) and the upper right quadrant for
monkey CH (P ⫽ 0.06). We also observed significant displacement even for across-hemifield sequences that were not fully
learned (monkey EM, upper left quadrant). We conclude that
the monkeys were not ultimately using a motor rule or another
automated approach to perform the across-hemifield sequences, but were in fact basing their behavior on the sensory
location of T2 and updating this representation in conjunction
with the first saccade.
We have shown that the monkeys were able to learn the
across-hemifield sequences and execute them under sensory
control. We next considered that the performance on these
across-hemifield sequences might be particularly susceptible to
increases in task difficulty. The following two experiments
address this possibility by asking whether across-hemifield
performance is robust in response to novel target geometries
(expt 4) and increased mnemonic load (expt 5).
3244
R. A. BERMAN, L. M. HEISER, R. C. SAUNDERS, AND C. L. COLBY
Experiment 5: Across-hemifield updating is intact in a
delayed double-step task
FIG. 14. Introduction of new spatial geometries was more deleterious for
across-hemifield than for within-hemifield updating. Average error (A) and
latency (B, C) for the new configuration (y-axis) compared with the standard
configuration (x-axis). Each symbol represents average performance from one
quadrant, for either the across (red) or within (green) condition.
unity line). Monkey CH showed a selective impairment on the
new across-hemifield sequences in some quadrants but not all,
and in some cases distance error increased only slightly (Fig.
14A, red circles above unity line). This monkey’s ability to
generalize in some quadrants is consistent with our observations from initial testing: we found that Monkey CH was able
to learn the across-hemifield sequence in the upper left quadrant on Day 1, and subsequently performed the across-hemifield sequences well in the lower field on Day 2 of testing.
With respect to saccade latencies, we found that introduction
of the new configuration led to similar changes in first-saccade
J Neurophysiol • VOL
Performance in the double-step task depends on remapping
an evanescent trace of a briefly appearing stimulus. We were
interested in the possibility that the stimulus trace for the
across-hemifield condition might fade more quickly in the
absence of the forebrain commissures. Our interest in this
issue was motivated by the variable across-hemifield performance of Monkey CH in initial testing. We noted that the
monkey was most impaired on the across-hemifield condition in the upper right quadrant, where latencies of the first
saccade were also slowest (Fig. 5C). This led us to ask
whether the monkey’s success in the other quadrants depended
on being able to generate the first saccade rapidly, so as arrive
at T1 in time to access a rapidly vanishing memory trace of the
stimulus.
We reasoned that performance on the across-hemifield condition might deteriorate in all quadrants if the monkey had to
hold the T2 stimulus trace in mind during a delay period. We
tested this by introducing a delay (300 –500 ms) between the
time of T2 appearance and the monkey’s cue to initiate the
double-step sequence. This experiment was conducted in monkey CH at a time when its performance had recovered. We
used a training procedure similar to the original one that
preceded expt 1. The monkey first learned to perform a vertical
version of the delay task and was then trained on the central
condition of the horizontal version of the task. Finally, we
introduced the across-hemifield and within-hemifield sequences simultaneously, to determine whether the monkey’s
performance was affected by the imposed delay.
We found that performance of the across-hemifield sequences was not selectively impaired in the delay paradigm.
The scatterplots of saccade endpoints show that performance
was less accurate for all three conditions in the delayed
version, compared with the standard version of the double-step
task (Fig. 15A; compare with Fig. 11). Across-hemifield performance was not selectively worse, however, relative to performance on the central or within conditions, except in one
quadrant (upper right; Fig. 15B). The monkey had shown
persistent impairment for this sequence in the standard version
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latencies for the within-hemifield and across-hemifield conditions. Monkey EM initiated the new sequences more slowly
(Fig. 14B, triangles above the line), whereas monkey CH
initiated them more quickly (Fig. 14B, circles below the line).
