Temporal properties of spatial frequency tuning of surround suppression in the primary visual cortex and the lateral geniculate nucleus of the cat

In primary visual cortex (V1) neurons, a stimulus placed in the extraclassical receptive field suppresses the response to a stimulus within the classical receptive field (CRF), a phenomenon referred to as surround suppression. The aim of the present study was to elucidate the mechanisms of surround suppression in V1. Using stationary‐flashed sinusoidal grating as stimuli, we observed temporal changes of surround suppression in V1 and the lateral geniculate nucleus (LGN) and of the response to CRF stimulation in V1. The spatial frequency (SF) tuning of surround suppression in V1 neurons changed over time after the stimulus onset. In the early phase (< 50 ms), the SF tuning was low‐pass, but later became band‐pass that tuned to the optimal SF in response to CRF stimulation. On the other hand, the SF tuning of CRF responses in V1 was band‐pass throughout the response time whereas the SF peak shifted slightly toward high SF. Thus, SF tuning properties of the CRF response dissociated from that of surround suppression in V1 only in the early phase. We also confirmed that the temporal changes of the SF tuning of surround suppression in the LGN occurred in the same direction as surround suppression in V1, but the shift from low‐pass to band‐pass SF tuning started later than that in V1. From these results, we suggest that subcortical mechanisms contribute to early surround suppression in V1, whereas cortical mechanisms contribute to late surround suppression.     

Surround suppression sharpens orientation tuning in the cat primary visual cortex

In the primary visual cortex (V1), the response of a neuron to stimulation of its classical receptive field (CRF) is suppressed by concurrent stimulation of the extraclassical receptive field (ECRF), a phenomenon termed 'surround suppression'. It is also known that the orientation tuning of V1 neurons becomes sharper as the size of the stimulus increases beyond the CRF. However, there have been few quantitative investigations of the relationship between sharpening of orientation tuning and surround suppression. We examined this relationship in 73 V1 neurons recorded from anesthetized and paralysed cats using sinusoidal grating patches as stimuli. We found that sharpening of orientation tuning was significantly correlated with the strength of surround suppression for large stimuli that cover both CRF and ECRF. Furthermore, simulation analysis using a variety of tuning widths and most suppressive orientation of orientation-tuned surround suppression demonstrated that broadly orientation-tuned surround suppression sharpens orientation tuning for large gratings without shift in optimal orientation. Our findings suggest that one of the functional roles of surround suppression in V1 is enhancement of orientation discrimination for large and uniformly patterned objects.     

Distinct mechanisms for size tuning in primate visual cortex

Most neurons in primary visual cortex (V1) are selective for stimulus size, a property with important implications for salient feature detection. Size selectivity involves dynamic interactions between neuronal circuits that establish the classical (center) and extraclassical (surround) of a neuron's receptive field. Although much is known about the tuning properties and stimulus selectivity of the center and surround subunits, relatively little is known about how these subunits interact to achieve size selectivity. To address this question, we examined the temporal dynamics of size selectivity in two classes of pyramidal neurons at similar hierarchical processing stages in V1 of alert monkeys. These two classes were comprised of neurons in cortical layer 6 with identified projections to the lateral geniculate nucleus. While both neuronal groups displayed comparable levels of size selectivity, the temporal dynamics of their tuning differed significantly. We compared the size tuning profiles of each cell type with a series of sum-of-Gaussian models and discovered that the receptive fields of neurons with fast-conducting axons contained an excitatory center and a suppressive surround with similar onset timing. In contrast, neurons with slow-conducting axons used two center components-an early wide-field component and a delayed narrow-field component that increased activity-in addition to the surround component. The early, wide-field component represents a novel mechanism for cortical neurons to integrate contextual information. These results demonstrate that size tuning in cortical neurons is established via multiple unique mechanisms, dictated by the rich circuit architecture in which neurons are embedded.     

