Abstract

The striatum is an input structure of the basal ganglia implicated in several time-dependent functions including reinforcement learning, decision making, and interval timing. To determine whether striatal ensembles drive subjects' judgments of duration, we manipulated and recorded from striatal neurons in rats performing a duration categorization psychophysical task. We found that the dynamics of striatal neurons predicted duration judgments, and that simultaneously recorded ensembles could judge duration as well as the animal. Furthermore, striatal neurons were necessary for duration judgments, as muscimol infusions produced a specific impairment in animals' duration sensitivity. Lastly, we show that time as encoded by striatal populations ran faster or slower when rats judged a duration as longer or shorter, respectively. These results demonstrate that the speed with which striatal population state changes supports the fundamental ability of animals to judge the passage of time.

Article and author information

Author details

  1. Thiago S Gouvêa

    Champalimaud Neuroscience Programme, Champalimaud Centre for the Unknown, Lisbon, Portugal
    Competing interests
    The authors declare that no competing interests exist.
  2. Tiago Monteiro

    Champalimaud Neuroscience Programme, Champalimaud Centre for the Unknown, Lisbon, Portugal
    Competing interests
    The authors declare that no competing interests exist.
  3. Asma Motiwala

    Champalimaud Neuroscience Programme, Champalimaud Centre for the Unknown, Lisbon, Portugal
    Competing interests
    The authors declare that no competing interests exist.
  4. Sofia Soares

    Champalimaud Neuroscience Programme, Champalimaud Centre for the Unknown, Lisbon, Portugal
    Competing interests
    The authors declare that no competing interests exist.
  5. Christian Machens

    Champalimaud Neuroscience Programme, Champalimaud Centre for the Unknown, Lisbon, Portugal
    Competing interests
    The authors declare that no competing interests exist.
  6. Joseph J Paton

    Champalimaud Neuroscience Programme, Champalimaud Centre for the Unknown, Lisbon, Portugal
    For correspondence
    joe.paton@neuro.fchampalimaud.org
    Competing interests
    The authors declare that no competing interests exist.

Reviewing Editor

  1. Timothy Behrens, Oxford University, United Kingdom

Ethics

Animal experimentation: All experiments were in accordance with the European Union Directive 86/609/EEC and approved by the Portuguese Veterinary General Board (Direcção-Geral de Veterinária, project approval 014303 - 0420/000/000/2011)

Version history

  1. Received: September 3, 2015
  2. Accepted: December 7, 2015
  3. Accepted Manuscript published: December 7, 2015 (version 1)
  4. Version of Record published: January 12, 2016 (version 2)

Copyright

© 2015, Gouvêa 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

  • 6,591
    views
  • 1,324
    downloads
  • 145
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

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)

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)

  1. Thiago S Gouvêa
  2. Tiago Monteiro
  3. Asma Motiwala
  4. Sofia Soares
  5. Christian Machens
  6. Joseph J Paton
(2015)
Striatal dynamics explain duration judgments
eLife 4:e11386.
https://doi.org/10.7554/eLife.11386

Share this article

https://doi.org/10.7554/eLife.11386

Further reading

    1. Neuroscience
    Anja T Zai, Anna E Stepien ... Richard HR Hahnloser
    Research Article

    Songbirds’ vocal mastery is impressive, but to what extent is it a result of practice? Can they, based on experienced mismatch with a known target, plan the necessary changes to recover the target in a practice-free manner without intermittently singing? In adult zebra finches, we drive the pitch of a song syllable away from its stable (baseline) variant acquired from a tutor, then we withdraw reinforcement and subsequently deprive them of singing experience by muting or deafening. In this deprived state, birds do not recover their baseline song. However, they revert their songs toward the target by about 1 standard deviation of their recent practice, provided the sensory feedback during the latter signaled a pitch mismatch with the target. Thus, targeted vocal plasticity does not require immediate sensory experience, showing that zebra finches are capable of goal-directed vocal planning.

    1. Neuroscience
    Amanda Chu, Nicholas T Gordon ... Michael A McDannald
    Research Article Updated

    Pavlovian fear conditioning has been extensively used to study the behavioral and neural basis of defensive systems. In a typical procedure, a cue is paired with foot shock, and subsequent cue presentation elicits freezing, a behavior theoretically linked to predator detection. Studies have since shown a fear conditioned cue can elicit locomotion, a behavior that – in addition to jumping, and rearing – is theoretically linked to imminent or occurring predation. A criticism of studies observing fear conditioned cue-elicited locomotion is that responding is non-associative. We gave rats Pavlovian fear discrimination over a baseline of reward seeking. TTL-triggered cameras captured 5 behavior frames/s around cue presentation. Experiment 1 examined the emergence of danger-specific behaviors over fear acquisition. Experiment 2 examined the expression of danger-specific behaviors in fear extinction. In total, we scored 112,000 frames for nine discrete behavior categories. Temporal ethograms show that during acquisition, a fear conditioned cue suppresses reward seeking and elicits freezing, but also elicits locomotion, jumping, and rearing – all of which are maximal when foot shock is imminent. During extinction, a fear conditioned cue most prominently suppresses reward seeking, and elicits locomotion that is timed to shock delivery. The independent expression of these behaviors in both experiments reveals a fear conditioned cue to orchestrate a temporally organized suite of behaviors.