Contrast Dependence of Response Normalization in Area MT of the Rhesus Macaque

2002 ◽  
Vol 88 (6) ◽  
pp. 3398-3408 ◽  
Author(s):  
Hilary W. Heuer ◽  
Kenneth H. Britten

Contrast normalization is a process whereby responses of neurons are scaled according to the total amount of contrast in a region of the image nearby the receptive field of a neuron. This process allows neurons to code for informative scene or object attributes in a manner unaffected by changes in illumination. Evidence for normalization is seen in striate and extrastriate cortex from experiments where multiple stimuli are presented with a single receptive field (RF). Neuronal responses in such experiments are smaller than that predicted by linear summation, revealing the presence of normalization. While the presence of normalization is often clear, its mechanism is less so. To study the mechanism of normalization, we measured the interaction between pairs of brief local stimuli (spatial Gabor functions) within the RFs of cells in the middle temporal (MT or V5) area of monkeys and varied both the location and contrast of the stimuli. We found response summed approximately linearly when contrast was low but rapidly became normalized as stimulus contrast increased. The rapid transition to effective normalization at low contrasts suggested cooperativity in the normalization, and a model embodying such a cooperative step provided a good account of our data.

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.


2011 ◽  
Vol 106 (4) ◽  
pp. 1888-1900 ◽  
Author(s):  
James M. G. Tsui ◽  
Christopher C. Pack

Neurons throughout the visual system have receptive fields with both excitatory and suppressive components. The latter are responsible for a phenomenon known as surround suppression, in which responses decrease as a stimulus is extended beyond a certain size. Previous work has shown that surround suppression in the primary visual cortex depends strongly on stimulus contrast. Such complex center-surround interactions are thought to relate to a variety of functions, although little is known about how they affect responses in the extrastriate visual cortex. We have therefore examined the interaction of center and surround in the middle temporal (MT) area of the macaque ( Macaca mulatta) extrastriate cortex by recording neuronal responses to stimuli of different sizes and contrasts. Our findings indicate that surround suppression in MT is highly contrast dependent, with the strongest suppression emerging unexpectedly at intermediate stimulus contrasts. These results can be explained by a simple model that takes into account the nonlinear contrast sensitivity of the neurons that provide input to MT. The model also provides a qualitative link to previous reports of a topographic organization of area MT based on clusters of neurons with differing surround suppression strength. We show that this organization can be detected in the gamma-band local field potentials (LFPs) and that the model parameters can predict the contrast sensitivity of these LFP responses. Overall our results show that surround suppression in area MT is far more common than previously suspected, highlighting the potential functional importance of the accumulation of nonlinearities along the dorsal visual pathway.


1984 ◽  
Vol 52 (3) ◽  
pp. 488-513 ◽  
Author(s):  
D. J. Felleman ◽  
J. H. Kaas

Response properties of single neurons in the middle temporal visual area (MT) of anesthetized owl monkeys were determined and quantified for flashed and moving bars of light under computer control for position, orientation, direction of movement, and speed. Receptive-field sizes, ranging from 4 to 25 degrees in width, were considerably larger than receptive fields with corresponding eccentricities in the striate cortex. Neurons were highly binocular with most cells equally or nearly equally activated by either eye. Neurons varied in selectivity for axis and direction of moving bars. Some neurons demonstrated little or no selectivity, others were bidirectional on a single axis, while the largest group was highly selective for direction with little or no response to bar movement opposite to the preferred direction. Over 70% of neurons were classified as highly selective and 90% showed some preference for direction and/or axis of stimulus movement. Neurons typically responded to bar movement only over a restricted range of velocities. The majority of neurons responded best to a particular velocity within the 5-60 degrees/s range, with marked attenuation of the response for velocities greater or less than the preferred. Some neurons failed to show significant response attenuation even at the lowest tested velocity, while other neurons preferred velocities of 100 degrees/s or more and failed to attenuate to the highest velocities. Response magnitude varied with stimulus dimensions. Increasing the length of the moving bar typically increased the magnitude of the response slightly until the stimulus exceeded the receptive-field borders. Other neurons responded less to increases in bar length within the excitatory receptive field. Neurons preferred narrow bars less than 1 degree in width, and marked reductions in responses characteristically occurred with wider stimuli. Moving patterns of randomly placed small dots were often as effective as or more effective than single bars in activating neurons. Selectivity for direction of movement remained for the dot pattern. for the dot pattern. Poststimulus time (PST) histograms of responses to bars flashed at a series of 21 different positions across the receptive field, in the "response-plane" format, indicated a spatially and temporally homogeneous receptive-field structure for nearly all neurons. Cells characteristically showed transient excitation at both stimulus onset and offset for all effective stimulus locations. Some cells responded mainly at bright stimulus onset or offset.