Spike synchronization in cat primary visual cortex depends on similarity of surround‐suppression magnitude

In the primary visual cortex (V1), the spike synchronization seen in neuron pairs with non‐overlapping receptive fields can be explained by similarities in their preferred orientation (PO). However, this is not true for pairs with overlapping receptive fields, as they can still exhibit spike synchronization even if their POs are only weakly correlated. Here, we investigated the relationship between spike synchronization and suppressive modulation derived from classical receptive‐field surround (surround suppression). We found that layer 4 and layer 2/3 pairs exhibited mainly asymmetric spike synchronization that had non‐zero time‐lags and was dependent on both the similarity of the PO and the strength of surround suppression. In contrast, layer 2/3 and layer 2/3 pairs showed mainly symmetric spike synchronization that had zero time‐lag and was dependent on the similarity of the strength of surround suppression but not on the similarity in POs. From these results, we propose that in cat V1 there exists a functional network that mainly depends on the similarity in surround suppression, and that in layer 2/3 neurons the network maintains surround suppression that is primarily inherited from layer 4 neurons.     

A model of surround suppression through cortical feedback.

Surround suppression occurs when a visual stimulus outside a neuron's classical receptive field causes a reduction in firing rate. It has become clear that several mechanisms are working together to induce center-surround effects such as surround suppression. While several models exist that rely on lateral connections within V1 to explain surround suppression, few have been proposed that show how cortical feedback might play a role. In this work, we propose a theory in which reductions in excitatory feedback contribute to a neuron's suppressed firing rate. We also provide a computational model that incorporates this idea.     

Contrast-dependent, contextual response modulation in primary visual cortex and lateral geniculate nucleus of the cat

In the primary visual cortex (V1), the responses of neurons to stimuli presented in their classical receptive fields (CRFs) are modulated by another stimulus concurrently presented in their surround (receptive field surround, SRF). We studied the nature of the modulatory effects of SRF stimulation with respect to stimulus contrast in cat V1. In 51 V1 neurons studied, large SRF stimuli (40 degreesx30 degrees ) induced only the suppression of responses to CRF stimulation and the suppressive effects became stronger as the contrast for SRF stimulation increased. The contrast sensitivity of SRF suppression did not correlate with that of CRF responses. By independently controlling contrast of CRF and SRF stimuli, we studied whether SRF effects vary with CRF response magnitude. Increasing contrast for CRF stimulation caused an upward shift of the range of effective contrasts for SRF stimulation, indicating that a high contrast for SRF stimulation is required for suppressing strong responses to CRF stimulation at high contrasts. To assess the possible origin of the suppressive SRF effect on V1 neurons, we also investigated the contrast dependency of SRF effects in 28 neurons from the lateral geniculate nucleus. Our results suggest that SRF effects obtained at the subcortical level strongly contribute to those in V1. Taken together, we conclude that along the thalamocortical projections, SRF modulation exhibits a gain-control mechanism that scales the suppressive SRF effect depending on the contrast for CRF stimulation. In addition, SRF effects can be facilitatory at low stimulus contrasts potentially due to the enlargement of the summation field.     

