Optic Nerve Signals in a Neuromorphic Chip I: , Member, IEEE,

Optic Nerve Signals in a Neuromorphic Chip I: , Member, IEEE,
Optic Nerve Signals in a Neuromorphic Chip I:
Outer and Inner Retina Models
Kareem A. Zaghloul, Member, IEEE, and Kwabena Boahen*
Abstract—We present a novel model for the mammalian retina
and analyze its behavior. Our outer retina model performs bandpass spatiotemporal filtering. It is comprised of two reciprocally
connected resistive grids that model the cone and horizontal cell
syncytia. We show analytically that its sensitivity is proportional
to the space-constant-ratio of the two grids while its half-max response is set by the local average intensity. Thus, this outer retina
model realizes luminance adaptation. Our inner retina model performs high-pass temporal filtering. It features slow negative feedback whose strength is modulated by a locally computed measure
of temporal contrast, modeling two kinds of amacrine cells, one
narrow-field, the other wide-field. We show analytically that, when
the input is spectrally pure, the corner-frequency tracks the input
frequency. But when the input is broadband, the corner frequency
is proportional to contrast. Thus, this inner retina model realizes
temporal frequency adaptation as well as contrast gain control. We
present CMOS circuit designs for our retina model in this paper as
well. Experimental measurements from the fabricated chip, and
validation of our analytical results, are presented in the companion
paper [Zaghloul and Boahen (2004)].
Index Terms—Adaptive circuits, neural systems, neuromorphic
engineering, prosthetics, vision.
HE RETINA, one of the best studied neural systems, is
a complex piece of biological wetware designed to signal
the onset or offset of visual stimuli in a sustained or transient
fashion [25]. To encode these signals into spike patterns for
transmission to higher processing centers, the retina has evolved
intricate neuronal circuits that capture information contained
within natural scenes efficiently [27]. This visual preprocessing,
realized by the retina, occurs in two stages, the outer retina and
the inner retina. Each local retinal microcircuit plays a specific
role in the retina’s function, and neurophysiologists have extracted a wealth of data characterizing how its constituent cell
types contribute to visual processing. These physiological functions can be replicated in artificial systems by emulating their
underlying synaptic interactions. In this paper, we present a
novel model for how the outer and inner retina process visual
Manuscript received September 6, 2002; revised June 25, 2003 This work
was supported in part by the National Institutes of Health (NIH) under Vision
Training Grant T32-EY07035 and in part by the Whitaker Foundation under
Grant 37005-00-00. The work of K. A. Zaghloul was completed while he was
with the Department of Neuroscience, University of Pennsylvania, Philadelphia,
PA 19104 USA. Asterisk indicates corresponding author.
K. A. Zaghloul is with the Department of Neurosurgery, University of Pennsylvania, Philadelphia, PA 19104 USA (e-mail: [email protected]).
*K. Boahen is with the Department of Bioengineering, 120 Hayden Hall,
3320 Smith Walk, University of Pennsylvania, Philadelphia, PA 19104 USA
(e-mail: [email protected]).
Digital Object Identifier 10.1109/TBME.2003.821039
information, implement this model in silicon, and analyze its
behavior. In the accompanying paper [30], we characterize how
our silicon chip processes visual information and validate our
analytical results.
Attempts have been made to duplicate neural function at high
levels of abstraction because detailed knowledge of neural circuits was unavailable, but these neuro-inspired systems proved
ill-suited to direct hardware implementation because of the
mathematical operations they require. Neuromorphic systems,
on the other hand, which are constructed from neuron-like
elements based on physiology, connected together into local
microcircuits based on anatomy, can now duplicate certain
brain computations in silicon [9], [19].
The advantage these neuromorphic chips offer over software models is their ability to replicate neural computations
in real-time at low power. This implementation efficiency
translates to a greater ability to explore model parameters to
further understand the underlying biological system and, by
communicating with other neuromorphic chips, a greater ability
to replicate more complicated neural systems. Furthermore,
with the continued miniaturization of silicon technology and
with a greater understanding of neural computations, attention
has recently been shifted to developing prosthetic devices
capable of restoring neural function [6], [32]. While these
efforts have been relatively successful in the cochlea, fully
implantable solutions remain elusive [21]. Neuroprostheses,
such as an intraocular retinal implant, may benefit from a fully
integrated approach made possible by the greater autonomy
and functionality of neuromorphic systems.
The most recent effort to model retinal processing in silicon
incorporated outer retina circuitry as well as bipolar cell (BC)
and amacrine cell interactions in the inner retina [3]. This outer
retina circuit took the difference between the photoreceptor
signal and its spatiotemporal average, computed by a network
of coupled lateral elements [horizontal cells (HCs)], through
negative (inhibitory) feedback. Cone-coupling in this model
attenuated high-frequency noise to realize a spatial bandpass
filter and dynamic range was extended by implementing local
automatic gain control. Furthermore, this model used HC
activity to boost cone to HC excitation [3], which eliminated
receptive-field expansion and temporal instability. This gain
boosting mechanism has some physiological basis since glutamate release from cones is modulated by HC hemichannels
[13], and may be enhanced further by HC autofeedback [14].
