Temporal properties of surround suppression in cat primary visual cortex

2007 ◽  
Vol 24 (5) ◽  
pp. 679-690 ◽  
Author(s):  
SÉVERINE DURAND ◽  
TOBE C.B. FREEMAN ◽  
MATTEO CARANDINI

The responses of neurons in primary visual cortex (V1) are suppressed by stimuli presented in the region surrounding the receptive field. There is debate as to whether this surround suppression is due to intracortical inhibition, is inherited from lateral geniculate nucleus (LGN), or is due to a combination of these factors. The mechanisms involved in surround suppression may differ from those involved in suppression within the receptive field, which is called cross-orientation suppression. To compare surround suppression to cross-orientation suppression, and to help elucidate its underlying mechanisms, we studied its temporal properties in anesthetized and paralyzed cats. We first measured the temporal resolution of suppression. While cat LGN neurons respond vigorously to drift rates up to 30 Hz, most cat V1 neurons stop responding above 10–15 Hz. If suppression originated in cortical responses, therefore, it should disappear above such drift rates. In a majority of cells, surround suppression decreased substantially when surround drift rate was above ∼15 Hz, but some neurons demonstrated suppression with surround drift rates as high as 21 Hz. We then measured the susceptibility of suppression to contrast adaptation. Contrast adaptation reduces responses of cortical neurons much more than those of LGN neurons. If suppression originated in cortical responses, therefore, it should be reduced by adaptation. Consistent with this hypothesis, we found that prolonged exposure to the surround stimulus decreased the strength of surround suppression. The results of both experiments differ markedly from those previously obtained in a study of cross-orientation suppression, whose temporal properties were found to resemble those of LGN neurons. Our results provide further evidence that these two forms of suppression are due to different mechanisms. Surround suppression can be explained by a mixture of thalamic and cortical influences. It could also arise entirely from intracortical inhibition, but only if inhibitory neurons respond to somewhat higher drift rates than most cortical cells.

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.


2017 ◽  
Author(s):  
Jingyang Zhou ◽  
Noah C. Benson ◽  
Kendrick Kay ◽  
Jonathan Winawer

AbstractNeuronal responses in visual cortex show a diversity of complex temporal properties. These properties include sub-additive temporal summation, response reduction with repeated or sustained stimuli (adaptation), and slower dynamics at low stimulus contrast. Here, we hypothesize that these seemingly disparate effects can be explained by a single, shared computational mechanism. We propose a model consisting of a linear stage, followed by history-dependent gain control. The model accounts for these various temporal phenomena, tested against an unusually diverse set of measurements - intracranial electrodes in patients, fMRI, and macaque single unit spiking. The model further enables us to uncover a systematic and rich variety of temporal encoding strategies across visual cortex: First, temporal receptive field shape differs both across and within visual field maps. Second, later visual areas show more rapid and pronounced adaptation. Our study provides a new framework to understand the transformation between visual input and dynamical cortical responses.Author SummaryThe nervous system extracts meaning from the distribution of light over space and time. Spatial vision has been a highly successful research area, and the spatial receptive field has served as a fundamental and unifying concept that spans perception, computation, and physiology. While there has also been a large interest in temporal vision, the temporal domain has lagged the spatial domain in terms of quantitative models of how signals are transformed across the visual hierarchy. Here we present a model of temporal dynamics of neuronal responses in human cerebral cortex. We show that the model can accurately predict responses at the millisecond scale using intracortical electrodes in patient volunteers, and that the same model generalizes to multiple types of other measurements, including functional MRI and action potentials from monkey cortex. Further, we show that a single model can account for a variety of temporal phenomena, including short-term adaptation and slower dynamics at low stimulus contrast. By developing a computational model and showing that it successfully generalizes across measurement types, cortical areas, and stimuli, we provide new insights into how time-varying images are encoded and transformed into dynamic cortical responses.


2012 ◽  
Vol 108 (5) ◽  
pp. 1381-1391 ◽  
Author(s):  
Aaron C. Stroud ◽  
Emily E. LeDue ◽  
Nathan A. Crowder

Contrast adaptation is a commonly studied phenomenon in vision, where prolonged exposure to spatial contrast alters perceived stimulus contrast and produces characteristic shifts in the contrast response functions of primary visual cortex neurons in cats and primates. In this study we investigated contrast adaptation in mouse primary visual cortex with two goals in mind. First, we sought to establish a quantitative description of contrast adaptation in an animal model, where genetic tools are more readily applicable to this phenomenon. Second, the orientation specificity of contrast adaptation was studied to comparatively assess the possible role of local cortical networks in contrast adaptation. In cats and primates, predictable differences in visual processing across the cortical surface are thought to be caused by inhomogeneous local network membership that arises from the pinwheel organization of orientation columns. Because mice lack this pinwheel organization, we predicted that local cortical networks would have access to a broad spectrum of orientation signals, and contrast adaptation in mice would not be specific to the recorded cell's preferred orientation. We found that most mouse V1 neurons showed contrast adaptation that was robust regardless of whether the adapting stimulus matched the cell's preferred orientation or was orthogonal to it.


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.


