1. Neuroscience
Download icon

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

  1. Norihiro Takakuwa
  2. Rikako Kato
  3. Peter Redgrave
  4. Tadashi Isa  Is a corresponding author
  1. National Institute for Physiological Sciences, Japan
  2. University of Sheffield, United Kingdom
Research Article
  • Cited 20
  • Views 2,256
  • Annotations
Cite this article as: eLife 2017;6:e24459 doi: 10.7554/eLife.24459

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.

Article and author information

Author details

  1. Norihiro Takakuwa

    Department of Developmental Physiology, National Institute for Physiological Sciences, Okazaki, Japan
    Competing interests
    The authors declare that no competing interests exist.
  2. Rikako Kato

    Department of Developmental Physiology, National Institute for Physiological Sciences, Okazaki, Japan
    Competing interests
    The authors declare that no competing interests exist.
  3. Peter Redgrave

    Department of Psychology, University of Sheffield, Sheffield, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  4. 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.
    ORCID icon "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).

Reviewing Editor

  1. Naoshige Uchida, Harvard University, United States

Publication history

  1. Received: December 20, 2016
  2. Accepted: June 15, 2017
  3. Accepted Manuscript published: June 19, 2017 (version 1)
  4. Version of Record published: July 26, 2017 (version 2)

Copyright

© 2017, Takakuwa et al.

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.

Metrics

  • 2,256
    Page views
  • 452
    Downloads
  • 20
    Citations

Article citation count generated by polling the highest count across the following sources: Scopus, Crossref, PubMed Central.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Download citations (links to download the citations from this article in formats compatible with various reference manager tools)

Open citations (links to open the citations from this article in various online reference manager services)

Further reading

    1. Neuroscience
    P Christiaan Klink et al.
    Research Article Updated

    Population receptive field (pRF) modeling is a popular fMRI method to map the retinotopic organization of the human brain. While fMRI-based pRF maps are qualitatively similar to invasively recorded single-cell receptive fields in animals, it remains unclear what neuronal signal they represent. We addressed this question in awake nonhuman primates comparing whole-brain fMRI and large-scale neurophysiological recordings in areas V1 and V4 of the visual cortex. We examined the fits of several pRF models based on the fMRI blood-oxygen-level-dependent (BOLD) signal, multi-unit spiking activity (MUA), and local field potential (LFP) power in different frequency bands. We found that pRFs derived from BOLD-fMRI were most similar to MUA-pRFs in V1 and V4, while pRFs based on LFP gamma power also gave a good approximation. fMRI-based pRFs thus reliably reflect neuronal receptive field properties in the primate brain. In addition to our results in V1 and V4, the whole-brain fMRI measurements revealed retinotopic tuning in many other cortical and subcortical areas with a consistent increase in pRF size with increasing eccentricity, as well as a retinotopically specific deactivation of default mode network nodes similar to previous observations in humans.

    1. Developmental Biology
    2. Neuroscience
    Eduardo Loureiro-Campos et al.
    Research Article

    The transcription factor activating protein two gamma (AP2γ) is an important regulator of neurogenesis both during embryonic development as well as in the postnatal brain, but its role for neurophysiology and behavior at distinct postnatal periods is still unclear. In this work, we explored the neurogenic, behavioral, and functional impact of a constitutive and heterozygous AP2γ deletion in mice from early postnatal development until adulthood. AP2γ deficiency promotes downregulation of hippocampal glutamatergic neurogenesis, altering the ontogeny of emotional and memory behaviors associated with hippocampus formation. The impairments induced by AP2γ constitutive deletion since early development leads to an anxious-like phenotype and memory impairments as early as the juvenile phase. These behavioral impairments either persist from the juvenile phase to adulthood or emerge in adult mice with deficits in behavioral flexibility and object location recognition. Collectively, we observed a progressive and cumulative impact of constitutive AP2γ deficiency on the hippocampal glutamatergic neurogenic process, as well as alterations on limbic-cortical connectivity, together with functional behavioral impairments. The results herein presented demonstrate the modulatory role exerted by the AP2γ transcription factor and the relevance of hippocampal neurogenesis in the development of emotional states and memory processes.