Orientation Tuning of Input Conductance, Excitation, and Inhibition in Cat Primary Visual Cortex

The input conductance of cells in the cat primary visual cortex (V1) has been shown recently to grow substantially during visual stimulation. Because increasing conductance can have a divisive effect on the synaptic input, theoretical proposals have ascribed to it specific functions. According to the veto model, conductance increases would serve to sharpen orientation tuning by increasing most at off-optimal orientations. According to the normalization model, conductance increases would control the cell's gain, by being independent of stimulus orientation and by growing with stimulus contrast. We set out to test these proposals and to determine the visual properties and possible synaptic origin of the conductance increases. We recorded the membrane potential of cat V1 cells while injecting steady currents and presenting drifting grating patterns of varying contrast and orientation. Input conductance grew with stimulus contrast by 20–300%, generally more in simple cells (40–300%) than in complex cells (20–120%), and in simple cells was strongly modulated in time. Conductance was invariably maximal for stimuli of the preferred orientation. Thus conductance changes contribute to a gain control mechanism, but the strength of this gain control does not depend uniquely on contrast. By assuming that the conductance changes are entirely synaptic, we further derived the excitatory and inhibitory synaptic conductances underlying the visual responses. In simple cells, these conductances were often arranged in push-pull: excitation increased when inhibition decreased and vice versa. Excitation and inhibition had similar preferred orientations and did not appear to differ in tuning width, suggesting that the intracortical synaptic inputs to simple cells of cat V1 originate from cells with similar orientation tuning. This finding is at odds with models where orientation tuning in simple cells is achieved by inhibition at off-optimal orientations or sharpened by inhibition that is more broadly tuned than excitation.

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Mechanisms of Direction Selectivity in Cat Primary Visual Cortex as Revealed by Visual Adaptation

Journal of Neurophysiology ◽

10.1152/jn.00241.2010 ◽

2010 ◽

Vol 104 (5) ◽

pp. 2615-2623 ◽

Cited By ~ 12

Author(s):

Nicholas J. Priebe ◽

Ilan Lampl ◽

David Ferster

Keyword(s):

Visual Cortex ◽

Primary Visual Cortex ◽

Cortical Neurons ◽

Visual Stimulation ◽

Direction Selectivity ◽

Dependent Manner ◽

Visual Responses ◽

Null Direction ◽

Simple Cells ◽

Complex Cells

In contrast to neurons of the lateral geniculate nucleus (LGN), neurons in the primary visual cortex (V1) are selective for the direction of visual motion. Cortical direction selectivity could emerge from the spatiotemporal configuration of inputs from thalamic cells, from intracortical inhibitory interactions, or from a combination of thalamic and intracortical interactions. To distinguish between these possibilities, we studied the effect of adaptation (prolonged visual stimulation) on the direction selectivity of intracellularly recorded cortical neurons. It is known that adaptation selectively reduces the responses of cortical neurons, while largely sparing the afferent LGN input. Adaptation can therefore be used as a tool to dissect the relative contribution of afferent and intracortical interactions to the generation of direction selectivity. In both simple and complex cells, adaptation caused a hyperpolarization of the resting membrane potential (−2.5 mV, simple cells, −0.95 mV complex cells). In simple cells, adaptation in either direction only slightly reduced the visually evoked depolarization; this reduction was similar for preferred and null directions. In complex cells, adaptation strongly reduced visual responses in a direction-dependent manner: the reduction was largest when the stimulus direction matched that of the adapting motion. As a result, adaptation caused changes in the direction selectivity of complex cells: direction selectivity was reduced after preferred direction adaptation and increased after null direction adaptation. Because adaptation in the null direction enhanced direction selectivity rather than reduced it, it seems unlikely that inhibition from the null direction is the primary mechanism for creating direction selectivity.

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Influence of Contrast on Orientation and Temporal Frequency Tuning in Ferret Primary Visual Cortex

Journal of Neurophysiology ◽

10.1152/jn.00943.2003 ◽

2004 ◽

Vol 91 (6) ◽

pp. 2797-2808 ◽

Cited By ~ 83

Author(s):

Henry J. Alitto ◽

W. Martin Usrey

Keyword(s):

