scholarly journals A unifying motif for spatial and directional surround suppression

2017 ◽  
Author(s):  
Liu D. Liu ◽  
Kenneth D. Miller ◽  
Christopher C. Pack

AbstractIn the visual system, the response to a stimulus in a neuron’s receptive field can be modulated by stimulus context, and the strength of these contextual influences vary with stimulus intensity. Recent work has shown how a theoretical model, the stabilized supralinear network (SSN), can account for such modulatory influences, using a small set of computational mechanisms. While the predictions of the SSN have been confirmed in primary visual cortex (V1), its computational principles apply with equal validity to any cortical structure. We have therefore tested the generality of the SSN by examining modulatory influences in the middle temporal area (MT) of the macaque visual cortex, using electrophysiological recordings and pharmacological manipulations. We developed a novel stimulus that can be adjusted parametrically to be larger or smaller in the space of all possible motion directions. We found, as predicted by the SSN, that MT neurons integrate across motion directions for low-contrast stimuli, but that they exhibit suppression by the same stimuli when they are high in contrast. These results are analogous to those found in visual cortex when stimulus size is varied in the space domain. We further tested the mechanisms of inhibition using pharmacologically manipulations of inhibitory efficacy. As predicted by the SSN, local manipulation of inhibitory strength altered firing rates, but did not change the strength of surround suppression. These results are consistent with the idea that the SSN can account for modulatory influences along different stimulus dimensions and in different cortical areas.Significance StatementVisual neurons are selective for specific stimulus features in a region of visual space known as the receptive field, but can be modulated by stimuli outside of the receptive field. The SSN model has been proposed to account for these and other modulatory influences, and tested in V1. As this model is not specific to any particular stimulus feature or brain region, we wondered whether similar modulatory influences might be observed for other stimulus dimensions and other regions. We tested for specific patterns of modulatory influences in the domain of motion direction, using electrophysiological recordings from MT. Our data confirm the predictions of the SSN in MT, suggesting that the SSN computations might be a generic feature of sensory cortex.

1995 ◽  
Vol 74 (2) ◽  
pp. 779-792 ◽  
Author(s):  
A. Das ◽  
C. D. Gilbert

1. Receptive field (RF) sizes of neurons in adult primary visual cortex are dynamic, expanding and contracting in response to alternate stimulation outside and within the RF over periods ranging from seconds to minutes. The substrate for this dynamic expansion was shown to lie in cortex, as opposed to subcortical parts of the visual pathway. The present study was designed to examine changes in cortical connection strengths that could underlie this observed plasticity by measuring the changes in cross-correlation histograms between pairs of primary visual cortex neurons that are induced to dynamically change their RF sizes. 2. Visually driven neural activity was recorded from single units in the superficial layers of primary visual cortex in adult cats, with two independent electrodes separated by 0.1–5 mm at their tips, and cross-correlated on-line. The neurons were then conditioned by stimulation with an “artificial scotoma,” a field of flashing random dots filling the region of visual space around a blank rectangle enclosing the RFs of the recorded neurons. The neuronal RFs were tested for expansion and their visually driven output again cross-correlated. After this, the neurons were stimulated vigorously through their RF centers to induce the field to collapse, and the visually driven output from the collapsed RFs was again cross-correlated. Cross-correlograms obtained before and after conditioning, and after RF collapse, were normalized by their flanks to control for changes in peak size due solely to fluctuations in spike rate. 3. A total of 37 pairs of neurons that showed distinct cross-correlogram peaks, and whose RF borders were clearly discernible both before and after conditioning, were used in the final analysis. Of these neuron pairs, conditioning led to a clear expansion of RF boundaries in 28 pairs, whereas in 9 pairs the RFs did not expand. RFs that did expand showed no significant shifts in their orientation preference, orientation selectivity, or ocularity. 4. When the RFs of a pair of neurons expanded with conditioning, the area of the associated flank-normalized cross-correlogram peaks also increased (by a factor ranging from 0.84 up to 3.5). Correlograms returned to their preconditioning values when RFs collapsed.(ABSTRACT TRUNCATED AT 400 WORDS)


2017 ◽  
Vol 118 (6) ◽  
pp. 3282-3292 ◽  
Author(s):  
Jason M. Samonds ◽  
Berquin D. Feese ◽  
Tai Sing Lee ◽  
Sandra J. Kuhlman