Our outer retina design is based on this approach [3].
The BC and amacrine cell interactions introduced by this
earlier design represented a model for inner retina processing
that, much like the circuit discussed here, attempted to capture
0018-9294/04$20.00 © 2004 IEEE
Cone Outer
Spatial Frequency
Fig. 1. Outer retina model. (a) Neural circuit: CTs receive a signal that is proportional to incident light intensity from the cone outer segment (CO) and excite
HCs). HCs spread their input laterally through gap junctions, provide shunting inhibition onto CT, and modulate cone coupling and cone excitation. (b) System
diagram: Signals travel from CO to CT and on to HC, which provides negative feedback. Excitation of HC by CT is modulated by HC, which also modulates the
attenuation from CO to CT. These interactions realize local automatic gain control in CT and keep receptive field size invariant. Both CT and HC form networks,
connected through gap junctions, that are governed by their respective space constants, l and l . (c) Frequency responses: Both HC and CT low-pass filter input
signals, but because of HCs larger space constant, l , HC inhibition eliminates low-frequency signals, yielding a spatially bandpass response in CT.
temporal adaptation through adjustment of amacrine cell feedback inhibition. However, this earlier design did not include the
retina’s complementary push-pull architecture [25]. Hence, at
low-frequency stimulation, dc current levels tended to rise and,
thus, modulation of the feedback loop gain was not realized as
intended [3]. Furthermore, this previous implementation did not
replicate synaptic interactions at the ganglion cell (GC) level
and, thus, did not faithfully capture the behavior of the retina’s
major output pathways [3].
In this paper, we present a novel model for processing in the
mammalian retina that addresses the design flaws in [3] and extends that model to include GC level synaptic interactions. Our
model is based on the functional architecture of the mammalian
retina, and on physiological studies that have characterized the
computations performed by the retina. Additionally, we build
upon these earlier studies to present new circuit components that
may account for some of the computations found in the retina.
While the ultimate goal of our modeling effort is to match the
mammalian retina, a detailed comparison between our model’s
outputs and the retina’s outputs will be presented in a forthcoming paper.
The present paper presents a detailed analysis of our mathematical model and describes its silicon implementation. The
remainder of this paper is organized as follows. In Section II,
we present our outer retina ciruit model, briefly revisiting a circuit design described earlier [3], and our model of BC circuitry
that divides signals into ON and OFF channels. In Section III,
we introduce a novel model for the inner retina that adjusts its
loop gain, allowing it to adapt to different input power spectra.
Finally, in Section IV, we discuss some of the assumptions underlying our analysis and justifications for our model. Section V
concludes the paper. An accompanying paper presents experimental results that characterize our model’s behavior.
Our model for the outer retina’s synaptic interactions, which
realize spatiotemporal bandpass filtering and local gain control, was described previously [3]. The synaptic interactions underlying our model are repeated in the Fig. 1(a) for reference.
Briefly, photons incident on the cone (CO) reduce current flow
to its cone terminal (CT), causing a hyperpolarization and a decrease in neurotransmitter release. CTs excite HCs which apply
shunting (or attenuating) inhibition on to CT [25]. This reciprocal interaction between cones and HCs, and electrical coupling of both cell types to their neighbors through gap junctions
[25], creates a spatiotemporally bandpassed signal at CT that
adapts to light intensity [26].
From the synaptic interactions, we derived the block diagram
shown in Fig. 1(b) by modeling both the cone and HC networks
as spatial low-pass filters. We can derive the system level equations that describe how CO determines HC and CT activity, repand
respectively, from this block diagram.
resented by
These equations, reproduced from [3], are
where and are the cone- and horizontal-network space-conis the attenuation from CO to CT, and
stants, respectively,
is the amplification from CT to HC. HCs have stronger coupling in our model (i.e., is larger than ), causing their spatial
low-pass filter to attenuate lower spatial frequencies. Thus, HC
low-pass filters the signal while CT bandpass filters it, as shown
in Fig. 1(c), with the same corner frequency. We can determine
this peak spatial frequency, , by taking the derivative of CT’s
system equation and equating it to zero. We find
To realize local automatic gain control in our model, we set
HC activity proportional to intensity and use this activity to
modulate CO to CT attenuation, , by changing cone-to-cone
conductance. This modulation adapts cone sensitivity to different light intensities [5]. Furthermore, to overcome the expansion in receptive-field size that this modulation caused in earlier
designs, we complemented HC modulation of cone gap-junctions with HC modulation of cone leakage conductance, through
shunting inhibition, making independent of luminance. We
also compensated for the change in loop-gain with HC modulation of cone excitation, by keeping proportional to , thus
fixing .
