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Feature selectivity is stable in primary visual cortex across a range of spatial frequencies.

ABSTRACT: Reliable perception of environmental signals is a critical first step to generating appropriate responses and actions in awake behaving animals. The extent to which stimulus features are stably represented at the level of individual neurons is not well understood. To address this issue, we investigated the persistence of stimulus response tuning over the course of 1-2 weeks in the primary visual cortex of awake, adult mice. Using 2-photon calcium imaging, we directly compared tuning stability to two stimulus features (orientation and spatial frequency) within the same neurons, specifically in layer 2/3 excitatory neurons. The majority of neurons that were tracked and tuned on consecutive imaging sessions maintained stable orientation and spatial frequency preferences (83% and 76% of the population, respectively) over a 2-week period. Selectivity, measured as orientation and spatial frequency bandwidth, was also stable. Taking into account all 4 parameters, we found that the proportion of stable neurons was less than two thirds (57%). Thus, a substantial fraction of neurons (43%) were unstable in at least one parameter. Furthermore, we found that instability of orientation preference was not predictive of instability of spatial frequency preference within the same neurons. Population analysis revealed that noise correlation values were stable well beyond the estimated decline in monosynaptic connectivity (~250-300 microns). Our results demonstrate that orientation preference is stable across a range of spatial frequencies and that the tuning of distinct stimulus features can be independently maintained within a single neuron.

SUBMITTER: Jeon BB

PROVIDER: S-EPMC6191427 | biostudies-literature | 2018 Oct

REPOSITORIES: biostudies-literature

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Feature selectivity is stable in primary visual cortex across a range of spatial frequencies.

Jeon Brian B BB Swain Alex D AD Good Jeffrey T JT Chase Steven M SM Kuhlman Sandra J SJ

Scientific reports 20181016 1

Reliable perception of environmental signals is a critical first step to generating appropriate responses and actions in awake behaving animals. The extent to which stimulus features are stably represented at the level of individual neurons is not well understood. To address this issue, we investigated the persistence of stimulus response tuning over the course of 1-2 weeks in the primary visual cortex of awake, adult mice. Using 2-photon calcium imaging, we directly compared tuning stability to ...[more]

PMID: 30327571

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Project description:In the cat primary visual cortex, it is accepted that neurons optimally responding to similar stimulus orientations are clustered in a column extending from the superficial to deep layers. The cerebral cortex is, however, folded inside a skull, which makes gyri and fundi. The primary visual area of cats, area 17, is located on the fold of the cortex called the lateral gyrus. These facts raise the question of how to reconcile the tangential arrangement of the orientation columns with the curvature of the gyrus. In the present study, we show a possible configuration of feature representation in the visual cortex using a three-dimensional (3D) self-organization model. We took into account preferred orientation, preferred direction, ocular dominance and retinotopy, assuming isotropic interaction. We performed computer simulation only in the middle layer at the beginning and expanded the range of simulation gradually to other layers, which was found to be a unique method in the present model for obtaining orientation columns spanning all the layers in the flat cortex. Vertical columns of preferred orientations were found in the flat parts of the model cortex. On the other hand, in the curved parts, preferred orientations were represented in wedge-like columns rather than straight columns, and preferred directions were frequently reversed in the deeper layers. Singularities associated with orientation representation appeared as warped lines in the 3D model cortex. Direction reversal appeared on the sheets that were delimited by orientation-singularity lines. These structures emerged from the balance between periodic arrangements of preferred orientations and vertical alignment of the same orientations. Our theoretical predictions about orientation representation were confirmed by multi-slice, high-resolution functional MRI in the cat visual cortex. We obtained a close agreement between theoretical predictions and experimental observations. The present study throws a doubt about the conventional columnar view of orientation representation, although more experimental data are needed.

Project description:Local excitatory connections in mouse primary visual cortex (V1) are stronger and more prevalent between neurons that share similar functional response features. However, the details of how functional rules for local connectivity shape neuronal responses in V1 remain unknown. We hypothesised that complex responses to visual stimuli may arise as a consequence of rules for selective excitatory connectivity within the local network in the superficial layers of mouse V1. In mouse V1 many neurons respond to overlapping grating stimuli (plaid stimuli) with highly selective and facilitatory responses, which are not simply predicted by responses to single gratings presented alone. This complexity is surprising, since excitatory neurons in V1 are considered to be mainly tuned to single preferred orientations. Here we examined the consequences for visual processing of two alternative connectivity schemes: in the first case, local connections are aligned with visual properties inherited from feedforward input (a 'like-to-like' scheme specifically connecting neurons that share similar preferred orientations); in the second case, local connections group neurons into excitatory subnetworks that combine and amplify multiple feedforward visual properties (a 'feature binding' scheme). By comparing predictions from large scale computational models with in vivo recordings of visual representations in mouse V1, we found that responses to plaid stimuli were best explained by assuming feature binding connectivity. Unlike under the like-to-like scheme, selective amplification within feature-binding excitatory subnetworks replicated experimentally observed facilitatory responses to plaid stimuli; explained selective plaid responses not predicted by grating selectivity; and was consistent with broad anatomical selectivity observed in mouse V1. Our results show that visual feature binding can occur through local recurrent mechanisms without requiring feedforward convergence, and that such a mechanism is consistent with visual responses and cortical anatomy in mouse V1.

Dataset Information

Feature selectivity is stable in primary visual cortex across a range of spatial frequencies.

Publications

Feature selectivity is stable in primary visual cortex across a range of spatial frequencies.

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