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Seeing beyond the receptive field in primary visual cortex
David Fitzpatrick
Recent studies on the response properties of neurons in
primary visual cortex emphasize the dynamics and the
complexities of facilitatory and suppressive interactions
between the receptive field center and surrounding areas of
visual space. These observations raise new questions about
the circuitry responsible for receptive field surround effects and
their contribution to visual perception.
Addresses
Department of Neurobiology, Box 3209, Duke University Medical
Center, Durham, NC 27710, USA; e-mail: [email protected]
Current Opinion in Neurobiology 2000, 10:438–443
0959-4388/00/$ — see front matter
© 2000 Elsevier Science Ltd. All rights reserved.
Introduction
Defining the limits of the receptive field of a neuron in visual cortex has never been a simple issue; however, a
fundamental distinction can be made between the region of
visual space in which stimuli evoke spike discharges (the socalled ‘classical receptive field’, or receptive field center) and
a surrounding region that, although not capable of driving
responses, can exert robust suppressive or facilitative effects
on the response to the presentation of stimuli in the classical
receptive field [1–7]. This distinction has had considerable
impact on studies of cortical function because center–surround interactions have the potential to explain a variety of
psychophysical observations in which context alters stimulus
detectability or appearance. For example, facilitatory surround effects have been implicated in processes such as
contour integration [5,8] and inhibitory effects have been
viewed as the basis for perceptual ‘pop-out’, curvature detection, and illusory contours [3,6,9–11]. Moreover, receptive
field centers and surrounds are thought to be mediated by
different cortical circuits. The properties of the classical
receptive field are thought to arise from the cortical column
and nearby regions of cortex (within 500 µm), whereas surround effects are the province of long-distance horizontal
connections that extend for several millimeters across the
cortical surface, and/or feedback connections from extrastriate areas (see [12,13] for reviews). The results of several
studies published in the period of review have considerably
extended our knowledge of the spatial properties of cortical
receptive fields and the underlying circuits. Taken together,
they emphasize the dynamic nature of the relationship
between the classical receptive field and surrounding regions
of visual space. At the same time, they pose new challenges
for understanding the neural mechanisms that are responsible for these effects as well as their perceptual significance.
Defining the receptive field center
Before considering center–surround interactions in more
detail, it is first necessary to distinguish two different
methods that have been used to define the borders of the
receptive field center. One approach has been to present a
small stimulus, usually a light or dark bar at the appropriate orientation, and to use either stimulus-onset location or
movement to delimit the area of visual space that elicits
spike discharges above some background level. This
approach yields what is generally referred to as a minimum
discharge field [14,15]. Another approach is to define the
receptive field center as the area of visual space over which
increasing the stimulus size elicits a larger response
[16–18]. This is often assessed using sine-wave gratings,
the length and width of the receptive field being defined
by characterizing the smallest stimulus dimensions that
produce the maximum discharge rate.
In principle, each measure provides useful information
about the spatial characteristics of a neuron’s receptive
field. However, the size of the receptive field center calculated using these two measures can be quite different (see
[19••] for a direct comparison). As nicely illustrated in a
recent intracellular study by Bringuier et al. [20•] (see also
[21•] for a similar account of orientation tuning), the reason
for this difference is likely to reside in the iceberg-like spatial profile of a cortical neuron’s stimulus sensitivity. The
peak sensitivity is found near the center of the receptive
field, and sensitivity declines to subthreshold levels as one
moves away from the center. The minimum discharge
field is a fraction of the region that is capable of eliciting a
depolarizing response — the peak of the iceberg.
Receptive field dimensions based on areal summation will
often be larger than those using the minimum discharge
measure because they are likely to include regions that are
incapable of driving the cell when stimulated in isolation
but will augment the rate of response to stimulation of the
more sensitive areas of the field. As will become apparent,
the use of these two different measures of receptive field
size contributes to difficulties in evaluating the findings
from different studies.
Facilitation beyond the classical receptive field?