We can determine how the CT activity produced by an edge
depends on these parameters by assuming that the dominant
contribution is from the peak and, hence, we insert the value
into CT’s system equation
where we have set
, assuming a proportionality constant
represents the frequency component
of unity for simplicity.
at . Hence, CT activity will be proportional to contrast
if , which is determined by HC activity, is proportional to local
intensity. We can determine the local HC activity and, hence, ,
) and the
by summing responses to the dc component (i.e.,
peak spatial frequency (i.e.,
is the intensity level at which the CT attenuation, ,
is unity, and where
represents the local average of input
as before. Therefore
From (4), we see that CT activity is primarily determined by
, saturates when increasing signal flucspatial contrast,
tuation causes this ratio to become large, and is entirely independent of absolute luminance. In the case when signal fluctuaincreases the level of
tion, , is large, increasing the ratio
, and have negcone saturation. In the limit where
ligible effect on the system’s peak sensitivity at low contrasts
CT activity governed by (4) in our model exhibits behavior
remarkably similar to the mammalian retina. Physiologists have
found that cone responses as a function of intensity of light stimulation against a background, or contrast, are described by a
simple equation
where is the peak amplitude of the cone response produced
by a given level of stimulating light intensity, .
is the maximum response and is the background intensity. The responses
[20]. This adaptive
reaches half of the maximum when
behavior is preserved across five decades of background intensities. In our model, cone responses take on the same S-shaped
response with contrast when
The complete outer retina CMOS circuit that implements
local gain control and spatiotemporal bandpass filtering, while
using HC modulation to maintain invariant spatial filtering and
temporal stability, is shown in Fig. 2(a) (adapted from [3]) for
, increasing
two adjacent nodes. Photocurrents discharge
CT activity, and excite the HC network through an nMOS
transistor followed by a pMOS current mirror. HC activity,
represented by , modulates this CT excitation and inhibits
CT activity—by dumping this same current on to . Cone
signals, , are electrically coupled to the six nearest neighbors
Fig. 2. Outer retina circuit. (a) Circuit: A phototransistor draws current
through an nMOS transistor whose source is tied to V and whose gate is tied
to V . This transistor passes a current proportional to the product of CT and
HC activity, thus modeling HC shunting inhibition. In addition, this current,
mirrored through pMOS transistors, dumps charge on the HC node, V ,
modeling CT excitation of HC, and HC autofeedback. V sets the mean level
of V , governing CT activity. (b) CT coupling is modulated by HC activity. A
HC node [V in (a)] gates three of the six transistors coupling its CT node [V
in (a)] to its nearest neighbors.
through nMOS transistors whose gates are controlled locally
[Fig. 2(b)]. These cone signals gate transistors that feed
currents into the BC circuit, such that increases in , which
to, increase the BC activity. HC
tracks the level we set
signals also communicate with one another, through pMOS
transistors, but this coupling is modulated globally by
since interplexiform cells that adjust HC coupling are not
present in our chip [15].
We rectify the cone signal using the circuit shown in Fig. 3
(described in [29]) to model complementary signaling by BCs.
Briefly, CT activity is represented by a current, , that is inversely related to (from our description above). And we compare to a reference current, , that is in turn inversely related
.1 Therefore, we define two new currents,
to a reference bias,
, to simplify our description of the
bipolar circuit. Mirroring these currents on to one another pre, which equals
serves their differential signal,
in our circuit sets quiescent current levels—decreasing
causes more current to flow through both channels—making
equal to the
rectification in our circuit incomplete. We set
mean value of such that the difference is positive when light
is brighter ( decreases) and negative when light is dimmer (
increases). We can see that as cone activity increases ( falls,
translating to a rise in , and a corresponding fall in ), current
is diverted through the ON channel, but this current level quickly
saturates. On the other hand, as cone activity decreases ( rises,
translating to a fall in , and a corresponding rise in ), current
flows through the OFF channel and increases as the reciprocal
of cone activity [29]. Thus, our bipolar circuitry divides signals
into ON and OFF channels, as expected, but the division is not
symmetric because one side of our circuit is fixed to the refer.
ence bias,
Our model of inner retina neurocircuitry, which realizes
low-pass and high-pass temporal filtering, adapts temporal
1In practice, we cannot simply tie V
to V because mean CT activity, V ,
is slightly higher than V , due to drain-voltage mismatch between nMOS and
pMOS transistor-pairs in the outer retina circuit.
Fig. 3. BC circuit. (a) CT activity, V , drives a current, I , that is compared to a reference current, I , driven by a reference bias, V . By mirroring these currents
on to one another, the difference between them is encoded by either I
or I
. V determines the level of residual dc signal present in I
and I
. (b)
and I
(top). When V
V (i.e., I
I ), residual dc currents are propotional
The difference between I and I determines differential signalling in I
to e
. Directly plotting the difference between cone activity, I , and I yields the curves on bottom. Increases in cone activity cause ON currents to saturate
while decreases in cone activity cause OFF currents to increase reciprocally.
receives full-wave rectified input from ON and OFF BT and NA
and, thus, rises above its baseline value of unity at both onset
and offset. BT drives the sustained GC, GCs, which responds
for the duration of the step, while the difference between BT
and NA activity drives the transient GC, GCt, which decays to
From the block diagram in Fig. 5(a), we can derive the system
level equations for NA and BT with the help of the Laplace
Fig. 4. Inner retina synaptic interactions. ON and OFF BCs relay cone signals
to GCs, and excite NAs and WAs. NAs inhibit BCs, WAs, and transient GCs;
their inhibition onto WAs is shunting. WAs modulate NA presynaptic inhibition
and spread their signals laterally through gap junctions. BCs also excite local
interneurons that inhibit complementary BCs and NAs.