Complex receptive field characteristics, distributed across a population of neurons, are thought to be critical for solving perceptual inference problems that arise during motion and image segmentation. For example, in a class of neurons referred to as “end-stopped,” increasing the length of stimuli outside of the bar-responsive region into the surround suppresses responsiveness. It is unknown whether these properties exist for receptive field surrounds in the mouse. We examined surround modulation in layer 2/3 neurons of the primary visual cortex in mice using two-photon calcium imaging. We found that surround suppression was significantly asymmetric in 17% of the visually responsive neurons examined. Furthermore, the magnitude of asymmetry was correlated with orientation selectivity. Our results demonstrate that neurons in mouse primary visual cortex are differentially sensitive to the addition of elements in the surround and that individual neurons can be described as being either uniformly suppressed by the surround, end-stopped, or side-stopped. NEW & NOTEWORTHY Perception of visual scenes requires active integration of both local and global features to successfully segment objects from the background. Although the underlying circuitry and development of perceptual inference is not well understood, converging evidence indicates that asymmetry and diversity in surround modulation are likely fundamental for these computations. We determined that these key features are present in the mouse. Our results support the mouse as a model to explore the neural basis and development of surround modulation as it relates to perceptual inference.


2001 ◽  
Vol 18 (4) ◽  
pp. 501-516 ◽  
Author(s):  
WILSON S. GEISLER ◽  
DUANE G. ALBRECHT ◽  
ALISON M. CRANE ◽  
LAWRENCE STERN

When an image feature moves with sufficient speed it should become smeared across space, due to temporal integration in the visual system, effectively creating a spatial motion pattern that is oriented in the direction of the motion. Recent psychophysical evidence shows that such “motion streak signals” exist in the human visual system. In this study, we report neurophysiological evidence that these motion streak signals also exist in the primary visual cortex of cat and monkey. Single neuron responses were recorded for two kinds of moving stimuli: single spots presented at different velocities and drifting plaid patterns presented at different spatial and temporal frequencies. Measurements were made for motion perpendicular to the spatial orientation of the receptive field (“perpendicular motion”) and for motion parallel to the spatial orientation of the receptive field (“parallel motion”). For moving spot stimuli, as the speed increases, the ratio of the responses to parallel versus perpendicular motion increases, and above some critical speed, the response to parallel motion exceeds the response to perpendicular motion. For moving plaid patterns, the average temporal tuning function is approximately the same for both parallel motion and perpendicular motion; in contrast, the spatial tuning function is quite different for parallel motion and perpendicular motion (band pass for the former and low pass for the latter). In general, the responses to spots and plaids are consistent with the conventional model of cortical neurons with one rather surprising exception: Many cortical neurons appear to be direction selective for parallel motion. We propose a simple explanation for “parallel motion direction selectivity” and discuss its implications for the motion streak hypothesis. Taken as a whole, we find that the measured response properties of cortical neurons to moving spot and plaid patterns agree with the recent psychophysics and support the hypothesis that motion streak signals are present in V1.


2009 ◽  
Vol 102 (4) ◽  
pp. 2069-2083 ◽  
Author(s):  
S. Shushruth ◽  
Jennifer M. Ichida ◽  
Jonathan B. Levitt ◽  
Alessandra Angelucci

In visual cortex, responses to stimulation of the receptive field (RF) are modulated by simultaneous stimulation of the RF surround. The mechanisms for surround modulation remain unidentified. We previously proposed that in the primary visual cortex (V1), near surround modulation is mediated by geniculocortical and horizontal connections and far surround modulation by interareal feedback connections. To understand spatial integration in the secondary visual cortex (V2) and its underlying circuitry, we have characterized spatial summation in different V2 layers and stripe compartments and compared it to that in V1. We used grating stimuli in circular and annular apertures of different sizes to estimate the extent and sensitivity of RF and surround components in V1 and V2. V2 RFs and surrounds were twice as large as those in V1. As in V1, V2 RFs doubled in size when measured at low contrast. In both V1 and V2, surrounds were about fivefold the size of the RF and the far surround could exceed 12.5° in radius, averaging 5.5° in V1 and 9.2° in V2. The strength of surround suppression was similar in both areas. Thus although differing in spatial scale, the interactions among RF components are similar in V1 and V2, suggesting similar underlying mechanisms. As in V1, the extent of V2 horizontal connections matches that of the RF center, but is much smaller than the largest far surrounds, which likely derive from interareal feedback. In V2, we found no laminar or stripe differences in size and magnitude of surround suppression, suggesting conservation across stripes of the basic circuit for surround modulation.