Evidence that stimuli presented beyond the minimum discharge field have a facilitatory influence over the response
to stimulation of the receptive field center has been provided in a number of studies [2,5,22]. The most effective
stimuli for eliciting surround facilitation are bars or gratings
at the cell’s preferred orientation that are placed in the
receptive field endzones (i.e. along the collinear axis in
visual space). However, the relationship between the facilitatory effects of presenting separate stimuli in the center
and surround and a neuron’s length summation area has
remained a matter of controversy. Some authors have
argued that facilitatory surround effects can be explained
as the placement of surround stimuli within a cell’s length
summation area; because these authors regard this as part
Seeing beyond the receptive field in primary visual cortex Fitzpatrick
of the receptive field center, they conclude that there are
no facilitatory inputs from the surround [16,17,23••]. Other
authors, however, have demonstrated that facilitatory
effects induced by the presentation of discrete stimuli in
the center and the surround can be elicited from regions
beyond the length summation area — in some cases,
regions that produce suppression (endstopping) when long
bars are used as stimuli [5].
Two recent studies in macaque striate cortex provide a resolution to this apparent contradiction by demonstrating
that the length summation areas of cortical neuron receptive fields are not fixed, but vary as a function of stimulus
contrast ([19••,24••]; see also [7] for similar results in cat
visual cortex). For many cells, the length tuning curve for
high-contrast stimuli plateaus at relatively short stimulus
lengths, and these cells often exhibit endstopping to
longer-length stimuli. At low contrast values, however, the
size of the length summation area is increased by as much
as 2 to 4 times that found at high contrast levels and there
is no sign of a reduced response to longer stimuli. Thus,
the same region of visual space can exert no effect, a facilitatory effect, or a suppressive effect on a cell’s response,
depending on stimulus contrast. A similar contrast dependence is evident in studies that have probed
center–surround interactions using multiple discrete stimuli. The type of effect induced by presentation of a
collinear stimulus outside the minimum discharge field
can often be changed from facilitation to suppression by
increasing the contrast of the stimulus in the receptive
field center [7,18,25,26,27•,28]. Thus, whether one views
this behavior as a contrast-dependent change in receptive
field size or as contrast dependence of surround effects, a
single, contrast-dependent spatial summation mechanism
is likely to account for many of the observations with both
discrete and continuous stimuli.
Why should cortical neurons enlarge their summation area at
low contrast levels? Sceniak et al. [24••] argue that this
mechanism may effectively trade resolution for sensitivity,
pooling signals to enhance the ability to detect contours
under conditions where signals are weak. In a general sense,
the changes in receptive field summation properties resemble the changes in the surrounds of retinal ganglion cells
under low levels of illumination, where the inhibition
evoked from receptive field surrounds is reduced in favor of
summation of weak signals [29]. This might suggest that the
role of summation in contour detection is limited to lowcontrast stimuli; indeed, the contribution of excitatory
summation to contour-integration mechanisms at higher
contrast levels has been challenged on several grounds [30•].
Kapadia et al. [19••], however, provide evidence that length
summation area is also enhanced for the presentation of
high-contrast stimuli in the receptive field center when they
are surrounded by a complex texture pattern. Furthermore,
the strength of surround facilitation to high-contrast stimuli
can be enhanced or reduced depending on attentional factors [31••]. Thus, increased levels of summation may be a
439
more general mechanism that operates whenever the signalto-noise ratio limits contour detection.
It seems likely that long-range horizontal connections play
a major role in shaping the length summation properties of
V1 neurons. The fact that these connections arise from
pyramidal neurons, that they preferentially link sites with
similar orientation preferences, and that they are elongated
along a collinear axis in the map of visual space, is consistent with many of the observed effects [32–34]. However,
the mechanism that underlies the contrast-dependent
change in summation properties remains unclear. Modeling
studies have suggested that the level of drive to the receptive field center determines the sign of the response,
favoring inhibition at high levels of activity and facilitation
at low levels [35,36]. However, the findings from Sceniak
et al. [24••], in which a difference-of-Gaussians receptive
field model was used to assess changes in surround facilitation and inhibition, suggest that the result may be
explained without a change in the strength of inhibition —
in other words, by changes in the efficacy of horizontal excitatory inputs alone. Clearly, an intracellular analysis of
length summation properties at different contrasts would
shed considerable light on this issue [37].