dynamics to input frequency and to contrast, and drives GC
responses, is shown in Fig. 4. Briefly, BC inputs to the inner
retina excite GCs, an electrically coupled network of wide-field
amacrine cells (WAs), and narrow-field amacrine cells (NAs)
that provide feedback inhibition on to the bipolar terminals
(BTs) [16]. WA, which receives excitation from both ON and
OFF BT and inhibition from both ON and OFF NA, modulates
presynaptic feedback inhibition from NA to BT. We use a large
membrane capacitance to model the NA’s slow, sustained,
response, which leads to a less sustained response at the BT
through presynaptic inhibition [18]. Push-pull inhibition is
realized by a third set of amacrine cells in our model and is
implemented by the ON-OFF BC circuit. These BT signals
excite both sustained and transient GCs, but transient cells
receive feedforward inhibition from NAs as well [25].
Our model of the inner retina is described by the system diagram in Fig. 5(a). We derived this diagram from the synaptic
interactions of Fig. 4 by modeling the NA as a low-pass filter.
Responses of the different inner retina cell types in this model
to a step input are shown in Fig. 5(b). BC activity is a low-pass
filtered version of light input to the outer retina. Increase in BC
causes an increase in BT and a much slower increase in NA. The
difference between BT activity and gain-modulated NA activity
determines WA activity, which in turn sets the gain of NA feedback inhibition on to BT and WA. Thus, after a unit step input,
BT activity initially rises but NA inhibition, setting in later, attenuates this rise until BT activity is equaled by gain-modulated
NA activity. WA represents our local measure of contrast and
is the gain of the excitation from BT to NA and where
is the time constant of NA and represents WA activity, which determines feedback strength. From (5) and (6),
we can see that BT high-pass filters and NA low-pass filters
. This
the BC signal; they have the same corner frequency,
closed-loop time-constant, , depends on the loop gain
therefore, on WA activity. For example, stimulating the inner
retina with a high frequency would provide more BT excitation
(high-pass response) than NA inhibition (low-pass response) to
WA. WA activity and, hence, , would subsequently rise, reducing the closed-loop time-constant , until the corner frereaches a point where BT excitation equaled NA
inhibition. This drop in , accompanied by a similar drop in ,
will also reduce overall sensitivity and advance the phase of the
The system behavior governed by (5) and (6) is remarkably
similar to the contrast gain control model proposed by Victor
[28], which accounts for response compression in amplitude and
in time with increasing contrast. Victor proposed a model for
, is
the inner retina whose high-pass filter’s time-constant,
determined by a “neural measure of contrast,” . The governing
equation is
This model’s time-constant depends on contrast in much the
same way that our model’s time constant depends on WA acis similar to our
and where
tivity (6), where Victor’s
is represented by how much WA activity
Victor’s ratio
Fig. 5. Inner retina model. (a) System diagram: NA signals represent a low-pass filtered version of BT signals and provide negative feedback on to the BC. The
WA network modulates the gain of NA feedback (X). WA receives full-wave rectified excitation from BT and full-wave rectified inhibition from modulated NA
(double arrows). BT drives sustained GCs directly while the difference between BT and NA drives transient ganglion cells (GCt’s). (b) Numerical solution to inner
retina model with a unit step input of 1 V. Traces show 1 s of ON cell responses for BC, BT, NA, GCt, and WA. Outer retina time constant, , is 96 ms; is 1 s.
increases above its value at dc in our model. As this activity is
sensitive to temporal contrast (see below), we propose that our
WA cells are the anatomical substrate that computes Victor’s
neural measure of contrast.
is set by the local temporal
In our model, the loop gain
contrast. Because WA cells are coupled together through gap
junctions, WA activity reflects inputs from BT and NA weighted
across spatial locations. These pooled excitatory and inhibitory
inputs should balance when the system is properly adapted
where we define
as the gap-junction current resulting from
spatial differences in WA activity .
, computed by sumfull-wave rectified versions of
ming ON and OFF signals. If all different phases are pooled spatially, these full-wave rectified signals will not fluctuate and will
be proportional to amplitude. And if we ignore
, yielding a temporal measure of contrast,
simply be
since it is the ratio of a temporal difference (high-pass signal,
) and a temporal average (low-pass signal, ). From (5), we
; hence, the loop gain is
see that at dc, this ratio is equal to
unity and the dc gain
GC responses in our inner retina model are derived from the
BT and NA signals of (5). Specifically, BT signals directly excite both sustained and transient types of GCs, but transient cells
receive feedforward NA inhibition as well. The system equations determining GCs’s and GCt’s responses, derived from (5),
as a function of the input to the inner retina, , are
When BT-to-NA excitation has unity gain
, feedforward
inhibition causes a purely high-pass (transient) response in GCt
while GCs retains a low-pass (sustained) component. With a
, the dc gain, , approaches 1/2 and BT’s
small loop-gain,
and GCs’s responses become all-pass. However, as the loop gain
increases, decreases and these responses become high-pass.