2008 ◽  
Vol 100 (3) ◽  
pp. 1622-1634 ◽  
Author(s):  
Ling Qin ◽  
JingYu Wang ◽  
Yu Sato

Previous studies in anesthetized animals reported that the primary auditory cortex (A1) showed homogenous phasic responses to FM tones, namely a transient response to a particular instantaneous frequency when FM sweeps traversed a neuron's tone-evoked receptive field (TRF). Here, in awake cats, we report that A1 cells exhibit heterogeneous FM responses, consisting of three patterns. The first is continuous firing when a slow FM sweep traverses the receptive field of a cell with a sustained tonal response. The duration and amplitude of FM response decrease with increasing sweep speed. The second pattern is transient firing corresponding to the cell's phasic tonal response. This response could be evoked only by a fast FM sweep through the cell's TRF, suggesting a preference for fast FM. The third pattern was associated with the off response to pure tones and was composed of several discrete response peaks during slow FM stimulus. These peaks were not predictable from the cell's tonal response but reliably reflected the time when FM swept across specific frequencies. Our A1 samples often exhibited a complex response pattern, combining two or three of the basic patterns above, resulting in a heterogeneous response population. The diversity of FM responses suggests that A1 use multiple mechanisms to fully represent the whole range of FM parameters, including frequency extent, sweep speed, and direction.


eLife ◽  
2016 ◽  
Vol 5 ◽  
Author(s):  
Bram-Ernst Verhoef ◽  
John HR Maunsell

Shifting attention among visual stimuli at different locations modulates neuronal responses in heterogeneous ways, depending on where those stimuli lie within the receptive fields of neurons. Yet how attention interacts with the receptive-field structure of cortical neurons remains unclear. We measured neuronal responses in area V4 while monkeys shifted their attention among stimuli placed in different locations within and around neuronal receptive fields. We found that attention interacts uniformly with the spatially-varying excitation and suppression associated with the receptive field. This interaction explained the large variability in attention modulation across neurons, and a non-additive relationship among stimulus selectivity, stimulus-induced suppression and attention modulation that has not been previously described. A spatially-tuned normalization model precisely accounted for all observed attention modulations and for the spatial summation properties of neurons. These results provide a unified account of spatial summation and attention-related modulation across both the classical receptive field and the surround.


Perception ◽  
1985 ◽  
Vol 14 (2) ◽  
pp. 105-126 ◽  
Author(s):  
John Allman ◽  
Francis Miezin ◽  
EveLynn McGuinness

The true receptive field of more than 90% of neurons in the middle temporal visual area (MT) extends well beyond the classical receptive field (crf), as mapped with conventional bar or spot stimuli, and includes a surrounding region that is 50 to 100 times the area of the crf. These extensive surrounds are demonstrated by simultaneously stimulating the crf and the surround with moving stimuli. The surrounds commonly have directional and velocity-selective influences that are antagonistic to the response from the crf. The crfs of MT neurons are organized in a topographic representation of the visual field. Thus MT neurons are embedded in an orderly visuotopic array, but are capable of integrating local stimulus conditions within a global context. The extensive surrounds of MT neurons may be involved in figure–ground discrimination, preattentive vision, perceptual constancies, and depth perception through motion cues.