2002 ◽  
Vol 19 (4) ◽  
pp. 439-452 ◽  
Author(s):  
JONATHAN B. LEVITT ◽  
JENNIFER S. LUND

We recorded activity of single units in macaque monkey primary visual cortex (V1) to define the retinotopic extent of the visual inputs that drive or modulate V1 neuron responses in parafoveal and peripheral (calcarine) cortex. We used high-contrast drifting grating stimuli to define the extent of the area over which responses summate and the extent of the receptive-field surround. We found responses of most V1 cells to summate over 1 deg, with a suppressive surround typically twice that in diameter, though for some cells (even in parafoveal V1) surrounds exceeded 13 deg in diameter. Surprisingly, we found no significant laminar differences in these dimensions or in the strength of surround suppression. We found that surround suppression in most cells arises from both the ends and sides of the receptive field. Our measures indicate that the strongest modulatory input arises from regions immediately adjacent to the excitatory summation area. These physiological measures suggest that the high-contrast summation field of V1 neurons can be accounted for by the sum of lateral geniculate nucleus (LGN) inputs offered to the local cortical column, with monosynaptic lateral connections within area V1 adding the larger dimensions of the low-contrast summation field and the near surround. Neither of these inputs suffice to explain the largest surrounds, which most likely derive from feedback from extrastriate visual areas.


2017 ◽  
Author(s):  
Maryam Bijanzadeh ◽  
Lauri Nurminen ◽  
Sam Merlin ◽  
Alessandra Angelucci

Visual perception is profoundly affected by spatial context. In visual cortex, neuronal responses to stimuli inside their receptive field (RF) are suppressed by contextual stimuli in the RF surround (surround suppression). How do neuronal RFs integrate information across visual space, and what role do different cortical layers play in the processing of spatial context? By recording simultaneously across all layers of macaque primary visual cortex, while presenting visual stimuli at increasing distances from the recorded cells RF, we find that near vs. far stimuli activate distinct layers. Stimuli in the near-surround evoke the earliest subthreshold responses in superficial and deep layers, and cause the earliest surround suppression of spiking responses in superficial layers. Instead, far-surround stimuli evoke the earliest subthreshold responses in feedback-recipient layers, i.e. 1 and the lower half of the deep layers, and suppress visually-evoked spiking responses almost simultaneously in all layers, except 4C, where suppression emerges latest. Our results reveal unique contributions of the cortical layers to the processing of local and global spatial context, and suggest distinct underlying circuits for local and global signal integration.


Author(s):  
Andreas J Keller ◽  
Morgane M Roth ◽  
Massimo Scanziani

We sense our environment through pathways linking sensory organs to the brain. In the visual system, these feedforward pathways define the classical feedforward receptive field (ffRF), the area in space where visual stimuli excite a neuron1. The visual system also uses visual context, the visual scene surrounding a stimulus, to predict the content of the stimulus2, and accordingly, neurons have been found that are excited by stimuli outside their ffRF3–8. The mechanisms generating excitation to stimuli outside the ffRF are, however, unclear. Here we show that feedback projections onto excitatory neurons in mouse primary visual cortex (V1) generate a second receptive field driven by stimuli outside the ffRF. Stimulating this feedback receptive field (fbRF) elicits slow and delayed responses compared to ffRF stimulation. These responses are preferentially reduced by anesthesia and, importantly, by silencing higher visual areas (HVAs). Feedback inputs from HVAs have scattered receptive fields relative to their putative V1 targets enabling the generation of the fbRF. Neurons with fbRFs are located in cortical layers receiving strong feedback projections and are absent in the main input layer, consistent with a laminar processing hierarchy. The fbRF and the ffRF are mutually antagonistic since large, uniform stimuli, covering both, suppress responses. While somatostatin-expressing inhibitory neurons are driven by these large stimuli, parvalbumin and vasoactive-intestinal-peptide-expressing inhibitory neurons have antagonistic fbRF and ffRF, similar to excitatory neurons. Therefore, feedback projections may enable neurons to use context to predict information missing from the ffRF and to report differences in stimulus features across visual space, regardless if excitation occurs inside or outside the ffRF. We have identified a fbRF which, by complementing the ffRF, may contribute to predictive processing.


