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

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Abstract

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.

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Norihiro Takakuwa

Department of Developmental Physiology, National Institute for Physiological Sciences, Okazaki, Japan

Competing interests
The authors declare that no competing interests exist.
Rikako Kato

Department of Developmental Physiology, National Institute for Physiological Sciences, Okazaki, Japan

Competing interests
The authors declare that no competing interests exist.
Peter Redgrave

Department of Psychology, University of Sheffield, Sheffield, United Kingdom

Competing interests
The authors declare that no competing interests exist.
Tadashi Isa

Department of Developmental Physiology, National Institute for Physiological Sciences, Okazaki, Japan

For correspondence
isa.tadashi.7u@kyoto-u.ac.jp

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0001-5652-4688

Funding

Japan Society for the Promotion of Science (KAKENHI Grant Number 22220006)

Tadashi Isa

Ministry of Education, Culture, Sports, Science, and Technology (26112008)

Tadashi Isa

Japan Society for the Promotion of Science (KAKENHI Grant Number 26221003)

Tadashi Isa

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Ethics

Animal experimentation: All the experimental procedures were performed in accordance with the National Institutes of Health Guidelines for the Care and Use of Laboratory Animals and approved by the Committee for Animal Experiment at the National Institute of Natural Sciences (Permit Number: 16A060).

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This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.