Differential Effects of Endogenous and Exogenous Attention on Sensory Tuning

Covert spatial attention (without concurrent eye movements) improves performance in many visual tasks (e.g., orientation discrimination and visual search). However, both covert attention systems—endogenous (voluntary) and exogenous (involuntary)—exhibit differential effects on performance in tasks mediated by spatial and temporal resolution suggesting an underlying mechanistic difference. We investigated whether these differences manifest in sensory tuning by assessing whether and how endogenous and exogenous attention differentially alter the representation of two basic visual dimensions—orientation and spatial frequency (SF). The same human observers detected a grating embedded in noise in two separate experiments (with endogenous or exogenous attention cues). Reverse correlation was used to infer the underlying neural representation from behavioral responses, and we linked our results to established neural computations via a normalization model of attention. Both endogenous and exogenous attention similarly improved performance at the attended location by enhancing the gain of all orientations without changing tuning width. In the SF dimension, endogenous attention enhanced the gain of SFs above and below the target SF, whereas exogenous attention only enhanced those above. Additionally, exogenous attention shifted peak sensitivity to SFs above the target SF, whereas endogenous attention did not. Both covert attention systems modulated sensory tuning via the same computation (gain changes). However, there were differences in the strength of the gain. Compared with endogenous attention, exogenous attention had a stronger orientation gain enhancement but a weaker overall SF gain enhancement. These differences in sensory tuning may underlie differential effects of endogenous and exogenous attention on performance.SIGNIFICANCE STATEMENT Covert spatial attention is a fundamental aspect of cognition and perception that allows us to selectively process and prioritize incoming visual information at a given location. There are two types: endogenous (voluntary) and exogenous (involuntary). Both typically improve visual perception, but there are instances where endogenous improves perception but exogenous hinders perception. Whether and how such differences extend to sensory representations is unknown. Here we show that both endogenous and exogenous attention mediate perception via the same neural computation—gain changes—but the strength of the orientation gain and the range of enhanced spatial frequencies depends on the type of attention being deployed. These findings reveal that both attention systems differentially reshape the tuning of features coded in striate cortex.     

Distinct functional properties of primary and posteromedial visual area of mouse neocortex

Visual input provides important landmarks for navigating in the environment, information that in mammals is processed by specialized areas in the visual cortex. In rodents, the posteromedial area (PM) mediates visual information between primary visual cortex (V1) and the retrosplenial cortex, which further projects to the hippocampus. To understand the functional role of area PM requires a detailed analysis of its spatial frequency (SF) and temporal frequency (TF) tuning. Here, we applied two-photon calcium imaging to map neuronal tuning for orientation, direction, SF and TF, and speed in response to drifting gratings in V1 and PM of anesthetized mice. The distributions of orientation and direction tuning were similar in V1 and PM. Notably, in both areas we found a preference for cardinal compared to oblique orientations. The overrepresentation of cardinal tuned neurons was particularly strong in PM showing narrow tuning bandwidths for horizontal and vertical orientations. A detailed analysis of SF and TF tuning revealed a broad range of highly tuned neurons in V1. On the contrary, PM contained one subpopulation of neurons with high spatial acuity and a second subpopulation broadly tuned for low SFs. Furthermore, ～20% of the responding neurons in V1 and only 12% in PM were tuned to the speed of drifting gratings with PM preferring slower drift rates compared to V1. Together, PM is tuned for cardinal orientations, high SFs, and low speed and is further located between V1 and the retrosplenial cortex consistent with a role in processing natural scenes during spatial navigation.     

Strong recurrent networks compute the orientation tuning of surround modulation in the primate primary visual cortex

In macaque primary visual cortex (V1), neuronal responses to stimuli inside the receptive field (RF) are modulated by stimuli in the RF surround. This modulation is orientation specific. Previous studies suggested that, for some cells, this specificity may not be fixed but changes with the stimulus orientation presented to the RF. We demonstrate, in recording studies, that this tuning behavior is instead highly prevalent in V1 and, in theoretical work, that it arises only if V1 operates in a regime of strong local recurrence. Strongest surround suppression occurs when the stimuli in the RF and the surround are iso-oriented, and strongest facilitation when the stimuli are cross-oriented. This is the case even when the RF is suboptimally activated by a stimulus of nonpreferred orientation but only if this stimulus can activate the cell when presented alone. This tuning behavior emerges from the interaction of lateral inhibition (via the surround pathways), which is tuned to the preferred orientation of the RF, with weakly tuned, but strong, local recurrent connections, causing maximal withdrawal of recurrent excitation at the feedforward input orientation. Thus, horizontal and feedback modulation of strong recurrent circuits allows the tuning of contextual effects to change with changing feedforward inputs.     