Local connections as a source of inhibitory
surround interactions
One of the principal reasons for assuming that long-distance horizontal connections are the substrate for receptive
field surround effects is that nearby sites in visual cortex
were thought to represent overlapping regions of visual
space; in order to mediate an effect from surrounding
regions of visual space, connections would have to extend
some distance (1.5–2 mm on average) across the cortical
map. But recent studies in cat visual cortex suggest that
our view of cortical topography may need to be revised and
that the structure of the visuotopic map may bring cells
with non-overlapping receptive fields into close proximity,
allowing short-range connections to mediate some types of
surround effects [38,39••].
Evidence that the mapping of visual space is less regular
than was previously believed comes from experiments in
which the positions of the minimum response fields of
individual neurons are compared to the maps of orientation
preference [38]. Previous studies using optical imaging
techniques have demonstrated that orientation is mapped
in a systematic fashion across the cortical surface such that
nearby sites prefer similar but slightly shifted orientation
values. However, this smooth progression is interrupted
periodically by small discontinuities (pinwheel centers or
fractures). In these regions, the orientation preference of
neurons from nearby sites can differ substantially, often by
90° [40,41]. This comparison demonstrates that recording
sites from regions near discontinuities in the orientation
map are often associated with jumps in receptive field
positions; these jumps are rarely encountered in other
parts of the orientation map. As a result of this distortion in
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Sensory systems
the mapping of visual space, sites that are separated by less
than 300 µm near orientation discontinuities can differ significantly in their response properties, preferring
orthogonal orientations presented to non-overlapping
regions of visual space.
What are the consequences of this organization for the
responses of cortical neurons? One possibility is that local
connectional patterns are altered such that regions of the
map with similar properties are strongly connected, whereas neurons in regions near high-rate-of-change areas are
less well connected. Using cross-correlation of spike discharges from pairs of neurons, Das and Gilbert [39••]
provide evidence that this is not the case. Neurons separated by distances of up to 800 µm exhibit a high degree of
temporal correlation in their firing patterns, regardless of
their location in the cortex. This correlation in firing falls
off with distance and does not depend on the orientation
preference of the members of the pair (cells with orthogonal preferences are just as likely to be correlated in their
firing patterns as those with similar orientation preference). Combined with anatomical evidence for a lack of
specificity in local horizontal connections [33,34,42], these
results suggest that local connections in layer 2/3 are a
source of common input for cells that have diverse receptive field properties. Thus, for neurons that lie near
discontinuities in the maps of visual space and orientation,
local connections could mediate receptive field surround
effects, linking cells with non-overlapping receptive fields
and different orientation preferences.
This possibility has been tested by exploring the effects of
presenting short bars oriented orthogonal to the cell’s preferred orientation in the region of visual space that lies just
outside the neuron’s minimum discharge field. In some
neurons, this stimulus configuration is found to suppress
the response to stimuli in the receptive field center.
Furthermore, the degree of suppression is dependent on
the position of the neuron within the cortical map. Flank
suppression is most prominent for neurons that are located
near map discontinuities, in regions where flank and
receptive field center stimulation would be expected to
activate nearby populations of cortical neurons. Flank suppression is considerably weaker for neurons located distant
from the discontinuities, where flank and receptive field
center stimulation would be expected to activate more
remote populations of cortical neurons. These differences
were evident even though the distance in visual space
between the receptive field center and the flank regions
was identical for both sets of neurons. Das and Gilbert
[39••] suggest that these suppressive interactions support
the detection of angles or T-junctions in the visual field
and that the machinery to map these more complex stimulus configurations may also be systematically mapped
across the cortical surface. In this view, pinwheel singularities are not epiphenoma of the mapping of orientation
preference in the cortex, but are a structural arrangement
that allows for the analysis of junctional borders.
