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Conditioning sharpens the spatial representation of rewarded stimuli in mouse primary visual cortex.

ABSTRACT: Reward is often employed as reinforcement in behavioral paradigms but it is unclear how the visuospatial aspect of a stimulus-reward association affects the cortical representation of visual space. Using a head-fixed paradigm, we conditioned mice to associate the same visual pattern in adjacent retinotopic regions with availability and absence of reward. Time-lapse intrinsic optical signal imaging under anesthesia showed that conditioning increased the spatial separation of mesoscale cortical representations of reward predicting- and non-reward predicting stimuli. Subsequent in vivo two-photon calcium imaging revealed that this improved separation correlated with enhanced population coding for retinotopic location, specifically for the trained orientation and spatially confined to the V1 region where rewarded and non-rewarded stimulus representations bordered. These results are corroborated by conditioning-induced differences in the correlation structure of population activity. Thus, the cortical representation of visual space is sharpened as consequence of associative stimulus-reward learning while the overall retinotopic map remains unaltered.

SUBMITTER: Goltstein PM

PROVIDER: S-EPMC6141231 | biostudies-literature | 2018 Sep

REPOSITORIES: biostudies-literature

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Conditioning sharpens the spatial representation of rewarded stimuli in mouse primary visual cortex.

Goltstein Pieter M PM Meijer Guido T GT Pennartz Cyriel Ma CM

eLife 20180917

Reward is often employed as reinforcement in behavioral paradigms but it is unclear how the visuospatial aspect of a stimulus-reward association affects the cortical representation of visual space. Using a head-fixed paradigm, we conditioned mice to associate the same visual pattern in adjacent retinotopic regions with availability and absence of reward. Time-lapse intrinsic optical signal imaging under anesthesia showed that conditioning increased the spatial separation of mesoscale cortical re ...[more]

PMID: 30222107

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Project description:Processing capabilities for many low-level visual features are experientially malleable, aiding sighted organisms in adapting to dynamic environments. Explicit instructions to attend a specific visual field location influence retinotopic visuocortical activity, amplifying responses to stimuli appearing at cued spatial positions. It remains undetermined both how such prioritization affects surrounding nonprioritized locations, and if a given retinotopic spatial position can attain enhanced cortical representation through experience rather than instruction. The current report examined visuocortical response changes as human observers (N = 51, 19 male) learned, through differential classical conditioning, to associate specific screen locations with aversive outcomes. Using dense-array EEG and pupillometry, we tested the preregistered hypotheses of either sharpening or generalization around an aversively associated location following a single conditioning session. Competing hypotheses tested whether mean response changes would take the form of a Gaussian (generalization) or difference-of-Gaussian (sharpening) distribution over spatial positions, peaking at the viewing location paired with a noxious noise. Occipital 15 Hz steady-state visual evoked potential responses were selectively heightened when viewing aversively paired locations and displayed a nonlinear, difference-of-Gaussian profile across neighboring locations, consistent with suppressive surround modulation of nonprioritized positions. Measures of alpha-band (8-12 Hz) activity were differentially altered in anterior versus posterior locations, while pupil diameter exhibited selectively heightened responses to noise-paired locations but did not evince differences across the nonpaired locations. These results indicate that visuocortical spatial representations are sharpened in response to location-specific aversive conditioning, while top-down influences indexed by alpha-power reduction exhibit posterior generalization and anterior sharpening.SIGNIFICANCE STATEMENT It is increasingly recognized that early visual cortex is not a static processor of physical features, but is instead constantly shaped by perceptual experience. It remains unclear, however, to what extent the cortical representation of many fundamental features, including visual field location, is malleable by experience. Using EEG and an aversive classical conditioning paradigm, we observed sharpening of visuocortical responses to stimuli appearing at aversively associated locations along with location-selective facilitation of response systems indexed by pupil diameter and EEG alpha power. These findings highlight the experience-dependent flexibility of retinotopic spatial representations in visual cortex, opening avenues toward novel treatment targets in disorders of attention and spatial cognition.

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.

Dataset Information

Conditioning sharpens the spatial representation of rewarded stimuli in mouse primary visual cortex.

Publications

Conditioning sharpens the spatial representation of rewarded stimuli in mouse primary visual cortex.

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