Synaptic input sequence discrimination on behavioral time-scales mediated by reaction-diffusion chemistry in dendrites

  1. Upinder Singh Bhalla  Is a corresponding author
  1. Tata Institute of Fundamental Research, India

Abstract

Sequences of events are ubiquitous in sensory, motor, and cognitive function. Key computational operations, including pattern recognition, event prediction, and plasticity, involve neural discrimination of spatio-temporal sequences. Here we show that synaptically-driven reaction-diffusion pathways on dendrites can perform sequence discrimination on behaviorally relevant time-scales. We used abstract signaling models to show that selectivity arises when inputs at successive locations are aligned with, and amplified by, propagating chemical waves triggered by previous inputs. We incorporated biological detail using sequential synaptic input onto spines in morphologically, electrically, and chemically detailed pyramidal neuronal models based on rat data. Again, sequences were recognized, and local channel modulation downstream of putative sequence-triggered signaling could elicit changes in neuronal firing. We predict that dendritic sequence-recognition zones occupy 5 to 30 microns and recognize time-intervals of 0.2 to 5s. We suggest that this mechanism provides highly parallel and selective neural computation in a functionally important time range.

Data availability

The following previously published data sets were used
    1. Ascoli GA
    2. Donohue DE
    3. Halavi M
    (2007) NeuroMorpho.org
    Publicly available at NeuroMorpho.org (accession no: NMO_09573).

Article and author information

Author details

  1. Upinder Singh Bhalla

    National Centre for Biological Sciences, Tata Institute of Fundamental Research, Bangalore, India
    For correspondence
    bhalla@ncbs.res.in
    Competing interests
    Upinder Singh Bhalla, Reviewing editor, eLife.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1722-5188

Funding

National Centre for Biological Sciences (Plan 4142)

  • Upinder Singh Bhalla

Department of Science and Technology, Ministry of Science and Technology (SR/CSI/66/2013)

  • Upinder Singh Bhalla

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

Copyright

© 2017, Bhalla

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

  • 2,425
    views
  • 430
    downloads
  • 35
    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. Upinder Singh Bhalla
(2017)
Synaptic input sequence discrimination on behavioral time-scales mediated by reaction-diffusion chemistry in dendrites
eLife 6:e25827.
https://doi.org/10.7554/eLife.25827

Share this article

https://doi.org/10.7554/eLife.25827

Further reading

    1. Genetics and Genomics
    2. Neuroscience
    Tanya Wolff, Mark Eddison ... Gerald M Rubin
    Research Article

    The central complex (CX) plays a key role in many higher-order functions of the insect brain including navigation and activity regulation. Genetic tools for manipulating individual cell types, and knowledge of what neurotransmitters and neuromodulators they express, will be required to gain mechanistic understanding of how these functions are implemented. We generated and characterized split-GAL4 driver lines that express in individual or small subsets of about half of CX cell types. We surveyed neuropeptide and neuropeptide receptor expression in the central brain using fluorescent in situ hybridization. About half of the neuropeptides we examined were expressed in only a few cells, while the rest were expressed in dozens to hundreds of cells. Neuropeptide receptors were expressed more broadly and at lower levels. Using our GAL4 drivers to mark individual cell types, we found that 51 of the 85 CX cell types we examined expressed at least one neuropeptide and 21 expressed multiple neuropeptides. Surprisingly, all co-expressed a small molecule neurotransmitter. Finally, we used our driver lines to identify CX cell types whose activation affects sleep, and identified other central brain cell types that link the circadian clock to the CX. The well-characterized genetic tools and information on neuropeptide and neurotransmitter expression we provide should enhance studies of the CX.

    1. Neuroscience
    Kayson Fakhar, Fatemeh Hadaeghi ... Claus C Hilgetag
    Research Article

    Efficient communication in brain networks is foundational for cognitive function and behavior. However, how communication efficiency is defined depends on the assumed model of signaling dynamics, e.g., shortest path signaling, random walker navigation, broadcasting, and diffusive processes. Thus, a general and model-agnostic framework for characterizing optimal neural communication is needed. We address this challenge by assigning communication efficiency through a virtual multi-site lesioning regime combined with game theory, applied to large-scale models of human brain dynamics. Our framework quantifies the exact influence each node exerts over every other, generating optimal influence maps given the underlying model of neural dynamics. These descriptions reveal how communication patterns unfold if regions are set to maximize their influence over one another. Comparing these maps with a variety of brain communication models showed that optimal communication closely resembles a broadcasting regime in which regions leverage multiple parallel channels for information dissemination. Moreover, we found that the brain’s most influential regions are its rich-club, exploiting their topological vantage point by broadcasting across numerous pathways that enhance their reach even if the underlying connections are weak. Altogether, our work provides a rigorous and versatile framework for characterizing optimal brain communication, and uncovers the most influential brain regions, and the topological features underlying their influence.