1. Neuroscience
Download icon

Distributed coding of duration in rodent prefrontal cortex during time reproduction

  1. Josephine Henke
  2. David Bunk
  3. Dina von Werder
  4. Stefan Häusler
  5. Virginia L Flanagin
  6. Kay Thurley  Is a corresponding author
  1. Ludwig-Maximilians-Universitaet Muenchen, Germany
Research Article
  • Cited 0
  • Views 388
  • Annotations
Cite this article as: eLife 2021;10:e71612 doi: 10.7554/eLife.71612

Abstract

As we interact with the external world, we judge magnitudes from sensory information. The estimation of magnitudes has been characterized in primates, yet it is largely unexplored in non-primate species. Here we use time interval reproduction to study rodent behavior and its neural correlates in the context of magnitude estimation. We show that gerbils display primate-like magnitude estimation characteristics in time reproduction. Most prominently their behavioral responses show a systematic overestimation of small stimuli and an underestimation of large stimuli, often referred to as regression effect. We investigated the underlying neural mechanisms by recording from medial prefrontal cortex and show that the majority of neurons respond either during the measurement or the reproduction of a time interval. Cells that are active during both phases display distinct response patterns. We categorize the neural responses into multiple types and demonstrate that only populations with mixed responses can encode the bias of the regression effect. These results help unveil the organizing neural principles of time reproduction and perhaps magnitude estimation in general.

Data availability

Raw data for this study are available at https://doi.org/10.12751/g-node.tarvrs (Henke et al., 2021).In addition, source data are given when mentioned in the respective figures.

The following data sets were generated

Article and author information

Author details

  1. Josephine Henke

    Faculty of Biology, Ludwig-Maximilians-Universitaet Muenchen, Planegg-Martinsried, Germany
    Competing interests
    The authors declare that no competing interests exist.
  2. David Bunk

    Faculty of Biology, Ludwig-Maximilians-Universitaet Muenchen, Planegg-Martinsried, Germany
    Competing interests
    The authors declare that no competing interests exist.
  3. Dina von Werder

    Faculty of Biology, Ludwig-Maximilians-Universitaet Muenchen, Planegg-Martinsried, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4193-5203
  4. Stefan Häusler

    Faculty of Biology, Ludwig-Maximilians-Universitaet Muenchen, Planegg-Martinsried, Germany
    Competing interests
    The authors declare that no competing interests exist.
  5. Virginia L Flanagin

    German Center for Vertigo and Balance Disorders,, Ludwig-Maximilians-Universitaet Muenchen, Munich, Germany
    Competing interests
    The authors declare that no competing interests exist.
  6. Kay Thurley

    Faculty of Biology, Ludwig-Maximilians-Universitaet Muenchen, Planegg-Martinsried, Germany
    For correspondence
    thurley@bio.lmu.de
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4857-1083

Funding

Bundesministerium für Bildung, Wissenschaft und Forschung (01GQ1004A)

  • Josephine Henke
  • Kay Thurley

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 experiments were approved according to national and European guidelines on animal welfare (Reg. von Oberbayern, District Government of Upper Bavaria; reference numbers: AZ 55.2-1-54-2532-10-11 and AZ 55.2-1-54-2532-70-2016).

Reviewing Editor

  1. Hugo Merchant, National Autonomous University of Mexico, Mexico

Publication history

  1. Received: June 24, 2021
  2. Accepted: December 14, 2021
  3. Accepted Manuscript published: December 23, 2021 (version 1)

Copyright

© 2021, Henke 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

  • 388
    Page views
  • 96
    Downloads
  • 0
    Citations

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

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
    Christian Brodbeck et al.
    Research Article

    Speech processing is highly incremental. It is widely accepted that human listeners continuously use the linguistic context to anticipate upcoming concepts, words, and phonemes. However, previous evidence supports two seemingly contradictory models of how a predictive context is integrated with the bottom-up sensory input: Classic psycholinguistic paradigms suggest a two-stage process, in which acoustic input initially leads to local, context-independent representations, which are then quickly integrated with contextual constraints. This contrasts with the view that the brain constructs a single coherent, unified interpretation of the input, which fully integrates available information across representational hierarchies, and thus uses contextual constraints to modulate even the earliest sensory representations. To distinguish these hypotheses, we tested magnetoencephalography responses to continuous narrative speech for signatures of local and unified predictive models. Results provide evidence that listeners employ both types of models in parallel. Two local context models uniquely predict some part of early neural responses, one based on sublexical phoneme sequences, and one based on the phonemes in the current word alone; at the same time, even early responses to phonemes also reflect a unified model that incorporates sentence level constraints to predict upcoming phonemes. Neural source localization places the anatomical origins of the different predictive models in non-identical parts of the superior temporal lobes bilaterally, with the right hemisphere showing a relative preference for more local models. These results suggest that speech processing recruits both local and unified predictive models in parallel, reconciling previous disparate findings. Parallel models might make the perceptual system more robust, facilitate processing of unexpected inputs, and serve a function in language acquisition.

    1. Neuroscience
    Travis A Hage et al.
    Research Article

    Understanding cortical microcircuits requires thorough measurement of physiological properties of synaptic connections formed within and between diverse subclasses of neurons. Towards this goal, we combined spatially precise optogenetic stimulation with multicellular recording to deeply characterize intralaminar and translaminar monosynaptic connections to supragranular (L2/3) neurons in the mouse visual cortex. The reliability and specificity of multiphoton optogenetic stimulation were measured across multiple Cre lines and measurements of connectivity were verified by comparison to paired recordings and targeted patching of optically identified presynaptic cells. With a focus on translaminar pathways, excitatory and inhibitory synaptic connections from genetically defined presynaptic populations were characterized by their relative abundance, spatial profiles, strength, and short-term dynamics. Consistent with the canonical cortical microcircuit, layer 4 excitatory neurons and interneurons within L2/3 represented the most common sources of input to L2/3 pyramidal cells. More surprisingly, we also observed strong excitatory connections from layer 5 intratelencephalic neurons and potent translaminar inhibition from multiple interneuron subclasses. The hybrid approach revealed convergence to and divergence from excitatory and inhibitory neurons within and across cortical layers. Divergent excitatory connections often spanned hundreds of microns of horizontal space. In contrast, divergent inhibitory connections were more frequently measured from postsynaptic targets near each other.