Neither monkey exhibited a specific first-saccade slowing on
the new across-hemifield condition. For the second saccade,
the effect of novelty differed for the two animals. Monkey EM
was uniformly slower to initiate the second saccade, both for
within and for across sequences (Fig. 14C, triangles above the
line). Monkey CH, however, showed a selective slowing on the
across-hemifield condition when the new configuration was
introduced (Fig. 14C, more red than green circles above the
line). These accuracy and latency data indicate that, overall,
generalization to new sequences is less robust for the acrosshemifield condition. The data from each monkey on performance of the new sequences parallel across-hemifield performance in initial testing sessions. Specifically, they indicate that
monkey CH was more adept at generalizing to new acrosshemifield sequences than was monkey EM.
BEHAVIOR OF SPATIAL UPDATING IN THE SPLIT-BRAIN MONKEY
3245
SUMMARY
These experiments provide five main findings regarding
spatial updating in the split-brain monkey. First, our standard
paradigm revealed an initial impairment and ultimate improvement of performance on double-step sequences that required
across-hemifield updating. Second, we found that the initial
impairment was not mitigated by placing the across-hemifield
target nearer to the midline. Third, once performance on
across-hemifield sequences began to improve, the monkeys
were able to generate the sequences under sensory control,
taking into account small shifts in target position. Fourth,
recovery of the across-hemifield sequences did not generalize
readily to new spatial configurations; rather, the monkeys
required experience with specific across-hemifield sequences
for performance to improve. Finally, an increase in working
memory load did not selectively disrupt double-step sequences
that required across-hemifield updating.
FIG. 15. Performance of the across-hemifield condition was not significantly impaired in the delayed double-step task. A: endpoints of the second
saccade; conventions as in Fig. 3. B–E: measures of accuracy and latency;
conventions as in Fig. 4.
of the double-step task. Therefore the increased error in the
delay task cannot be attributed to the additional mnemonic
requirements of this paradigm. Latencies for both the first
and second saccades were also not significantly prolonged
for the across-hemifield sequences (Fig. 15, D and E; shown
for S2 only). We conclude that the remembered T2 representation is robust for the across-hemifield sequences and
that the circuitry supporting across-hemifield updating in the
split-brain monkey is not disrupted by increased working
memory demands.
J Neurophysiol • VOL
The construction of a continuously accurate spatial map
requires that visual representations be updated in conjunction
with saccades. The neural circuits by which this updating is
accomplished remain unknown. In the present study, we investigated the mechanisms for updating a representation from
one visual field to the other. Specifically, we asked whether
performance of the double-step task was impaired in the
split-brain monkey when updating required the transfer of
visual signals from one hemisphere to the other. Two central
findings emerge from these behavioral experiments.
The first is that spatial updating typically relies on communication by direct cortico-cortical links. In a series of experiments, we showed that across-hemifield updating is compromised in the absence of the forebrain commissures. The splitbrain monkeys were initially impaired on double-step
sequences that required updating of the second target representation from one visual hemifield to the other (expt 1). This
impairment was most evident in increased distance error and,
to a lesser extent, in increased saccade latencies for the acrosshemifield sequences. The task design allowed us to attribute
these deficits to a disruption of spatial updating and not to
confusion caused by unfamiliar sequences: the across-hemifield sequences were selectively impaired relative to equally
unfamiliar within-hemifield sequences. We also ruled out three
alternatives for the initial impairment in split-brain monkeys. It
cannot be attributed to: 1) inaccuracy of the first saccade; 2)
basic sensory, memory, or eye movement deficits; or 3) a
deficit in generating sequences that require a reversal in saccade direction. Further, we found that the impairment persisted
even when the target of the second saccade was placed very
near to the midline (expt 2). This indicates that ipsilateral
visual representations were unable to support updating. This
finding is compatible with physiological studies, which demonstrate that ipsilateral visual representations in the ventral
stream depend on the corpus callosum and anterior commissure
(Gross et al. 1977). Finally, we found that in some cases, the
across-hemifield impairment was reinstated when we introduced new sets of targets (expt 4). This indicates that alternate
interhemispheric routes may be used on an as-needed basis
between restricted portions of the visual field. These results are
consistent with reports of experience-dependent plasticity and
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DISCUSSION
3246
R. A. BERMAN, L. M. HEISER, R. C. SAUNDERS, AND C. L. COLBY
Role of the forebrain commissures in visuospatial behavior
Our findings build on previous investigations of visual
processing in split-brain individuals. Earlier neuropsychological and physiological studies have shown that, in the absence
of the forebrain commissures, interhemispheric transfer is
clearly disrupted for color and form information, including
visual associative memory (Corballis 1995; Eacott and Gaffan
1989; Hasegawa et al. 1998; Land et al. 1983; Tomita et al.