2014 ◽  
Vol 112 (3) ◽  
pp. 603-619 ◽  
Author(s):  
Satoshi Shimegi ◽  
Ayako Ishikawa ◽  
Hiroyuki Kida ◽  
Hiroshi Sakamoto ◽  
Sin-ichiro Hara ◽  
...  

In the primary visual cortex (V1), a neuronal response to stimulation of the classical receptive field (CRF) is predominantly suppressed by a stimulus presented outside the CRF (extraclassical receptive field, ECRF), a phenomenon referred to as ECRF suppression. To elucidate the neuronal mechanisms and origin of ECRF suppression in V1 of anesthetized cats, we examined the temporal properties of the spatial extent and orientation specificity of ECRF suppression in V1 and the lateral geniculate nucleus (LGN), using stationary-flashed sinusoidal grating. In V1, we found three components of ECRF suppression: 1) local and fast, 2) global and fast, and 3) global and late. The local and fast component, which resulted from within 2° of the boundary of the CRF, started no more than 10 ms after the onset of the CRF response and exhibited low specificity for the orientation of the ECRF stimulus. These spatiotemporal properties corresponded to those of geniculate ECRF suppression, suggesting that the local and fast component of V1 is inherited from the LGN. In contrast, the two global components showed rather large spatial extents ∼5° from the CRF boundary and high specificity for orientation, suggesting that their possible origin is the cortex, not the LGN. Correspondingly, the local component was observed in all neurons of the thalamocortical recipient layer, while the global component was biased toward other layers. Therefore, we conclude that both subcortical and cortical mechanisms with different spatiotemporal properties are involved in ECRF suppression.


1993 ◽  
Vol 10 (6) ◽  
pp. 1129-1139 ◽  
Author(s):  
John D. Allison ◽  
Vivien A. Casagrande ◽  
Edward J. Debruyn ◽  
A. B. Bonds

AbstractIt has been argued that in order for the visual system to detect edges accurately under a range of conditions, the visual system needs to adapt to the local contrast level to preserve sensitivity (Blakemore & Campbell, 1969). Cells in the primary visual cortex of cats adapt to stimuli with low to moderate contrast. Curiously, macaque monkey neurons in primary visual cortex (V1) do not show evidence for similar adaptation. To address the question of whether this differential sensitivity in contrast adaptation might be due to phylogenetic variation between cats and primates or to specializations for visual niche (e.g. nocturnal vs. diurnal), contrast adaptation to temporally and spatially optimized gratings was examined in 30 V1 cells of three nocturnal primate bush babies (Galago crassicaudatus). A second objective was to examine the relationship between the degree of contrast adaptation and cell classification or cell location relative to cortical layers or compartments [i.e. cytochrome-oxidase (CO) blobs and interblobs]. All cells were classified (simple vs. complex) and anatomically localized relative to cortical layers and cytochrome-oxidase (CO) blob and interblob compartments. Two independent measures of contrast adaptation were used. In the first test, contrast was sequentially increased from 3–56% and then decreased. The contrast required to maintain a half-maximum response amplitude in the 30 cells tested increased an average of 0.24 (±0.12) log units during the sequential decrements in contrast. For the second test, four sets of five interleaved contrasts within ±1 octave of a central adapting contrast (10%, 14%, 20%, and 28%, respectively) were presented. The cells produced a mean adaptation index of 0.57 (±0.47) which is very similar to that exhibited by cat cortical neurons (0.54 ± 0.41). Interestingly, cells in interblobs showed a trend toward greater adaptation than did blob cells. Moreover, cells in the supragranular layers exhibited greater adaptation than cells in the infragranular layers. No significant differences in adaptation were found to correlate with other cell classification indices. Taken together, our results suggest that contrast adaptation may be more important for maintaining sensitivity in nocturnal species (primates or cats) than in diurnal species (macaque monkeys), and that in the nocturnal bush baby, cells in cortical layers and compartments may be differentially specialized for contrast adaptation.


2000 ◽  
Vol 83 (2) ◽  
pp. 1019-1030 ◽  
Author(s):  
Valentin Dragoi ◽  
Mriganka Sur

A fundamental feature of neural circuitry in the primary visual cortex (V1) is the existence of recurrent excitatory connections between spiny neurons, recurrent inhibitory connections between smooth neurons, and local connections between excitatory and inhibitory neurons. We modeled the dynamic behavior of intermixed excitatory and inhibitory populations of cells in V1 that receive input from the classical receptive field (the receptive field center) through feedforward thalamocortical afferents, as well as input from outside the classical receptive field (the receptive field surround) via long-range intracortical connections. A counterintuitive result is that the response of oriented cells can be facilitated beyond optimal levels when the surround stimulus is cross-oriented with respect to the center and suppressed when the surround stimulus is iso-oriented. This effect is primarily due to changes in recurrent inhibition within a local circuit. Cross-oriented surround stimulation leads to a reduction of presynaptic inhibition and a supraoptimal response, whereas iso-oriented surround stimulation has the opposite effect. This mechanism is used to explain the orientation and contrast dependence of contextual interactions in primary visual cortex: responses to a center stimulus can be both strongly suppressed and supraoptimally facilitated as a function of surround orientation, and these effects diminish as stimulus contrast decreases.


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