Visual Cortex ◽

Primary Visual Cortex ◽

Cortical Neurons ◽

Frequency Tuning ◽

Temporal Frequency ◽

Orientation Tuning ◽

Visual Response ◽

Stimulus Contrast ◽

Tuning Curves ◽

Simple And Complex Cells

Neurons in primary visual cortex are highly sensitive to the contrast, orientation, and temporal frequency of a visual stimulus. These three stimulus properties can be varied independently of one another, raising the question of how they interact to influence neuronal responses. We recorded from individual neurons in ferret primary visual cortex to determine the influence of stimulus contrast on orientation tuning, temporal-frequency tuning, and latency to visual response. Results show that orientation-tuning bandwidth is not affected by contrast level. Thus neurons in ferret visual cortex display contrast-invariant orientation tuning. Stimulus contrast does, however, influence the structure of orientation-tuning curves as measures of circular variance vary inversely with contrast for both simple and complex cells. This change in circular variance depends, in part, on a contrast-dependent change in the ratio of null to preferred orientation responses. Stimulus contrast also has an influence on the temporal-frequency tuning of cortical neurons. Both simple and complex cells display a contrast-dependent rightward shift in their temporal frequency-tuning curves that results in an increase in the highest temporal frequency needed to produce a half-maximum response (TF50). Results show that the degree of the contrast-dependent increase in TF50 is similar for cortical neurons and neurons in the lateral geniculate nucleus (LGN) and indicate that subcortical mechanisms likely play a major role in establishing the degree of effect displayed by downstream neurons. Finally, results show that LGN and cortical neurons experience a contrast-dependent phase advance in their visual response. This phase advance is most pronounced for cortical neurons indicating a role for both subcortical and cortical mechanisms.

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Sensory experience during locomotion promotes recovery of function in adult visual cortex

eLife ◽

10.7554/elife.02798 ◽

2014 ◽

Vol 3 ◽

Cited By ~ 53

Author(s):

Megumi Kaneko ◽

Michael P Stryker

Keyword(s):

Visual Cortex ◽

Primary Visual Cortex ◽

Neural Circuits ◽

Visual Stimulation ◽

Recovery Of Function ◽

Sensory Deprivation ◽

Sensory Experience ◽

Inhibitory Neurons ◽

Visual Responses ◽

Effective Stimulus

Recovery from sensory deprivation is slow and incomplete in adult visual cortex. In this study, we show that visual stimulation during locomotion, which increases the gain of visual responses in primary visual cortex, dramatically enhances recovery in the mouse. Excitatory neurons regained normal levels of response, while narrow-spiking (inhibitory) neurons remained less active. Visual stimulation or locomotion alone did not enhance recovery. Responses to the particular visual stimuli viewed by the animal during locomotion recovered, while those to another normally effective stimulus did not, suggesting that locomotion promotes the recovery only of the neural circuits that are activated concurrent with the locomotion. These findings may provide an avenue for improving recovery from amblyopia in humans.

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Serotonergic Modulation of Orientation Tuning of Neurons in Primary Visual Cortex of Anesthetized Mice

Basic and Clinical Neuroscience Journal ◽

10.32598/bcn.2021.3180.1 ◽

2021 ◽

Author(s):

Sareh Rostami ◽

◽

Amin Asgharzadeh Alvar ◽

Parviz Ghaderi ◽

Leila Dargahi ◽

...

Keyword(s):

Electrical Stimulation ◽

Visual Cortex ◽

Firing Rate ◽

Primary Visual Cortex ◽

Serotonergic System ◽

Orientation Tuning ◽

Visual Response ◽

Visual Responses ◽

Patch Clamp Recording ◽

Serotonergic Modulation

Introduction: Sensory processing is profoundly regulated by brain neuromodulatory systems. One of the main neuromodulators is serotonin which influences higher cognitive functions such as different aspects of perceptual processing. So, malfunction in the serotonergic system may lead to visual illusion in psychiatric disorders such as autism and schizophrenia. In this work, we examined the serotonergic modulation of visual responses of neurons to stimulus orientation in the primary visual cortex. Methods: Eight-weeks old naive mice were anesthetized and craniotomy was done on the region of interest in primary visual cortex. Spontaneous and visual-evoked activities of neurons were recorded before and during the electrical stimulation of dorsal raphe nucleus using in vivo whole-cell patch-clamp recording. Square-wave grating of 12 orientations was presented. Data was analyzed and Wilcoxon signed-rank test, used in order to compare the data of two conditions that belong to the same neurons, with or without electrical stimulation. Results: The serotonergic system changed orientation tuning of about 60 % recorded neurons by decreasing the mean firing rate in two independent visual response components: gain and baseline response. It also increased mean firing rate in a small number of neurons (about 20%). Beyond that, it left the preferred orientation and sensitivity of neurons unchanged. Conclusion: However, serotonergic modulation showed a bi-directional effect; it seems to cause predominately divisive and subtractive decreases in the visual responses of the neurons in the primary visual cortex that can modify the balance between internal and external sensory signals and result in disorders.