The change in with loop gain is matched in both BT and NA,
and so taking the difference between these two signals always
cancels the sustained component in GCt. Thus, GCt produces a
purely high-pass response irrespective of the system’s loop gain.
A. Adapting to Temporal Frequency
Most physiological studies have characterized the retina’s response when stimulated with only one temporal frequency. We
can adopt a similar approach to characterize our model’s GC responses, but to do so, we must determine how our system adapts
to a single temporal frequency by deriving a mathematical expression for ’s dependence on contrast, , as well as input frequency, . As we stimulate our model with the same temporal
frequency and contrast at all spatial locations, such that there is
no difference between surround and center loop gain, we can set
in (8), provided the spatial frequency is not too high.
Then we introduce the frequency dependencies of
in order to determine the behavior of the system’s closed-loop
We assume sinusoidal inputs,
, with amplitude . We
also assume that the frequencies we are interested in are less
than the outer retina’s temporal cutoff, so that we can ignore
outer retina filtering for the moment, and that
have energy at these input frequencies, plus a dc component.
Hence, we obtain the spectra
where , , and are defined as above and
is the input
are the residual activity (dc and offsets)
, respectively. From our bipolar circuitry, we find
. The source of NA residual activity,
that is determined by
, is explained below.
, and
These currents only have energy at
so, using Parseval’s relationship, the ratio of the magnitudes of
these two currents is simply the square-root of the ratio of the
energy contained in ’s two impulses over that in ’s. Setting
to simplify the computation, we find
thus, reduce the slope of its rise. Furthermore, although does
not affect the temporal dynamics of the GCt’s response, we can
see that mismatch in will introduce low-frequency responses
in GCt. In summary, this analysis makes specific predictions
, temporal frequency
about how the open-loop time-constant
, and contrast interact to determine the frequency response,
when we stimulate with a single temporal frequency.
Fig. 6. Change in loop gain with frequency. The system loop gain, wg ,
depends both on temporal frequency and on contrast. Plots of this relationship
are shown on both a small (left) and large (right) frequency scale. Loop gain
rises with temporal frequency, ! , and saturates at a point determined by the
contrast level. For a given temporal frequency, higher contrasts generate a
larger loop gain.
gives the system loop-gain as a function of , , and , when
is substituted for . Recall that
, which
determines . Numerical solutions
means that the loop gain
to this relationship are plotted in Fig. 6 for five different contrast
of 1 s.
levels, with a
Finding approximations to (13) over different temporal frequency ranges, we obtain
, the system’s loop gain is
In the dc case, when
, which sets the
1, as expected. As
closed-loop time-constant,
, tracks
over the range
. In this region, the inner retina
effectively adapts to temporal frequency by matching its corner
frequency to the input. The adaptation, however, only takes
, the
place over these intermediate frequencies—below
, and above
system’s corner frequency is floored at
, it saturates at
We can use these loop gain expressions to determine the frequency response of our GC outputs. For temporal frequencies
, we can make the approximation
Ignoring the dc component, and invoking the relationship
, the GC frequency responses
simplify to
B. Adapting to Contrast
In addition to tracking temporal frequency, the inner retina
also adapts to input contrast. We can see from Fig. 6 that
loop-gain increases as we increase stimulus contrast and,
, so as to
hence, the system will adjust its corner frequency,
increase it, causing a speed up in the GC response and rejecting
a larger range of low frequencies. This contrast-dependence
, saturates with
arises because the point where loop gain,
temporal frequency occurs at higher temporal frequencies for
higher contrasts. This happens because NA’s response drops
at frequencies above
, making it
below its dc offset
impossible to track frequencies beyond this point.
However, to explore how our model responds to contrast in
natural scenes, which stimulate the retina with several temporal
frequencies simultaneously, we need to understand how much
each spectral component contributes to setting the loop gain,
. For any individual frequency, WA activity will reflect what
the adapted activity for that individual frequency ought to be
only to a limited extent since the WA activity will reflect the
weighted contributions of all the frequencies to loop gain. Thus,
although sensitivity to all frequencies drops when stimulus contrast increases, low-frequency gains are attenuated more [24]
since the system’s loop gain is pushed to a higher level by the
higher frequencies than would normally be the case if low input
frequencies solely determined system loop gain.
We use the same approach as above to formalize this intuition, but we now integrate the energy over the entire spectrum
acof temporal frequencies present to determine how and
tivity affect loop gain, . We assume a flat spectrum, with amplitude proportional to contrast, that is assumed to be low-pass
filtered by the outer retina. In this case, we define the contrast
spectral density, , as contrast, or amplitude, per unit frequency.
The relation between and the input signal contrast, , is given
, since we divide the input spectrum’s energy, or
contrast squared, by the bandwidth we are interested in. In this
and ’s spectra are given by
We can see from these equations that for input
at dc to
GCs’ response rises from
. Hence, we
Actually, it rises to at frequencies above
expect that GCs’ response will be hardly affected by changes in
since GCs’ response is practically flat across all . Finally,
we expect GC’s response to remain independent of , since it
does not appear in the equations.