1999; Trevarthen 1990). What has been less clear is the extent
to which spatial representations can be transferred interhemispherically when both the corpus callosum and anterior commissure are severed. Studies of human split-brain patients have
shown that spatial information can be transferred in the absence of the corpus callosum, but with limited resolution and
for limited purposes. These patients are capable of comparing
locations of stimuli presented in opposite hemifields, but only
at a coarse spatial resolution (Holtzman 1984). Further, a
stimulus presented in one visual hemifield may be able to guide
attention in the opposite hemifield (Holtzman et al. 1981; but
see Hines et al. 2002; Reuter-Lorenz and Fendrich 1990), yet
this stimulus cannot be used for explicit identification of
locations in the opposite hemifield (Holtzman et al. 1981).
J Neurophysiol • VOL
These findings suggest that subcortical– cortical interactions
can subserve interhemispheric transfer of limited spatial information, although it is also important to note that the preserved
functions in these split-brain patients may be mediated either
subcortically or by the intact anterior commissures. Our results
provide new evidence that the representations of stimulus
traces can be transferred between hemispheres in the absence
of all direct cortico-cortical links, and that these updated
representations can be used to guide subsequent eye movements with fine spatial resolution.
Pathways for spatial updating
Our results demonstrate that spatial updating is a robust
phenomenon, supported by a redundant circuitry that includes
not only cortical but also subcortical structures. The present
study has focused on the substrate for transferring visual
representations in conjunction with saccades and complements
recent research that delineates a subcortical– cortical pathway
for communicating a corollary discharge signal. Corollary
discharge—a copy of the command to move the eyes—must be
used to initiate the updating of stimulus representations in
visual areas (Goldberg et al. 1990). Recent physiological and
inactivation studies indicate that corollary discharge information is conveyed from superior colliculus to the frontal eye field
by the mediodorsal thalamus (Sommer and Wurtz 2004a,b).
Inactivation of this pathway disrupts the communication of
information about the impending saccade, causing a deficit in
performance on the double-step task (Sommer and Wurtz
2004b). These investigators found a significant yet partial
deficit, indicating that alternate pathways and/or mechanisms
may also contribute to the ability to monitor ongoing eye
movements. The anatomical basis of corollary discharge signals is a subject of current interest (Bellebaum et al. 2005;
Guillery 2003; Sommer and Wurtz 2002, 2003, 2004a,b; White
et al. 2004). These signals may arise from many brain structures, both cortical and subcortical. A full understanding of the
circuitry for spatial updating will need to account for the
pathways by which this motor information modifies visual
representations, particularly those in higher-order areas such as
parietal cortex.
Role of parietal cortex in spatial updating
Parietal cortex plays a central role in spatial updating (Colby
and Goldberg 1999; Duhamel et al. 1992a; Gottlieb et al. 1998;
Medendorp et al. 2003; Merriam et al. 2003; Pierrot-Deseilligny et al. 2004; Pisella and Mattingley 2004; Quaia et al.