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Population receptive fields of human primary visual cortex organised as DC-balanced bandpass filters

Scientific Reports ◽

10.1038/s41598-021-01891-2 ◽

2021 ◽

Vol 11 (1) ◽

Author(s):

Daniel Gramm Kristensen ◽

Kristian Sandberg

Keyword(s):

Visual Cortex ◽

Primary Visual Cortex ◽

Visual Stimulation ◽

Receptive Fields ◽

Bandpass Filters ◽

Model Complexity ◽

Stimulus Contrast ◽

Mathematical Basis ◽

Dc Offset ◽

Difference Of Gaussians

AbstractThe response to visual stimulation of population receptive fields (pRF) in the human visual cortex has been modelled with a Difference of Gaussians model, yet many aspects of their organisation remain poorly understood. Here, we examined the mathematical basis and signal-processing properties of this model and argue that the DC-balanced Difference of Gaussians (DoG) holds a number of advantages over a DC-biased DoG. Through functional magnetic resonance imaging (fMRI) pRF mapping, we compared performance of DC-balanced and DC-biased models in human primary visual cortex and found that when model complexity is taken into account, the DC-balanced model is preferred. Finally, we present evidence indicating that the BOLD signal DC offset contains information related to the processing of visual stimuli. Taken together, the results indicate that V1 pRFs are at least frequently organised in the exact constellation that allows them to function as bandpass filters, which makes the separation of stimulus contrast and luminance possible. We further speculate that if the DoG models stimulus contrast, the DC offset may reflect stimulus luminance. These findings suggest that it may be possible to separate contrast and luminance processing in fMRI experiments and this could lead to new insights on the haemodynamic response.

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Propagation of orientation selectivity in a spiking network model of layered primary visual cortex

10.1101/425694 ◽

2018 ◽

Author(s):

Benjamin Merkt ◽

Friedrich Schüßler ◽

Stefan Rotter

Keyword(s):

Visual Cortex ◽

Primary Visual Cortex ◽

Visual Stimulation ◽

Orientation Selectivity ◽

System Level ◽

Orientation Tuning ◽

Dimensional System ◽

Firing Rates ◽

Wide Range ◽

Low Dimensional

AbstractNeurons in different layers of sensory cortex generally have different functional properties. But what determines firing rates and tuning properties of neurons in different layers? Orientation selectivity in primary visual cortex (V1) is an interesting case to study these questions. Thalamic projections essentially determine the preferred orientation of neurons that receive direct input. But how is this tuning propagated though layers, and how can selective responses emerge in layers that do not have direct access to the thalamus? Here we combine numerical simulations with mathematical analyses to address this problem. We find that a large-scale network, which just accounts for experimentally measured layer and cell-type specific connection probabilities, yields firing rates and orientation selectivities matching electrophysiological recordings in rodent V1 surprisingly well. Further analysis, however, is complicated by the fact that neuronal responses emerge in a dynamic fashion and cannot be directly inferred from static neuroanatomy, as some connections tend to have unintuitive effects due to recurrent interactions and strong feedback loops. These emergent phenomena can be understood by linearizing and coarse-graining. In fact, we were able to derive a low-dimensional linear dynamical system effectively describing stimulus-driven activity layer by layer. This low-dimensional system explains layer-specific firing rates and orientation tuning by accounting for the different gain factors of the aggregate system. Our theory can also be used to design novel optogenetic stimulation experiments, thus facilitating further exploration of the interplay between connectivity and function.Author summaryUnderstanding the precise roles of neuronal sub-populations in shaping the activity of networks is a fundamental objective of neuroscience research. In complex neuronal network structures like the neocortex, the relation between the connec-tome and the algorithm implemented in it is often not self-explaining. To this end, our work makes three important contributions. First, we show that the connectivity extracted by anatomical and physiological experiments in visual cortex suffices to explain important properties of the various sub-populations, including their selectivity to visual stimulation. Second, we introduce a novel system-level approach for the analysis of input-output relations of recurrent networks, which leads to the observed activity patterns. Third, we present a method for the design of future optogenetic experiments that can be used to devise specific stimuli resulting in a predictable change of neuronal activity. In summary, we introduce a novel frame-work to determine the relevant features of neuronal microcircuit function that can be applied to a wide range of neuronal systems.

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