Emergence of visually-evoked reward expectation signals in dopamine neurons via the superior colliculus in V1 lesioned monkeys

Responses of midbrain dopamine (DA) neurons reflecting expected reward from sensory cues are critical for reward-based associative learning. However, critical pathways by which reward-related visual information is relayed to DA neurons remain unclear. To address this question, we investigated Pavlov...

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Main Authors: Norihiro Takakuwa, Rikako Kato, Peter Redgrave, Tadashi Isa
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2017-06-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/24459
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spelling doaj-708afeb71bca4a9791808a8995b151ad2021-05-05T13:33:02ZengeLife Sciences Publications LtdeLife2050-084X2017-06-01610.7554/eLife.24459Emergence of visually-evoked reward expectation signals in dopamine neurons via the superior colliculus in V1 lesioned monkeysNorihiro Takakuwa0https://orcid.org/0000-0003-4075-5697Rikako Kato1Peter Redgrave2Tadashi Isa3https://orcid.org/0000-0001-5652-4688Department of Developmental Physiology, National Institute for Physiological Sciences, Okazaki, Japan; Department of Physiological Sciences, SOKENDAI, Hayama, Japan; Department of Neuroscience, Graduate School of Medicine Kyoto University, Kyoto, JapanDepartment of Developmental Physiology, National Institute for Physiological Sciences, Okazaki, Japan; Department of Neuroscience, Graduate School of Medicine Kyoto University, Kyoto, JapanDepartment of Psychology, University of Sheffield, Sheffield, United KingdomDepartment of Developmental Physiology, National Institute for Physiological Sciences, Okazaki, Japan; Department of Physiological Sciences, SOKENDAI, Hayama, Japan; Department of Neuroscience, Graduate School of Medicine Kyoto University, Kyoto, JapanResponses of midbrain dopamine (DA) neurons reflecting expected reward from sensory cues are critical for reward-based associative learning. However, critical pathways by which reward-related visual information is relayed to DA neurons remain unclear. To address this question, we investigated Pavlovian conditioning in macaque monkeys with unilateral primary visual cortex (V1) lesions (an animal model of ‘blindsight’). Anticipatory licking responses to obtain juice drops were elicited in response to visual conditioned stimuli (CS) in the affected visual field. Subsequent pharmacological inactivation of the superior colliculus (SC) suppressed the anticipatory licking. Concurrent single unit recordings indicated that DA responses reflecting the reward expectation could be recorded in the absence of V1, and that these responses were also suppressed by SC inactivation. These results indicate that the subcortical visual circuit can relay reward-predicting visual information to DA neurons and integrity of the SC is necessary for visually-elicited classically conditioned responses after V1 lesion.https://elifesciences.org/articles/24459associative learningdopamine neuronprediction errorsubcortical visionblindsightmonkey
collection DOAJ
language English
format Article
sources DOAJ
author Norihiro Takakuwa
Rikako Kato
Peter Redgrave
Tadashi Isa
spellingShingle Norihiro Takakuwa
Rikako Kato
Peter Redgrave
Tadashi Isa
Emergence of visually-evoked reward expectation signals in dopamine neurons via the superior colliculus in V1 lesioned monkeys
eLife
associative learning
dopamine neuron
prediction error
subcortical vision
blindsight
monkey
author_facet Norihiro Takakuwa
Rikako Kato
Peter Redgrave
Tadashi Isa
author_sort Norihiro Takakuwa
title Emergence of visually-evoked reward expectation signals in dopamine neurons via the superior colliculus in V1 lesioned monkeys
title_short Emergence of visually-evoked reward expectation signals in dopamine neurons via the superior colliculus in V1 lesioned monkeys
title_full Emergence of visually-evoked reward expectation signals in dopamine neurons via the superior colliculus in V1 lesioned monkeys
title_fullStr Emergence of visually-evoked reward expectation signals in dopamine neurons via the superior colliculus in V1 lesioned monkeys
title_full_unstemmed Emergence of visually-evoked reward expectation signals in dopamine neurons via the superior colliculus in V1 lesioned monkeys
title_sort emergence of visually-evoked reward expectation signals in dopamine neurons via the superior colliculus in v1 lesioned monkeys
publisher eLife Sciences Publications Ltd
series eLife
issn 2050-084X
publishDate 2017-06-01
description Responses of midbrain dopamine (DA) neurons reflecting expected reward from sensory cues are critical for reward-based associative learning. However, critical pathways by which reward-related visual information is relayed to DA neurons remain unclear. To address this question, we investigated Pavlovian conditioning in macaque monkeys with unilateral primary visual cortex (V1) lesions (an animal model of ‘blindsight’). Anticipatory licking responses to obtain juice drops were elicited in response to visual conditioned stimuli (CS) in the affected visual field. Subsequent pharmacological inactivation of the superior colliculus (SC) suppressed the anticipatory licking. Concurrent single unit recordings indicated that DA responses reflecting the reward expectation could be recorded in the absence of V1, and that these responses were also suppressed by SC inactivation. These results indicate that the subcortical visual circuit can relay reward-predicting visual information to DA neurons and integrity of the SC is necessary for visually-elicited classically conditioned responses after V1 lesion.
topic associative learning
dopamine neuron
prediction error
subcortical vision
blindsight
monkey
url https://elifesciences.org/articles/24459
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