Challenges to the T-junction proposal
These are novel and appealing ideas that relate the fine
structure of functional maps to receptive field properties
and patterns of connectivity. However, additional studies are
necessary to confirm the correlation between rate of change
in orientation and rate of change in receptive field position
that is central to this hypothesis. For example, a recent
study that used tetrode recordings to evaluate the fine structure of the mapping of visual space in cat visual cortex did
not find a correlation; however, this study did not specifically target regions where orientation preference values are
changing rapidly and this could account for the difference
[43•]. Also, analysis of the map of visual space in the tree
shrew, using imaging and electrode recordings, indicates
that the mapping of visual space is smooth and continuous
throughout, showing no sign of jumps that could correlate
with orientation pinwheel centers [44]. Likewise, the
V1–V2 border region of the ferret, where there are large
jumps in the mapping of visual space, is not associated with
an increase in the density of pinwheels or fractures in the
orientation map [45•,46]. Thus, the relationship between
the mapping of visual space and the mapping of orientation
preference described in the cat is not universal; it remains to
be seen whether discontinuities in the mapping of visual
space are present in other species, including primates.
The relation of these findings to other accounts of the orientation tuning and spatial distribution of inhibitory inputs is
also far from clear. Previous studies of inhibitory surround
effects have demonstrated that iso-orientation stimuli are far
more effective at suppressing responses than orthogonal ones
[3,17,22,23••,47]. There is, however, evidence that orthogonal
stimuli evoke inhibition within the receptive field center,
using the areal summation measure as the basis for defining
the extent of the center [16,48,49]. This so-called ‘cross-orientation inhibition’ has been revealed in extracellular
recordings by superimposing within the receptive field a grating of the preferred orientation with one of the orthogonal
orientation. In these experiments, the most robust suppressive effects are found when the contrast of the grating at the
preferred orientation is roughly half that of the orthogonal
grating; the same characteristics apply to the flank suppression described by Das and Gilbert [39••]. More details about
the orientation tuning and the spatial distribution of the
flanking suppression are necessary to fully compare the two
effects; however, if they are the same phenomenon, then
there is reason to question whether the flank suppression
described by Das and Gilbert has the strict spatial organization or the tight orientation tuning that would be required to
serve as a T-junction detector. Receptive field center suppression, at least, is broadly tuned for orientation, a factor that
has led to the view that it plays a role in normalizing cortical
cell responses, maintaining selectivity of response despite
changes in stimulus contrast [16,48,50].
Asymmetric surround suppression
Despite the inconsistencies described above, the more general point — that inhibitory surrounds are often localized to
Seeing beyond the receptive field in primary visual cortex Fitzpatrick
small regions of space and can be quite varied in their position relative to the receptive field center — finds support in
another study of cat visual cortex in which small patches of
gratings are used to evaluate the spatial layout of iso-orientation inhibitory flanks [23••]. On the basis of previous
studies using relatively large surround stimuli, iso-orientation inhibitory flanks are conceived as being symmetrical in
their distribution around the receptive field, localized
either in the end-zones (the source of end-stopping) or
along the sides (side-band inhibition). This new analysis
demonstrates that inhibitory flanks beyond the excitatory
summation zone are more often asymmetric, restricted to
one end of the receptive field or to one side. Furthermore,
some cells exhibit a single inhibitory flank that is located at
an oblique angle to the field — in other words, neither at
the ends nor at the sides. The functional significance of this
array of spatial relationships is not clear; however, it emphasizes that the nature of inhibitory surround interactions is
far more intricate and diverse than had been appreciated.
The source of suppressive effects
Ultimately, the final common path for the expression of
these inhibitory effects is the population of smooth-dendritic GABAergic interneurons. This is an extremely
diverse class of neurons that differ in their morphology,
peptide content, and synaptic properties [51••,52].
