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Dopaminergic reward signals selectively decrease fMRI activity in primate visual cortex.

ABSTRACT: Stimulus-reward coupling without attention can induce highly specific perceptual learning effects, suggesting that reward triggers selective plasticity within visual cortex. Additionally, dopamine-releasing events-temporally surrounding stimulus-reward associations-selectively enhance memory. These forms of plasticity may be evoked by selective modulation of stimulus representations during dopamine-inducing events. However, it remains to be shown whether dopaminergic signals can selectively modulate visual cortical activity. We measured fMRI activity in monkey visual cortex during reward-only trials apart from intermixed cue-reward trials. Reward without visual stimulation selectively decreased fMRI activity within the cue representations that had been paired with reward during other trials. Behavioral tests indicated that these same uncued reward trials strengthened cue-reward associations. Furthermore, such spatially-specific activity modulations depended on prediction error, as shown by manipulations of reward magnitude, cue-reward probability, cue-reward familiarity, and dopamine signaling. This cue-selective negative reward signal offers a mechanism for selectively gating sensory cortical plasticity.

SUBMITTER: Arsenault JT

PROVIDER: S-EPMC3610182 | biostudies-literature | 2013 Mar

REPOSITORIES: biostudies-literature

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Dopaminergic reward signals selectively decrease fMRI activity in primate visual cortex.

Arsenault John T JT Nelissen Koen K Jarraya Bechir B Vanduffel Wim W

Neuron 20130301 6

Stimulus-reward coupling without attention can induce highly specific perceptual learning effects, suggesting that reward triggers selective plasticity within visual cortex. Additionally, dopamine-releasing events-temporally surrounding stimulus-reward associations-selectively enhance memory. These forms of plasticity may be evoked by selective modulation of stimulus representations during dopamine-inducing events. However, it remains to be shown whether dopaminergic signals can selectively modu ...[more]

PMID: 23522051

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Project description:Our perception of how objects are laid out in visual scenes is remarkably stable, despite rapid shifts in the patterns of light that fall on the retina with each saccade. One mechanism that may help establish perceptual stability is border ownership assignment. Studies in macaque area V2 have identified border ownership neurons that signal which side of a border belongs to a foreground surface. This signal persists for hundreds of milliseconds after border ownership has been rendered ambiguous by deleting the stimulus features that distinguish foreground from background. Remarkably, this signal survives eye movements: border ownership neurons also exhibit border ownership signals de novo when an eye movement places the newly ambiguous border within their receptive field. The grouping cell hypothesis proposes the existence of hypothetical grouping cells in a downstream brain area. These cells would compute persistent proto-object representations and therefore have the properties to endow cells in upstream brain areas with selectivity for border ownership. Such grouping cells have been predicted to show a centripetal and persistent pattern of preferred side of ownership for a border placed parallel to the perimeter of their classical receptive field, and such a centripetal ownership preference pattern should also occur de novo in these same cells if an ambiguous border lands in their receptive field after a saccade. It is unknown if grouping cells exist. Here we used laminar multielectrodes in area V4 - the main source of feedback to V2 - of behaving macaques to determine whether such grouping cells exist. Consistent with the model prediction we find a substantial population of neurons with these properties, in all laminar compartments, and they exhibit a response latency that is short enough to act as the source that endows neurons in V2 with selectivity for border ownership. While grouping cell activity provides information about the location of foreground surfaces, these neurons are, counterintuitively, not as strongly tuned for luminance contrast polarity, a feature of those surfaces, as are border ownership cells. Our data suggest a division of labor in which these newly discovered grouping cells provide spatiotemporal continuity of segmented surfaces whereas border ownership cells link this location information with surface features such as luminance contrast.

Dataset Information

Dopaminergic reward signals selectively decrease fMRI activity in primate visual cortex.

Publications

Dopaminergic reward signals selectively decrease fMRI activity in primate visual cortex.

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