Temporal Coding of Contrast in Primary Visual Cortex: When, What, and Why

How do neurons in the primary visual cortex (V1) encode the contrast of a visual stimulus? In this paper, the information that V1 responses convey about the contrast of static visual stimuli is explicitly calculated. These responses often contain several easily distinguished temporal components, which will be called latency, transient, tonic, and off. Calculating the information about contrast conveyed in each component and in groups of components makes it possible to delineate aspects of the temporal structure that may be relevant for contrast encoding. The results indicate that as much or more contrast-related information is encoded into the temporal structure of spike train responses as into the firing rate and that the temporally coded information is manifested most strongly in the latency to response onset. Transient, tonic, and off responses contribute relatively little. The results also reveal that temporal coding is important for distinguishing subtle contrast differences, whereas firing rates are useful for gross discrimination. This suggests that the temporal structure of neurons' responses may extend the dynamic range for contrast encoding in the primate visual system.

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Homeostatic plasticity mechanisms in mouse V1

Philosophical Transactions of the Royal Society B Biological Sciences ◽

10.1098/rstb.2016.0504 ◽

2017 ◽

Vol 372 (1715) ◽

pp. 20160504 ◽

Cited By ~ 10

Author(s):

Megumi Kaneko ◽

Michael P. Stryker

Keyword(s):

Visual Cortex ◽

Primary Visual Cortex ◽

Neuronal Activity ◽

Dynamic Range ◽

Ocular Dominance ◽

Homeostatic Plasticity ◽

Ocular Dominance Plasticity ◽

The Brain

Mechanisms thought of as homeostatic must exist to maintain neuronal activity in the brain within the dynamic range in which neurons can signal. Several distinct mechanisms have been demonstrated experimentally. Three mechanisms that act to restore levels of activity in the primary visual cortex of mice after occlusion and restoration of vision in one eye, which give rise to the phenomenon of ocular dominance plasticity, are discussed. The existence of different mechanisms raises the issue of how these mechanisms operate together to converge on the same set points of activity. This article is part of the themed issue ‘Integrating Hebbian and homeostatic plasticity’.

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Pure tones modulate the representation of orientation and direction in the primary visual cortex

Journal of Neurophysiology ◽

10.1152/jn.00069.2019 ◽

2019 ◽

Vol 121 (6) ◽

pp. 2202-2214 ◽

Cited By ~ 5

Author(s):

John P. McClure ◽

Pierre-Olivier Polack

Keyword(s):

Visual Cortex ◽

Primary Visual Cortex ◽

Visual Stimulus ◽

Visual Stimuli ◽

Direction Selectivity ◽

Multimodal Integration ◽

Visual Responses ◽

V1 Neurons ◽

Pure Tones ◽

The Impact

Multimodal sensory integration facilitates the generation of a unified and coherent perception of the environment. It is now well established that unimodal sensory perceptions, such as vision, are improved in multisensory contexts. Whereas multimodal integration is primarily performed by dedicated multisensory brain regions such as the association cortices or the superior colliculus, recent studies have shown that multisensory interactions also occur in primary sensory cortices. In particular, sounds were shown to modulate the responses of neurons located in layers 2/3 (L2/3) of the mouse primary visual cortex (V1). Yet, the net effect of sound modulation at the V1 population level remained unclear. In the present study, we performed two-photon calcium imaging in awake mice to compare the representation of the orientation and the direction of drifting gratings by V1 L2/3 neurons in unimodal (visual only) or multimodal (audiovisual) conditions. We found that sound modulation depended on the tuning properties (orientation and direction selectivity) and response amplitudes of V1 L2/3 neurons. Sounds potentiated the responses of neurons that were highly tuned to the cue’s orientation and direction but weakly active in the unimodal context, following the principle of inverse effectiveness of multimodal integration. Moreover, sound suppressed the responses of neurons untuned for the orientation and/or the direction of the visual cue. Altogether, sound modulation improved the representation of the orientation and direction of the visual stimulus in V1 L2/3. Namely, visual stimuli presented with auditory stimuli recruited a neuronal population better tuned to the visual stimulus orientation and direction than when presented alone. NEW & NOTEWORTHY The primary visual cortex (V1) receives direct inputs from the primary auditory cortex. Yet, the impact of sounds on visual processing in V1 remains controverted. We show that the modulation by pure tones of V1 visual responses depends on the orientation selectivity, direction selectivity, and response amplitudes of V1 neurons. Hence, audiovisual stimuli recruit a population of V1 neurons better tuned to the orientation and direction of the visual stimulus than unimodal visual stimuli.