2010 ◽  
Vol 104 (2) ◽  
pp. 960-971 ◽  
Author(s):  
Joonyeol Lee ◽  
John H. R. Maunsell

It remains unclear how attention affects the tuning of individual neurons in visual cerebral cortex. Some observations suggest that attention preferentially enhances responses to low contrast stimuli, whereas others suggest that attention proportionally affects responses to all stimuli. Resolving how attention affects responses to different stimuli is essential for understanding the mechanism by which it acts. To explore the effects of attention on stimuli of different contrasts, we recorded from individual neurons in the middle temporal visual area (MT) of rhesus monkeys while shifting their attention between preferred and nonpreferred stimuli within their receptive fields. This configuration results in robust attentional modulation that makes it possible to readily distinguish whether attention acts preferentially on low contrast stimuli. We found no evidence for greater enhancement of low contrast stimuli. Instead, the strong attentional modulations were well explained by a model in which attention proportionally enhances responses to stimuli of all contrasts. These data, together with observations on the effects of attention on responses to other stimulus dimensions, suggest that the primary effect of attention in visual cortex may be to simply increase the strength of responses to all stimuli by the same proportion.


1991 ◽  
Vol 66 (3) ◽  
pp. 777-793 ◽  
Author(s):  
J. W. McClurkin ◽  
T. J. Gawne ◽  
B. J. Richmond ◽  
L. M. Optican ◽  
D. L. Robinson

1. Using behaving monkeys, we studied the visual responses of single neurons in the parvocellular layers of the lateral geniculate nucleus (LGN) to a set of two-dimensional black and white patterns. We found that monkeys could be trained to make sufficiently reliable and stable fixations to enable us to plot and characterize the receptive fields of individual neurons. A qualitative examination of rasters and a statistical analysis of the data revealed that the responses of neurons were related to the stimuli. 2. The data from 5 of the 13 "X-like" neurons in our sample indicated the presence of antagonistic center and surround mechanisms and linear summation of luminance within center and surround mechanisms. We attribute the lack of evidence for surround antagonism in the eight neurons that failed to exhibit center-surround antagonism either to a mismatch between the size of the pixels in the stimuli and the size of the receptive field or to the lack of a surround mechanism (i.e., the type II neurons of Wiesel and Hubel). 3. The data from five other neurons confirm and extend previous reports indicating that the surround regions of X-like neurons can have nonlinearities. The responses of these neurons were not modulated when a contrast-reversing, bipartite stimulus was centered on the receptive field, which suggests a linear summation within the center and surround mechanisms. However, it was frequently the case for these neurons that stimuli of identical pattern but opposite contrast elicited responses of similar polarity, which indicates nonlinear behavior. 4. We found a wide variety of temporal patterns in the responses of individual LGN neurons, which included differences in the magnitude, width, and number of peaks of the initial on-transient and in the magnitude of the later sustained component. These different temporal patterns were repeatable and clearly different for different visual patterns. These results suggest that visual information may be carried in the shape as well as in the amplitude of the response waveform.


2006 ◽  
Vol 18 (4) ◽  
pp. 562-579 ◽  
Author(s):  
Ko Sakai ◽  
Haruka Nishimura

Contextual modulation reported in early- to intermediate-level visual areas could be an essential component to signal border ownership (BO) that specifies the direction of figure along a contour. The surrounding regions that evoke significant suppression or facilitation are highly localized and asymmetric with respect to the center of the classical receptive field (CRF). We propose a hypothesis that such surrounding modulation is a basis for BO-selectivity. Although this idea has been discussed for several years, it is uncertain how many of a vast variety of surrounding organizations could signal correctly the direction of ownership, and how many could signal consistently for various stimuli. We carried out computationally a population study of the surrounding effects to investigate how many cells exhibit effective and consistent BO signals. We tested hundreds of various organizations, and found that most of the asymmetric, iso-orientation suppressive regions, regardless of position or size, lead to surprisingly high consistency in the direction of ownership for various stimuli. The combinations of iso-orientation suppression and cross-orientation facilitation indicate both high robustness and consistency in the ownership determination. We constructed a model for BO-selective neurons based on the surrounding effects, and investigated whether the model reproduces major characteristics of the neuronal responses, including a variety in the BO selectivity among neurons, consistency with respect to various stimuli, invariance to stimulus size, and co-selectivity to BO and contrast. The model reproduced successfully the major characteristics of BO-selective neurons.


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