Spatial and temporal frequency tuning in striate cortex: functional uniformity and specializations related to receptive field eccentricity

In light of anatomical evidence suggesting differential connection patterns in central vs. peripheral representations of cortical areas, we investigated the extent to which the response properties of cells in the primary visual area (V1) of the marmoset change as a function of eccentricity. Responses to combinations of the spatial and temporal frequencies of visual stimuli were quantified for neurons with receptive fields ranging from 3° to 70° eccentricity. Optimal spatial frequencies and stimulus speeds reflected the expectation that the responses of cells throughout V1 are essentially uniform, once scaled according to the cortical magnification factor. In addition, temporal frequency tuning was similar throughout V1. However, spatial frequency tuning curves depended both on the cell’s optimal spatial frequency and on the receptive field eccentricity: cells with peripheral receptive fields showed narrower bandwidths than cells with central receptive fields that were sensitive to the same optimal spatial frequency. Although most V1 cells had separable spatial and temporal frequency tuning, the proportion of neurons displaying significant spatiotemporal interactions increased in the representation of far peripheral vision (> 50°). In addition, of the fewer than 5% of V1 cells that showed robust (spatial frequency independent) selectivity to stimulus speed, most were concentrated in the representation of the far periphery. Spatiotemporal interactions in the responses of many cells in the peripheral representation of V1 reduced the ambiguity of responses to high‐speed (> 30°/s) signals. These results support the notion of a relative specialization for motion processing in the far peripheral representations of cortical areas, including V1.     

Stimulus Contrast Affects Spatial Integration in the Lateral Geniculate Nucleus of Macaque Monkeys

Gain-control mechanisms adjust neuronal responses to accommodate the wide range of stimulus conditions in the natural environment. Contrast gain control and extraclassical surround suppression are two manifestations of gain control that govern the responses of neurons in the early visual system. Understanding how these two forms of gain control interact has important implications for the detection and discrimination of stimuli across a range of contrast conditions. Here, we report that stimulus contrast affects spatial integration in the lateral geniculate nucleus of alert macaque monkeys (male and female), whereby neurons exhibit a reduction in the strength of extraclassical surround suppression and an expansion in the preferred stimulus size with low-contrast stimuli compared with high-contrast stimuli. Effects were greater for magnocellular neurons than for parvocellular neurons, indicating stream-specific interactions between stimulus contrast and stimulus size. Within the magnocellular pathway, contrast-dependent effects were comparable for ON-center and OFF-center neurons, despite ON neurons having larger receptive fields, less pronounced surround suppression, and more pronounced contrast gain control than OFF neurons. Together, these findings suggest that the parallel streams delivering visual information from retina to primary visual cortex, serve not only to broaden the range of signals delivered to cortex, but also to provide a substrate for differential interactions between stimulus contrast and stimulus size that may serve to improve stimulus detection and stimulus discrimination under pathway-specific lower and higher contrast conditions, respectively.SIGNIFICANCE STATEMENT Stimulus contrast is a salient feature of visual scenes. Here we examine the influence of stimulus contrast on spatial integration in the lateral geniculate nucleus (LGN). Our results demonstrate that increases in contrast generally increase extraclassical suppression and decrease the size of optimal stimuli, indicating a reduction in the extent of visual space from which LGN neurons integrate signals. Differences between magnocellular and parvocellular neurons are noteworthy and further demonstrate that the feedforward parallel pathways to cortex increase the range of information conveyed for downstream cortical processing, a range broadened by diversity in the ON and OFF pathways. These results have important implications for more complex visual processing that underly the detection and discrimination of stimuli under varying natural conditions.     