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Orientation Tuning, But Not Direction Selectivity, Is Invariant to Temporal Frequency in Primary Visual Cortex

Journal of Neurophysiology ◽

10.1152/jn.01224.2004 ◽

2005 ◽

Vol 94 (2) ◽

pp. 1336-1345 ◽

Cited By ~ 21

Author(s):

Bartlett D. Moore ◽

Henry J. Alitto ◽

W. Martin Usrey

Keyword(s):

Visual Cortex ◽

Primary Visual Cortex ◽

Visual Stimulus ◽

Visual Processing ◽

Cortical Neurons ◽

Temporal Frequency ◽

Direction Selectivity ◽

Orientation Tuning ◽

Orientation Contrast ◽

Wide Range

The activity of neurons in primary visual cortex is influenced by the orientation, contrast, and temporal frequency of a visual stimulus. This raises the question of how these stimulus properties interact to shape neuronal responses. While past studies have shown that the bandwidth of orientation tuning is invariant to stimulus contrast, the influence of temporal frequency on orientation-tuning bandwidth is unknown. Here, we investigate the influence of temporal frequency on orientation tuning and direction selectivity in area 17 of ferret visual cortex. For both simple cells and complex cells, measures of orientation-tuning bandwidth (half-width at half-maximum response) are ∼20–25° across a wide range of temporal frequencies. Thus cortical neurons display temporal-frequency invariant orientation tuning. In contrast, direction selectivity is typically reduced, and occasionally reverses, at nonpreferred temporal frequencies. These results show that the mechanisms contributing to the generation of orientation tuning and direction selectivity are differentially affected by the temporal frequency of a visual stimulus and support the notion that stability of orientation tuning is an important aspect of visual processing.

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Neural Representation of the Luminance and Brightness of a Uniform Surface in the Macaque Primary Visual Cortex

Journal of Neurophysiology ◽

10.1152/jn.2001.86.5.2559 ◽

2001 ◽

Vol 86 (5) ◽

pp. 2559-2570 ◽

Cited By ~ 107

Author(s):

Masaharu Kinoshita ◽

Hidehiko Komatsu

Keyword(s):

Visual Cortex ◽

Receptive Field ◽

Primary Visual Cortex ◽

Neural Activity ◽

Dynamic Range ◽

Neural Representation ◽

Homogeneous Surface ◽

V1 Neurons ◽

Classical Receptive Field ◽

Multiple Unit

The perceived brightness of a surface is determined not only by the luminance of the surface (local information), but also by the luminance of its surround (global information). To better understand the neural representation of surface brightness, we investigated the effects of local and global luminance on the activity of neurons in the primary visual cortex (V1) of awake macaque monkeys. Single- and multiple-unit recordings were made from V1 while the monkeys were performing a visual fixation task. The classical receptive field of each neuron was identified as a region responding to a spot stimulus. Neural responses were assessed using homogeneous surfaces at least three times as large as the receptive field as stimuli. We first examined the sensitivity of neurons to variation in local surface luminance, while the luminance of the surround was held constant. The activity of a large majority of surface-responsive neurons (106/115) varied monotonically with changes in surface luminance; in some the dynamic range was over 3 log units. This monotonic relation between surface luminance and neural activity was more evident later in the stimulus period than early on. The effect of the global luminance on neural activity was then assessed in 81 of the surface-responsive neurons by varying the luminance of the surround while holding the luminance of the surface constant. The activity of one group of neurons (25/81) was unaffected by the luminance of the surround; these neurons appear to encode the physical luminance of a surface covering the receptive field. The responses of the other neurons were affected by the luminance of the surround. The effects of the luminances of the surface and the surround on the activities of 26 of these neurons were in the same direction (either increased or decreased), while the effects on the remaining 25 neurons were in opposite directions. The activities of the latter group of neurons seemed to parallel the perceived brightness of the surface, whereas the former seemed to encode the level of illumination. There were differences across different types of neurons with regard to the layer distribution. These findings indicate that global luminance information significantly modulates the activity of surface-responsive V1 neurons and that not only physical luminance, but also perceived brightness, of a homogeneous surface is represented in V1.

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Locomotion enhances neural encoding of visual stimuli in mouse V1

10.1101/102673 ◽

2017 ◽

Cited By ~ 2

Author(s):

Maria C. Dadarlat ◽

Michael P. Stryker

Keyword(s):

Visual Cortex ◽

Primary Visual Cortex ◽

Visual Stimuli ◽

Major Effect ◽

Neural Population ◽

Neural Encoding ◽

Firing Rates ◽

Fold Reduction ◽

Layer V ◽

The Relationship

AbstractNeurons in mouse primary visual cortex (V1) are selective for particular properties of visual stimuli. Locomotion causes a change in cortical state that leaves their selectivity unchanged but strengthens their responses. Both locomotion and the change in cortical state are initiated by projections from the mesencephalic locomotor region (MLR), the latter through a disinhibitory circuit in V1. The function served by this change in cortical state is unknown. By recording simultaneously from a large number of single neurons in alert mice viewing moving gratings, we investigated the relationship between locomotion and the information contained within the neural population. We found that locomotion improved encoding of visual stimuli in V1 by two mechanisms. First, locomotion-induced increases in firing rates enhanced the mutual information between visual stimuli and single neuron responses over a fixed window of time. Second, stimulus discriminability was improved, even for fixed population firing rates, because of a decrease in noise correlations across the population during locomotion. These two mechanisms contributed differently to improvements in discriminability across cortical layers, with changes in firing rates most important in the upper layers and changes in noise correlations most important in layer V. Together, these changes resulted in a three- to five-fold reduction in the time needed to precisely encode grating direction and orientation. These results support the hypothesis that cortical state shifts during locomotion to accommodate an increased load on the visual system when mice are moving.Significance StatementThis paper contains three novel findings about the representation of information in neurons within the primary visual cortex of the mouse. First, we show that locomotion reduces by at least a factor of three the time needed for information to accumulate in the visual cortex that allows the distinction of different visual stimuli. Second, we show that the effect of locomotion is to increase information in cells of all layers of the visual cortex. Third we show that the means by which information is enhanced by locomotion differs between the upper layers, where the major effect is the increasing of firing rates, and in layer V, where the major effect is the reduction in noise correlations.