On the other hand, the GCt response rises from
, following GCs’ behavior. Because
dc to
, GCt’s response is close to zero at dc. Reducing
shift the onset of its saturation range to higher frequencies and,
are defined as above. To facilitate
where , , , , and
our analysis, we approximate the outer retina as two low-pass
filters, with an identical fixed time constant of , that sharply
attenuate frequencies greater than
. Sketches of
’s spectra are shown in Fig. 7(a).
To find the loop gain, we take the ratio of the magnitudes of
and , computed using Parseval’s relationship. Simplifying
Fig. 7. Effect of contrast on loop gain. (a) BT activity, i , is the sum of three components: a dc component that depends on residual BT activity, b , a low-pass
component that equals d and cuts off at ! , and a high-pass component that rises as d ! , exceeds the low-pass component at !
1= , and saturates at
! . The outer retina provides an absolute cutoff at ! . NA activity, i , is the sum of a dc component that depends on NA residual activity, n , and a low-pass
component that equals dg and that cuts off at ! . Loop gain, wg , is determined by the ratio between the energy in i and the energy in i . (b) A numerical
solution for loop gain as a function of contrast (c = d ! ) for three different levels of residual activity, b . As b increases, the curves shift to the right, implying
that the contrast signal is not as strong. is 1.038 s and is 77 ms for this simulation.
our analysis by setting
and by treating the temporal
cutoffs at
as infinitely steep, we find
Recalling from (6) that is a function of loop gain
, we can
depends on input contrast.
find a numerical solution to how
This relationship is shown in Fig. 7(b) for three different values
approaches 1 as contrast per unit frequency,
of . Loop gain
, approaches
rises sublinearly with contrast over a range
. The
and saturates at a value determined by the ratio
contrast that realizes this saturation is determined by the amount
increases, the linear regime
of residual BC activity . As
shifts to higher contrasts. This implies that the determines the
system’s contrast threshold—the higher , the more contrast
we need to produce a given loop gain. This property, whereby
the amount of residual activity determines the strength of the
term from
input contrast signal, is analogous to Victor’s
The gross behavior of this analytical solution is captured by
the approximation
Loop gain rises sublinearly with contrast and saturates when
contrast exceeds some threshold, , that depends on . We can
derive approximately what this threshold, , is by recognizing
saturates when
in the denominator of
the second term of (19). Assuming that
in this case,
given above as
yields a
the saturation value for
limiting contrast value of
To better illustrate how varying levels of contrast affect
the range of temporal frequencies over which adaptation
takes place, we can recognize that, below , loop gain
quite well. Hence, our expressions
approximated by
for GC outputs (9) and (10) can be rewritten as
Fig. 8. Inner retina circuit. The inputs to the circuit, I and I , represent
complementary inputs to the rectifying BC circuit. We make five copies at the
output of this circuit (only three are shown in the figure). One copy drives
the ON-OFF low-pass filter to excite the NA on one side of the circuit while
inhibiting NA on the other side. A second copy is used to excite WAs, which
modulates NA feedback inhibition on to BT. The remaining three copies feed ON
and OFF versions of transient and sustained GCs (OnT, OnS, OffT, and OffS).
Frequencies below
are attenuated by
while frequencies above are not. Thus, the amount of attenuation, as well as the range of frequencies over which this attenuation takes place, gets larger with increasing contrast.
From our analysis, we see that both temporal frequency and
contrast are interrelated in their effect on the dynamics governing our inner retina model. Furthermore, because of the relationship between temporal frequency and contrast, changes in
one of these parameters cause changes in the model’s adaptation
to the other. Increasing either one of these parameters causes
the time constants of our model both to speed up, which affects
how our inner retina processes natural images. This adaptation
to contrast and temporal frequency makes retinal coding more
efficient, from an information theoretic perspective (see Discussion).
C. Circuit Implementation
The complete inner retina circuit that realizes the synaptic
interactions of Fig. 4 is shown in Fig. 8 (described in detail in
[29]). Briefly, differential signals from BC circuitry,
, drive either half of the circuit. Excitatory BT-to-NA current excite the NA node on one side of our circuit while also
inhibiting the NA node on the complementary side, thus realizing push-pull inhibition. These inputs are divided by the sum
of ON and OFF NA activity to compensate for the exponential voltage-current relationship in the subthreshold regime. NA
provides feedback inhibition on to BT, modulated by WA activity. Convergence of ON and OFF signals on to WA implements
full-wave rectification for both BT excitation and NA inhibition
of WA. WA nodes are coupled to one another through an nMOS
. A copy of NA current inhibits
diffusion network gated by
the transient GC. In fact, our circuit generates two copies of
transient signals so that we can pool transient GC inputs over
larger areas [30].
Because we have control over both WA coupling
and BT-to-NA gain
, we can explore how changing
these parameters changes GC responses. As WA modulation
determines the dynamics of GC responses, we expect the extent
, to
of spatial coupling in the WA network, controlled by
affect circuit dynamics. In our model, WA activity reflects
inputs weighted across spatial locations, and is influenced
by differences in center and surround WA activity. Relative
contributions from different loop gains at different spatial
locations are determined by the resistance of the WA network,
in (8). Here,
is the difference between
WA activity in a surround location, , and a center location,
, and is the resistance coupling these two locations. Thus,
depending on the strength of WA coupling, if WA activity in
the surround is larger than that in the center, we expect the loop
gain in the center to increase, whereas if the opposite is true,
we expect loop gain in the center to decrease.
