Persistent coding of outcome-predictive cue features in the rat nucleus accumbens
Abstract
The nucleus accumbens (NAc) is important for learning from feedback, and for biasing and invigorating behavior in response to cues that predict motivationally relevant outcomes. NAc encodes outcome-related cue features such as the magnitude and identity of reward. However, little is known about how features of cues themselves are encoded. We designed a decision making task where rats learned multiple sets of outcome-predictive cues, and recorded single-unit activity in the NAc during performance. We found that coding of cue identity and location occurred alongside coding of expected outcome. Furthermore, this coding persisted both during a delay period, after the rat made a decision and was waiting for an outcome, and after the outcome was revealed. Encoding of cue features in the NAc may enable contextual modulation of ongoing behavior, and provide an eligibility trace of outcome-predictive stimuli for updating stimulus-outcome associations to inform future behavior.
Data availability
Preprocessed data and data analysis code, sufficient to reproduce the results in the paper, are available on this public GitHub repository: https://github.com/jgmaz/vStrCueCodingPaper (commit 56c5f52).
Article and author information
Author details
Funding
Natural Sciences and Engineering Research Council of Canada
- James E Carmichael
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Reviewing Editor
- Geoffrey Schoenbaum, National Institute on Drug Abuse, National Institutes of Health, United States
Ethics
Animal experimentation: All experimental procedures were approved by the the University of Waterloo Animal Care Committee (protocol# 11-06) and carried out in accordance with Canadian Council for Animal Care (CCAC) guidelines.
Version history
- Received: April 5, 2018
- Accepted: September 15, 2018
- Accepted Manuscript published: September 20, 2018 (version 1)
- Version of Record published: October 16, 2018 (version 2)
Copyright
© 2018, Gmaz 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
-
- 1,882
- views
-
- 278
- downloads
-
- 11
- citations
Views, downloads and citations are aggregated across all versions of this paper published by eLife.
Download links
Downloads (link to download the article as PDF)
Open citations (links to open the citations from this article in various online reference manager services)
Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)
Further reading
-
- Neuroscience
Dopamine axons are the only axons known to grow during adolescence. Here, using rodent models, we examined how two proteins, Netrin-1 and its receptor, UNC5C, guide dopamine axons toward the prefrontal cortex and shape behaviour. We demonstrate in mice (Mus musculus) that dopamine axons reach the cortex through a transient gradient of Netrin-1-expressing cells – disrupting this gradient reroutes axons away from their target. Using a seasonal model (Siberian hamsters; Phodopus sungorus) we find that mesocortical dopamine development can be regulated by a natural environmental cue (daylength) in a sexually dimorphic manner – delayed in males, but advanced in females. The timings of dopamine axon growth and UNC5C expression are always phase-locked. Adolescence is an ill-defined, transitional period; we pinpoint neurodevelopmental markers underlying this period.
-
- Neuroscience
Acetylcholine is released in visual cortex by axonal projections from the basal forebrain. The signals conveyed by these projections and their computational significance are still unclear. Using two-photon calcium imaging in behaving mice, we show that basal forebrain cholinergic axons in the mouse visual cortex provide a binary locomotion state signal. In these axons, we found no evidence of responses to visual stimuli or visuomotor prediction errors. While optogenetic activation of cholinergic axons in visual cortex in isolation did not drive local neuronal activity, when paired with visuomotor stimuli, it resulted in layer-specific increases of neuronal activity. Responses in layer 5 neurons to both top-down and bottom-up inputs were increased in amplitude and decreased in latency, whereas those in layer 2/3 neurons remained unchanged. Using opto- and chemogenetic manipulations of cholinergic activity, we found acetylcholine to underlie the locomotion-associated decorrelation of activity between neurons in both layer 2/3 and layer 5. Our results suggest that acetylcholine augments the responsiveness of layer 5 neurons to inputs from outside of the local network, possibly enabling faster switching between internal representations during locomotion.