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Faculty Opinions recommendation of Synchrony and covariation of firing rates in the primary visual cortex during contour grouping.

Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature ◽

10.3410/f.1021053.241469 ◽

2004 ◽

Author(s):

Thomas S Collett

Keyword(s):

Visual Cortex ◽

Primary Visual Cortex ◽

Firing Rates ◽

Contour Grouping

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Scaling of information in large neural populations reveals signatures of information-limiting correlations

10.1101/2020.01.10.902171 ◽

2020 ◽

Cited By ~ 2

Author(s):

MohammadMehdi Kafashan ◽

Anna Jaffe ◽

Selmaan N. Chettih ◽

Ramon Nogueira ◽

Iñigo Arandia-Romero ◽

...

Keyword(s):

Visual Cortex ◽

Primary Visual Cortex ◽

Visual Stimulus ◽

Brain Area ◽

Correlated Noise ◽

Neuronal Populations ◽

Total Information ◽

Neural Populations ◽

The Brain ◽

Stimulus Direction

AbstractHow is information distributed across large neuronal populations within a given brain area? One possibility is that information is distributed roughly evenly across neurons, so that total information scales linearly with the number of recorded neurons. Alternatively, the neural code might be highly redundant, meaning that total information saturates. Here we investigated how information about the direction of a moving visual stimulus is distributed across hundreds of simultaneously recorded neurons in mouse primary visual cortex (V1). We found that information scales sublinearly, due to the presence of correlated noise in these populations. Using recent theoretical advances, we compartmentalized noise correlations into information-limiting and nonlimiting components, and then extrapolated to predict how information grows when neural populations are even larger. We predict that tens of thousands of neurons are required to encode 95% of the information about visual stimulus direction, a number much smaller than the number of neurons in V1. Overall, these findings suggest that the brain uses a widely distributed, but nonetheless redundant code that supports recovering most information from smaller subpopulations.

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Direction-selective motion discrimination by traveling waves in visual cortex

10.1101/2020.03.03.974089 ◽

2020 ◽

Author(s):

Stewart Heitmann ◽

G. Bard Ermentrout

Keyword(s):

Visual Cortex ◽

Visual Field ◽

Primary Visual Cortex ◽

Visual Stimulus ◽

Traveling Waves ◽

Neural Activity ◽

Time Delays ◽

Neural Mechanism ◽

Neural Responses ◽

Transmission Delays

AbstractThe majority of neurons in primary visual cortex respond selectively to bars of light that have a specific orientation and move in a specific direction. The spatial and temporal responses of such neurons are non-separable. How neurons accomplish that computational feat without resort to explicit time delays is unknown. We propose a novel neural mechanism whereby visual cortex computes non-separable responses by generating endogenous traveling waves of neural activity that resonate with the space-time signature of the visual stimulus. The spatiotemporal characteristics of the response are defined by the local topology of excitatory and inhibitory lateral connections in the cortex. We simulated the interaction between endogenous traveling waves and the visual stimulus using spatially distributed populations of excitatory and inhibitory neurons with Wilson-Cowan dynamics and inhibitory-surround coupling. Our model reliably detected visual gratings that moved with a given speed and direction provided that we incorporated neural competition to suppress false motion signals in the opposite direction. The findings suggest that endogenous traveling waves in visual cortex can impart direction-selectivity on neural responses without resort to explicit time delays. They also suggest a functional role for motion opponency in eliminating false motion signals.Author summaryIt is well established that the so-called ‘simple cells’ of the primary visual cortex respond preferentially to oriented bars of light that move across the visual field with a particular speed and direction. The spatiotemporal responses of such neurons are said to be non-separable because they cannot be constructed from independent spatial and temporal neural mechanisms. Contemporary theories of how neurons compute non-separable responses typically rely on finely tuned transmission delays between signals from disparate regions of the visual field. However the existence of such delays is controversial. We propose an alternative neural mechanism for computing non-separable responses that does not require transmission delays. It instead relies on the predisposition of the cortical tissue to spontaneously generate spatiotemporal waves of neural activity that travel with a particular speed and direction. We propose that the endogenous wave activity resonates with the visual stimulus to elicit direction-selective neural responses to visual motion. We demonstrate the principle in computer models and show that competition between opposing neurons robustly enhances their ability to discriminate between visual gratings that move in opposite directions.

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