BT-to-NA gain is determined by the relationship between
, , and
sets the source voltages for the NA
subcircuit such that WA activity can be represented by voltage
. A bias voltage, , determines leakage
deviations below
current, , from NA’s large membrane capacitor and, hence,
the time constant for both common-mode and differential signals. And the gain of BT-to-NA excitation is determined by a
, applied to the source of the current mirror’s
bias voltage,
should be set equal to
input transistor. Ideally,
a gain of one [29]. If
, then the gain, , is greater
than one, thus, WA activity should be lower and GCt responses
, then is less
should be inhibited. However, if
than one, causing the opposite effects [29]. Finally, another bias
in the model’s
voltage, , sets quiescent NA activity (i.e.,
equation) by exciting NA on both sides of the circuit with a current that is divided by ON and OFF NA activity (not shown). This
ensures that ON and OFF NA activity are limited by a geometric
does in the BT circuit).
mean constraint (just like
In this paper, we have presented our model and analyzed its
behavior. In order to construct our model, and in order to facilitate its analysis, we made several simplifications. We address
these assumptions and present our justifications here.
While our analysis of the outer retina demonstrates how our
model filters signals in space, capacitances associated with the
cone and HC networks create time constants that produce temporal filtering that is inseparable from spatial filtering. Details of
our outer retina’s temporal properties and their effect on spatial
filtering are discussed elsewhere [3]–[5]. Briefly, CT responses
in our model change from bandpass to low-pass in space as temporal frequency increases. They also change from bandpass to
low-pass in time as spatial frequency increases. This interplay
between spatial and temporal filtering creates a CT response that
peaks at a single temporal frequency for low spatial frequencies
and at a single spatial frequency for low temporal frequencies.
HCs modulate synaptic interactions to realize luminance adaptation in our outer retina model, but in the mammalian retina
this role is most likely played by dopaminergic amacrine cells
[12] and light sensing GCs [2].
Although temporal filtering in the outer retina is not addressed in this paper, we do use a simplified version of the outer
retina’s temporal filter for our analysis of contrast adaptation
in the inner retina. This analysis, presented in Section III,
models the outer retina as two low-pass filters with the same
time constant, . We felt this simplification was valid because
our inner retina analysis is limited to high spatial frequencies
where WA averaging across space occurs. At these high spatial
frequencies, spatiotemporal filtering in the outer retina is
indeed low-pass in time [3]–[5]. We examined responses in
this simpler condition to determine how the inner retina adapts
to temporal frequencies and contrast. The same adaptation
process still takes place when a more complex spatiotemporally
filtered signal is presented by the outer retina and, hence, the
simple picture we have painted may provide useful intuition.
Our inner retina model is based upon the functional architecture and physiological behavior of the mammalian retina. All the
synaptic interactions we included have been identified anatomically, as well as the complementary ON and OFF channels.
Complementary signaling starts at cone-to-bipolar synapses, by
using a sign-reversing synapse in one channel and half-wave
rectification in both [8]. Push-pull interactions maintain complementary signaling in the inner retina through reciprocal inhibition between ON and OFF channels, via vertically diffuse
amacrine cells that span the ON and OFF laminae [23]. Serial
inhibition [10] may also play a vital role in these interactions.
While the outer retina adapts its sensitivity to light intensity,
the inner retina adapts its low-pass and high-pass temporal filters to contrast and frequency. Encoding signals found in natural scenes optimally requires the retina’s bandpass filters to
peak at the spatial and temporal frequency where input signal
power drops to the noise floor [1], [27]. Therefore, as stimuli
with different spectra are presented to the retina, optimal coding
requires this filter’s peak frequency to move accordingly. Thus,
the retina must adapt to spatial and temporal frequency and to
luminance and contrast to continue to convey information efficiently to higher cortical structures. As stimulus power increases—as in the case of increased contrast—optimal filtering
demands that the peak of this bandpass filter moves to higher
frequencies, with a corresponding drop in low-frequency sensitivity.
Our inner retina model’s temporal filter realizes this adaptation to contrast—GC responses compress in time and amplitude
when driven by steps of increasing contrast [28]—by adjusting
its time constant [24], [28]. Our model proposes that this adaptation is implemented through WA modulation of NA feedback
(pre-synaptic inhibition). Thus, we offer an anatomical substrate
through which earlier dynamic models can be realized. A likely
biological candidate for this WA is the A19 amacrine cell [16],
which lies at the border between ON and OFF laminae, has thick
dendrites, a large axodendritic field, and is electrically coupled
to other A19 amacrine cells through gap junctions. Our inner
retina circuit design also corrects flaws in the design in [3],
which failed to produce temporal adaptation, and adds GC level
synaptic interactions and convergence.