1998; Van Donkelaar and Muri 2002). Neuropsychological
studies have shown that accurate performance of the doublestep task depends on parietal but not frontal cortex (Duhamel
et al. 1992b; Heide et al. 1995). Patients with parietal damage
can accurately generate double-step sequences when both saccades are visually guided, but are impaired when the second
saccade is memory guided and requires spatial updating of the
second target location. The importance of parietal cortex in
performance of the double-step task has also been demonstrated in monkeys. Inactivation of area LIP impairs performance on the double-step task, as evidenced by decreased
accuracy and increased latencies for the second eye movement
(Li and Andersen 2001). These findings provide converging
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recovery in both the auditory and visual systems (Huxlin and
Pasternak 2004; Karni and Sagi 1991; Recanzone et al. 1993;
Rudolph and Pasternak 1999). Taken together, our behavioral
findings clearly demonstrate that across-hemifield updating is
compromised in the absence of direct cortico-cortical pathways.
The second main finding is that direct cortico-cortical links
are ultimately not required for accurate spatial updating. In the
absence of the forebrain commissures, the impairment of
across-hemifield performance was not universal or permanent.
One of the split-brain monkeys exhibited rapid improvement
on one of the across-hemifield sequences during the first day of
testing in the upper visual field. On the subsequent day, we
found that this same monkey was effectively unimpaired in the
lower visual field. This may reflect a successful generalization.
Both monkeys were ultimately able to perform the acrosshemifield double-step sequences even in quadrants where impairment was initially profound. We found that improvement
of the individual across-hemifield sequences occurred over
different time courses. There is no obvious explanation for
these differences, which we observed both between monkeys
and among quadrants within each individual monkey. The
differences may reflect several factors, including the ability to
generalize to new across-hemifield sequences, complex variations in strategy, and biases in the representation of visual
space (Ellison and Walsh 2000; Maunsell and Van Essen 1987;
Previc 1990). The critical result is that both monkeys were
ultimately successful in performing double-step sequences that
required updating of the second target representation from one
hemifield to the other. Two further experiments showed that
this successful across-hemifield performance was precise and
robust in the split-brain monkey. We found that across-hemifield updating was under sensory control (expt 3) and was
unaffected by increased working memory demands (expt 5).
These important and unexpected findings demonstrate that
spatial representations can be updated across visual hemifields
in the absence of the forebrain commissures.
BEHAVIOR OF SPATIAL UPDATING IN THE SPLIT-BRAIN MONKEY
ACKNOWLEDGMENTS
We thank K. McCracken and Dr. Kevin Hitchens for technical assistance,
and our colleagues at the Center for the Neural Basis of Cognition for
constructive comments.
Present addresses: R. Berman, Laboratory of Sensorimotor Research, National Eye Institute, National Institutes of Health, Bethesda, MD 20892; L.
Heiser, Life Sciences Division, Lawrence Berkeley National Lab, Berkeley,
CA 94720.
GRANTS
This work was supported by National Institutes of Health Grant EY-12032,
technical support was provided by core grant EY-08908, and collection of MR
images was supported by P41RR-03631. Support was also provided by
National Science Foundation Fellowship to R. A. Berman, and National
Aeronautics and Space Administration Fellowship to L. M. Heiser.
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evidence for the proposal that parietal cortex is the site where
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one hemisphere can still be accurately updated to the opposite
hemisphere. This raises the possibility that parietal cortex is no
longer engaged in across-hemifield updating; the transformations may be accomplished entirely by subcortical pathways. In
the accompanying paper, we describe physiological experiments that test whether LIP neurons participate in acrosshemifield updating in the split-brain monkey.
These investigations shed new light on the circuitry that
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Like visual representations themselves, the pathways that support spatial updating are not static but dynamic. Direct cortical
links are not the only substrate for producing updated spatial
representations. Instead, updating is subserved by a flexible
network of cortical and subcortical structures, in which motor
signals act on visual information to create a stable representation of the world around us.
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