Attention and normalization circuits in macaque V1

Attention affects neuronal processing and improves behavioural performance. In extrastriate visual cortex these effects have been explained by normalization models, which assume that attention influences the circuit that mediates surround suppression. While normalization models have been able to explain attentional effects, their validity has rarely been tested against alternative models. Here we investigate how attention and surround/mask stimuli affect neuronal firing rates and orientation tuning in macaque V1. Surround/mask stimuli provide an estimate to what extent V1 neurons are affected by normalization, which was compared against effects of spatial top down attention. For some attention/surround effect comparisons, the strength of attentional modulation was correlated with the strength of surround modulation, suggesting that attention and surround/mask stimulation (i.e. normalization) might use a common mechanism. To explore this in detail, we fitted multiplicative and additive models of attention to our data. In one class of models, attention contributed to normalization mechanisms, whereas in a different class of models it did not. Model selection based on Akaike's and on Bayesian information criteria demonstrated that in most cells the effects of attention were best described by models where attention did not contribute to normalization mechanisms. This demonstrates that attentional influences on neuronal responses in primary visual cortex often bypass normalization mechanisms.     

Comparison of spatial integration and surround suppression characteristics in spiking activity and the local field potential in macaque V1

Neurons in primary visual cortex exhibit well documented centre–surround receptive field organization, whereby the centre is dominated by excitatory influences and the surround is generally dominated by inhibitory influences. These effects have largely been established by measuring the output of neurons, i.e. their spiking activity. How excitation and inhibition are reflected in the local field potential (LFP) is little understood. As this can bear on the interpretation of human fMRI BOLD data and on our understanding of the mechanisms of local field potential oscillations, we measured spatial integration and centre–surround properties in single- and multiunit recordings of V1 in the awake fixating macaque monkey, and compared these to spectral power in different frequency bands of simultaneously recorded LFPs. We quantified centre–surround organization by determining the size of the summation and suppression area in spiking activity as well as in different frequency bands of the LFP, with the main focus on the gamma band. Gratings extending beyond the summation area usually inhibited spiking activity while the LFP gamma-band activity increased monotonically for all grating sizes. This increase was maximal for stimuli infringing upon the near classical receptive field surround, where suppression started to dominate spiking activity. Thus, suppressive influences in primary cortex can be inferred from spiking activity, but they also seem to affect specific features of gamma-band LFP activity.     

Receptive‐field properties of V1 and V2 neurons in mice and macaque monkeys

We report the results of extracellular single‐unit recording experiments where we quantitatively analyzed the receptive‐field (RF) properties of neurons in V1 and an adjacent extrastriate visual area (V2L) of anesthetized mice with emphasis on the RF center‐surround organization. We compared the results with the RF center‐surround organization of V1 and V2 neurons in macaque monkeys. If species differences in spatial scale are taken into consideration, mouse V1 and V2L neurons had remarkably fine stimulus selectivity, and the majority of response properties in V2L were not different from those in V1. The RF center‐surround organization of mouse V1 neurons was qualitatively similar to that for macaque monkeys (i.e., the RF center is surrounded by extended suppressive regions). However, unlike in monkey V2, a significant proportion of cortical neurons, largely complex cells in V2L, did not exhibit quantifiable RF surround suppression. Simple cells had smaller RF centers than complex cells, and the prevalence and strength of surround suppression were greater in simple cells than in complex cells. These findings, particularly on the RF center‐surround organization of visual cortical neurons, give new insights into the principles governing cortical circuits in the mouse visual cortex and should provide further impetus for the use of mice in studies on the genetic and molecular basis of RF development and synaptic plasticity. J. Comp. Neurol. 518:2051–2070, 2010. © 2010 Wiley‐Liss, Inc.     

Asymmetric suppression outside the classical receptive field of the visual cortex.

Areas beyond the classical receptive field (CRF) can modulate responses of the majority of cells in the primary visual cortex of the cat (). Although general characteristics of this phenomenon have been reported previously, little is known about the detailed spatial organization of the surrounds. Previous work suggests that the surrounds may be uniform regions that encircle the CRF or may be limited to the "ends" of the CRF. We have examined the spatial organization of surrounds of single-cell receptive fields in the primary visual cortex of anesthetized, paralyzed cats. The CRF was stimulated with an optimal drifting grating, whereas the surround was probed with a second small grating patch placed at discrete locations around the CRF. For most cells that exhibit suppression, the surrounds are spatially asymmetric, such that the suppression originates from a localized region. We find a variety of suppressive zone locations, but there is a slight bias for suppression to occur at the end zones of the CRF. The spatial pattern of suppression is independent of the parameters of the suppressive stimulus used, although the effect is clearest with iso-oriented surround stimuli. A subset of cells exhibit axially symmetric or uniform surround fields. These results demonstrate that the surrounds are more specific than previously realized, and this specialization has implications for the processing of visual information in the primary visual cortex. One possibility is that these localized surrounds may provide a substrate for figure-ground segmentation of visual scenes.     