Although most of these neurons have rather restricted axon
arbors, one class, the basket cell, gives rise to axons that
can spread upwards of 1.5 mm across the cortical surface
[53]. Comparison of the distribution of the axon terminals
of this cell class with maps of orientation preference
reveals that they contact sites with a broad range of orientation preferences [42]; this suggests that they could be the
source of the broadly tuned inhibition that characterizes
the receptive field center suppression. However, the isoorientation suppression from the surround is likely to
involve excitatory long-distance horizontal connections
that synapse with a population of local inhibitory neurons.
Although injections of tracer substances generally show a
broad distribution of horizontal inputs [32–34], individual
neurons may sample selectively from this array to generate
the restricted and variable position of the inhibitory flanks.
Conclusions
The division between the receptive field center and surround continues to provide a framework for understanding
how the information from multiple stimuli is encoded in
the responses of individual neurons. As recent studies
emphasize, however, the distinction between center and
surround is less rigid than was once thought. The area of
visual space that evokes spike discharges in a neuron is
surrounded by a large subthreshold region capable of eliciting depolarizing responses. Consistent with this
observation, the size of the spike discharge zone is not
fixed but can vary with contrast and context and can be
altered by attentional factors. Likewise, the strict linkage
between horizontal connections and receptive field surround effects has to be tempered with the evidence for
441
irregularity in the mapping of visual space. Ultimately, elucidating the mechanisms that underlie spatial interactions
in visual processing will require techniques that relate the
responses of individual neurons to large-scale patterns of
activity in the cortical network [54,55•,56••]. In this light,
the availability of new voltage-sensitive dye techniques for
visualizing cortical activity patterns with high temporal and
spatial resolution [57•] may provide the next step in understanding the significance of the complex array of excitatory
and inhibitory interactions that occur within and beyond
the receptive field.
Acknowledgements
Thanks to Frank Sengpiel, Michele Pucak, and Heather Chisum for helpful
comments on the manuscript. Support provided by National Institutes of
Health grants EY06821, EY06729, and the McKnight Foundation.
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Science 2000, 287:273-278.
Based on an impressive number of simultaneous patch recordings from
GABAergic interneurons and their postsynaptic targets in rat cortical slices, the
authors provide evidence for 14 different classes of interneurons, on the basis of
discharge pattern and axonal tree morphology. Furthermore, these 14 classes sort
into three functional groups that differ in their response to repetitive stimulation.
52. Miles R: Diversity in inhibition. Science 2000, 287:244.
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55. Jancke D, Erlhagen W, Dinse HR, Akhavan AC, Giese M, Steinhage A,
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Schoner G: Parametric population representation of retinal
location: neuronal interaction dynamics in cat primary visual
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Using the responses of neurons in cat visual cortex to the presentation of
small squares of light, the authors construct distributions of population
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activity for each stimulus and then compare the response to individual
stimuli with that to two stimuli at varied separations. The results provide
evidence for a non-linear distance-dependent repulsive effect that results
from the spatiotemporal spread of excitation and inhibition.
56. Tsodyks M, Kenet T, Grinvald A, Arieli A: Linking spontaneous
•• activity of single cortical neurons and the underlying functional
architecture. Science 1999, 286:1943-1946.
By combining real-time voltage-sensitive dye imaging with extracellular
recordings from individual neurons, the authors demonstrate that the
spontaneous activity of single neurons reflects the instantaneous spatial
pattern of activity in a large cortical area and that this pattern is similar
to that seen when neurons are activated by visual stimuli. The results
emphasize the extent of, and the specificity in, the distributed activity
patterns of cortical circuits — factors that are likely to play a significant
role in the excitatory and inhibitory spatial interactions that constitute
receptive field surround effects.
57.
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Shoham D, Glaser DE, Arieli A, Kenet T, Wijnbergen C, Toledo Y,
Hildesheim R, Grinvald A: Imaging cortical dynamics at high spatial
and temporal resolution with novel blue voltage-sensitive dyes.
Neuron 1999, 24:791-802.
An excellent review of the advances in in vivo voltage-sensitive dye recordings that allow the visualization of large-scale patterns of cortical activity.