2014 ◽  
Vol 111 (9) ◽  
pp. 1783-1791 ◽  
Author(s):  
Sung Jun Joo ◽  
Scott O. Murray

Neural responses in early visual cortex depend on stimulus context. One of the most well-established context-dependent effects is orientation-specific surround suppression: the neural response to a stimulus inside the receptive field of a neuron (“target”) is suppressed when it is surrounded by iso-oriented compared with orthogonal stimuli (“flankers”). Despite the importance of orientation-specific surround suppression in potentially mediating a number of important perceptual effects, including saliency, contour integration, and orientation discrimination, the underlying neural mechanisms remain unknown. The suppressive signal could be inherited from precortical areas as early as the retina and thalamus, arise from local circuits through horizontal connections, or be fed back from higher visual cortex. Here, we show, using two different methodologies, measurements of scalp-recorded event-related potentials (ERPs) and behavioral contrast adaptation aftereffects in humans, that orientation-specific surround suppression is dependent on the surface structure in an image. When the target and flankers can be grouped on the same surface (independent of their distance), orientation-specific surround suppression occurs. When the target and flankers are on different surfaces (independent of their distance), orientation-specific surround suppression does not occur. Our results demonstrate a surprising role of high-level, global processes such as grouping in determining when contextual effects occur in early visual cortex.


2007 ◽  
Vol 24 (1) ◽  
pp. 99-109 ◽  
Author(s):  
CHRIS TAILBY ◽  
SAMUEL G. SOLOMON ◽  
JONATHAN W. PEIRCE ◽  
ANDREW B. METHA

The preferred stimulus size of a V1 neuron decreases with increases in stimulus contrast. It has been supposed that stimulus contrast is the primary determinant of such spatial summation in V1 cells, though the extent to which it depends on other stimulus attributes such as orientation and spatial frequency remains untested. We investigated this by recording from single cells in V1 of anaesthetized cats and monkeys, measuring size-tuning curves for high-contrast drifting gratings of optimal spatial configuration, and comparing these curves with those obtained at lower contrast or at sub-optimal orientations or spatial frequencies. For drifting gratings of optimal spatial configuration, lower contrasts produced less surround suppression resulting in increases in preferred size. High contrast gratings of sub-optimal spatial configuration produced more surround suppression than optimal low-contrast gratings, and as much or more surround suppression than optimal high-contrast gratings. For sub-optimal spatial frequencies, preferred size was similar to that for the optimal high-contrast stimulus, whereas for sub-optimal orientations, preferred size was smaller than that for the optimal high-contrast stimulus. These results indicate that, while contrast is an important determinant of spatial summation in V1, it is not the only determinant. Simulation of these experiments on a cortical receptive field modeled as a Gabor revealed that the small preferred sizes observed for non-preferred stimuli could result simply from linear filtering by the classical receptive field. Further simulations show that surround suppression in retinal ganglion cells and LGN cells can be propagated to neurons in V1, though certain properties of the surround seen in cortex indicate that it is not solely inherited from earlier stages of processing.


2011 ◽  
Vol 23 (12) ◽  
pp. 3829-3840 ◽  
Author(s):  
Navid G. Sadeghi ◽  
Vani Pariyadath ◽  
Sameer Apte ◽  
David M. Eagleman ◽  
Erik P. Cook

How does the brain represent the passage of time at the subsecond scale? Although different conceptual models for time perception have been proposed, its neurophysiological basis remains unknown. We took advantage of a visual duration illusion produced by stimulus novelty to link changes in cortical activity in monkeys with distortions of duration perception in humans. We found that human subjects perceived the duration of a subsecond motion pulse with a novel direction longer than a motion pulse with a repeated direction. Recording from monkeys viewing identical motion stimuli but performing a different behavioral task, we found that both the duration and amplitude of the neural response in the middle temporal area of visual cortex were positively correlated with the degree of novelty of the motion direction. In contrast to previous accounts that attribute distortions in duration perception to changes in the speed of a putative internal clock, our results suggest that the known adaptive properties of neural activity in visual cortex contributes to subsecond temporal distortions.


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