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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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 |
work_keys_str_mv |
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1721461546866966528 |