Contribution of feedforward thalamic afferents and corticogeniculate feedback to the spatial summation area of macaque V1 and LGN

Neurons in the primary visual cortex (V1) respond best to oriented gratings of optimal size within their receptive field (RF) and are suppressed by larger gratings involving the nonclassical RF surround. A V1 neuron's optimal stimulus size is larger at lower stimulus contrast. A central question in visual neuroscience is what circuits generate the size tuning of V1 cells. We recently demonstrated that V1 horizontal connections integrate signals within a region of the RF center corresponding to the V1 neuron's optimal stimulus size at low contrast; extrastriate feedback connections to V1, instead, are longer range and can integrate signals from the most distant regions of the V1 cell's RF surround. Here, we have determined the contribution of geniculocortical feedforward and corticogeniculate feedback connections to the size-tuning of macaque V1 and lateral geniculate (LGN) neurons, respectively. Specifically, we have quantitatively compared the visuotopic extent of geniculate feedforward afferents to V1 with the size of the RF center and surround of neurons in the V1 input layers and the visuotopic extent of V1 feedback connections to the LGN with the RF size of cells in V1 layer 6, where these connections originate. We find geniculate feedforward connections to provide visuotopic information to V1 that is spatially coextensive with the V1 neuron's optimal stimulus size measured with high-contrast gratings. V1 feedback connections restrict their influence to an LGN region visuotopically coextensive with the size of the minimum response field (or classical RF) of V1 layer 6 cells and commensurate with the LGN region from which they receive feedforward connections.     

Spectral properties of V4 neurons in the macaque

Spectral properties of 129 cells in the V4 area of 5 macaque monkeys were studied quantitatively with narrow-band and broad-band colored lights. The large majority of cells exhibited some degree of wavelength sensitivity within their receptive fields. The half-bandwidth of the primary peak in the spectral-response curve was less than 50 nm for 72% of the cells; the mean half-bandwidth of these cells, 27 nm, is similar to that found for color-opponent ganglion cells and cells in the parvocellular dorsal lateral geniculate nucleus (dLGN). Contrast-response functions indicated that the narrow spectral tuning of these cells derived from cone opponent interactions. From comparison of receptive-field sizes, we suggest that a typical V4 neuron sums inputs that ultimately derive from several thousand ganglion or parvocellular dLGN cells. In spite of their wavelength sensitivity, most V4 cells had properties that would not fit some simple criteria for classification as "color selective." First, few cells showed overt signs of color opponency, namely, on-inhibition or off-excitation to spectrally opponent wavelengths. Second, about 30% of the cells in V4 had spectral-response curves with 2 peaks. (The wavelength distribution of these second peaks was almost identical to that of primary peaks, and combinations of peak wavelengths were fairly random.) Third, most cells responded to white light; overall, the response to white light was about 60% of that to the best narrow-band or broad-band colored light. Similarly, most V4 cells gave at least a small response to all or nearly all of the different broad-band colored lights we presented. Therefore, a given V4 cell is very likely to respond to most of the colored or white surfaces in natural scenes. These combinations of response properties probably explain the widely divergent percentages of "color" cells reported in previous studies of V4. The most unusual spectral property we found in V4 was a large, spectrally sensitive surround outside the "classical receptive field" of most cells. Although stimulation of the surround by itself did not cause any response, surround stimulation could completely suppress the response to even the optimally colored stimulus in the receptive field. In general, the optimal wavelengths for receptive-field excitation and surround suppression were the same or nearly so. Thus, "color contrast" may be computed in V4. In some cases, contrasting wavelengths in the surround caused moderate enhancement of response to a receptive-field stimulus.(ABSTRACT TRUNCATED AT 400 WORDS)     