Our retina model’s output is encoded as spike trains in four
types of GC outputs. We sought to model parasol (also called
Y in cat) and midget (also called X in cat) GCs, which respond
in a transient and in a sustained manner, respectively, at stimulus onset or offset. Both types of GCs receive synaptic input
from BCs and amacrine cells, although parasol cells receive
more amacrine synapses, and, presumably, more feedforward
inhibition [11], [17]. Hence, we included feedforward inhibition in our transient cells, but not in sustained cells. Furthermore, parasol cells also sample the visual scene nine times more
sparsely than midget cells, and have proportionately larger receptive fields [7]. Thus, we tiled our transient cells less densely,
and included convergence of bipolar signals on to these cells
(see [30]). Ninety percent of the total primate GC population is
made up of ON and OFF midget and parasol cells [22] and so we
concentrated our modeling efforts on these four cell types.
By morphing the retina’s functional architecture into a VLSI
circuit, we were able to create a circuit that expresses some
of the defining features of visual processing in the mammalian
retina. In our outer retina model, interaction between an excitatory cone network, which has relatively small space and time
constants, and an inhibitory HC network, which has larger space
and time constants, creates a bandpass spatiotemporal response.
This model adapts to input luminance through HC modulation
of cone-coupling and cone excitation, and through autofeedback, to produce a contrast signal at the CT. From our analysis,
we see that CT activity is determined by input contrast, and independent of mean luminance. Hence, our model’s CT’s S-shaped
behavior conveys a contrast signal to subsequent retina circuitry
that does not change with light intensity, similar to the behavior
exhibited by the mammalian retina. BCs in our model rectify
these signals into ON and OFF channels to replicate the retina’s
complementary signaling. Our design was based on push-pull
signaling in the mammalian retina that divides signals into complementary pathways to ensure efficient coding.
Furthermore, by morphing the inner retina’s functional architecture into a VLSI circuit, we were able to extend previous
models of visual processing in the mammalian retina. In our
inner retina model, modulation of NA presynaptic inhibition by
WAs realizes contrast gain control and time-constant adaptation.
WAs serve as an anatomical substrate for computing a neural
measure of contrast in our model. We use this measure of contrast in the same way that the retina is hypothesized to—modulation of feedback inhibition changes the system’s closed-loop
time constant. This adaptation allows our model to optimally
encode signals by adjusting its temporal filter based on input
frequency and contrast. Thus, in response to natural scenes, our
model measures all input frequencies present and computes how
the system should best filter these signals.
A number of parameters in our model and circuit determine
the system’s behavior. Manual control over HC coupling in our
outer retina model allows us to explore how changing space
constants in this network affects GC output. By adjusting the
NA leakage current, we also have control over the system’s
open-loop time constant. Changing this time constant affects the
circuits temporal response and changes the temporal frequency
above which closed-loop gain saturates. And by adjusting the
BT to NA gain, we have control of residual transient cell activity.
Finally, by adjusting coupling strength in the WA network, we
can explore the effect of spatial frequency on how loop gain is
computed over space. We explore some of these parameters in a
companion paper [30], where test results from a fabricated chip
are presented.
By reproducing some of the synaptic interactions found in the
mammalian retina, we were able to derive models for the outer
and inner retina that spatiotemporally filter signals, adapt to luminance, and exhibit contrast gain control. Our procedure has
been to construct a neural model based on known anatomy in
order to elicit some of the known behavior found in the physiology. While our model assigns novel roles to circuit elements
that can account for this behavior, we still need to validate these
conjectures by comparing our model’s behavior with that of the
mammalian retina. This detailed comparison will be presented
in a forthcoming paper.
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Kareem A. Zaghloul (S’00–M’03) received the
B.S. degree from the Department of Electrical
Engineering and Computer Science, Massachusetts
Institute of Technology, Cambridge, in the in 1995,
where he made Tau Beta Kappa and Eta Kappa Nu.
He recently completed a combined M.D./Ph.D. program at the University of Pennsylvania, Philadelphia.
The Ph.D. degree was awarded in the Department
of Neuroscience, where he worked on understanding
information processing in the mammalian retina
with K. A. Boahen. His work was supported by
a Vision Training Grant from the National Institutes of Health and a Ben
Franklin Fellowship from the University of Pennsylvania School of Medicine.
He is currently a Resident Physician in the Department of Neurosurgery at the
University of Pennsylvania.
Kwabena A. Boahen received the B.S. and M.S.E.
degrees in electrical and computer engineering
from the Johns Hopkins University, Baltimore
MD, in the concurrent masters-bachelors program,
both in 1989, where he made Tau Beta Kappa. He
received the Ph.D. degree in computation and neural
systems from the California Institute of Technology,
Pasadena, in 1997, where he held a Sloan Fellowship
for Theoretical Neurobiology.
He is an Associate Professor in the Bioengineering Department, University of Pennsylvania,
Philadelphia, where he holds a secondary appointment in the electrical engineering. He was awarded a Packard Fellowship in 1999. His current research
interests include mixed-mode multichip VLSI models of biological sensory
and perceptual systems, and their epigenetic develoipment, and asynchronous
digital interfaces for interchip connectivity.
Dr. Boahen received a National Science Foundation (NSF) CAREER Award
in 2001 and an Office of Naval Research (ONR) YIP Award in 2002.
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