Spatio-temporal prediction and inference by V1 neurons

In normal vision, visual scenes are predictable, as they are both spatially and temporally redundant. Evidence suggests that the visual system may use the spatio-temporal regularities of the external world, available in the retinal signal, to extract information from the visual environment and better reconstruct current and future stimuli. We studied this by recording neuronal responses of primary visual cortex (area V1) in anaesthetized and paralysed macaques during the presentation of dynamic sequences of bars, in which spatio-temporal regularities and local information were independently manipulated. Most V1 neurons were significantly modulated by events prior to and distant from stimulation of their classical receptive fields (CRFs); many were more strongly tuned to prior and distant events than they were to CRFs bars; and several showed tuning to prior information without any CRF stimulation. Hence, V1 neurons do not simply analyse local contours, but impute local features to the visual world, on the basis of prior knowledge of a visual world in which useful information can be distributed widely in space and time.     

The contribution of vertical and horizontal connections to the receptive field center and surround in V1.

Here we review the results of anatomical and physiological studies in tree shrew visual cortex which focus on the contribution of vertical and horizontal inputs to receptive field center and surround properties of layer 2/3 neurons. A fundamental feature of both sets of connections is the arrangement of axon arbors in a fashion that respects both the orientation preference and retinotopic displacement of the target site. As a result, layer 2/3 neurons receive convergent input from populations of layer 4 and other layer 2/3 neurons whose receptive fields are displaced along an axis in visual space that corresponds to their preferred orientation. Although, horizontal connections extend for greater distances across the cortical surface than vertical connections, the majority of these inputs link neurons with overlapping receptive fields, emphasizing that both feed-forward and recurrent circuits are likely to play a constructive role in generating properties (such as orientation selectivity) that define the receptive field center. Both within and beyond the dimensions of the receptive field center, the distribution of horizontal connections accords remarkably well with the magnitude and axial tuning of length summation effects. Taken together, these results suggest a continuum of functional properties that transcends the traditional designation of receptive field center and surround. By extension, we suggest that the perceptual effects of stimulus context may arise from stimulus interactions within the receptive field center as well as between center and surround.     

Transient enhancement of inhibition following visual cortical lesions in the mouse superior colliculus

Numerous studies have investigated the effects of lesions of the primary visual cortex (V1) on visual responses in neurons of the superficial layer of the superior colliculus (sSC), which receives visual information from both the retina and V1. However, little is known about the changes in the local circuit dynamics of the sSC after receiving V1 lesions. Here, we show that surround inhibition of sSC neurons is transiently enhanced following V1 lesions in mice and that this enhancement may be attributed to alterations in the balance between excitatory and inhibitory inputs to sSC neurons. Extracellular recordings in vivo revealed that sSC neuronal responses to large visual stimuli were transiently reduced at about 1 week after visual cortical lesions compared with normal mice and that this reduction was partially recovered at about 1 month after the lesions. By using whole‐cell patch‐clamp recordings from sSC neurons in slice preparations obtained from mice that had received visual cortical lesions at 1 week prior to the recordings, we found cell type‐dependent changes in the balance between excitation and inhibition. In non‐GABAergic cells, inhibition predominated over excitation, whereas the excitation–inhibition balance did not change in GABAergic neurons. These results suggest that enhanced inhibition may be partially responsible for the reduced responses to large visual stimuli in some sSC neurons. Thus, we propose that the enhanced surround inhibition shortly after visual cortical lesions may prevent hyperexcitability in the sSC local circuit, contributing to reconstructing the finely tuned receptive field organization of sSC neurons after the visual cortical lesions.