Dendritic nonlinearities are tuned for efficient spike-based computations in cortical circuits

  1. Balazs B Ujfalussy  Is a corresponding author
  2. Judit K Makara
  3. Tiago Branco
  4. Máté Lengyel
  1. University of Cambridge, United Kingdom
  2. Institute of Experimental Medicine, Hungary
  3. MRC Laboratory of Molecular Biology, United Kingdom

Abstract

Cortical neurons integrate thousands of synaptic inputs in their dendrites in highly nonlinear ways. It is unknown how these dendritic nonlinearities in individual cells contribute to computations at the level of neural circuits. Here we show that dendritic nonlinearities are critical for the efficient integration of synaptic inputs in circuits performing analog computations with spiking neurons. We developed a theory that formalises how a neuron's dendritic nonlinearity that is optimal for integrating synaptic inputs depends on the statistics of its presynaptic activity patterns. Based on their in vivo preynaptic population statistics (firing rates, membrane potential fluctuations, and correlations due to ensemble dynamics), our theory accurately predicted the responses of two different types of cortical pyramidal cells to patterned stimulation by two-photon glutamate uncaging. These results reveal a new computational principle underlying dendritic integration in cortical neurons by suggesting a functional link between cellular and systems-level properties of cortical circuits.

Article and author information

Author details

  1. Balazs B Ujfalussy

    Computational and Biological Learning Lab, Department of Engineering, University of Cambridge, Cambridge, United Kingdom
    For correspondence
    balazs.ujfalussy@gmail.com
    Competing interests
    The authors declare that no competing interests exist.
  2. Judit K Makara

    Lendület Laboratory of Neuronal Signaling, Institute of Experimental Medicine, Budapest, Hungary
    Competing interests
    The authors declare that no competing interests exist.
  3. Tiago Branco

    MRC Laboratory of Molecular Biology, Cambridge, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  4. Máté Lengyel

    Computational and Biological Learning Lab, Department of Engineering, University of Cambridge, Cambridge, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.

Reviewing Editor

  1. Frances K Skinner, University Health Network, Canada

Ethics

Animal experimentation: Hippocampal experiments were conducted according to methods approved by the Janelia Farm Institutional Animal Care and Use Committee and 26 the Animal Care and Use Committee (ACUC) of the Institute of Experimental Medicine, Hungarian Academy of 27 Sciences, and in accordance with 86/609/EEC/2 and DIRECTIVE 2010/63/EU Directives of the EU. Neocortical experiments were performed in strict accordance with guidelines of the Wolfson Institute for Biomedical Research and with the national guidelines.

Version history

  1. Received: July 14, 2015
  2. Accepted: December 23, 2015
  3. Accepted Manuscript published: December 24, 2015 (version 1)
  4. Version of Record published: March 31, 2016 (version 2)

Copyright

© 2015, Ujfalussy 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

  • 2,892
    views
  • 849
    downloads
  • 22
    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. Balazs B Ujfalussy
  2. Judit K Makara
  3. Tiago Branco
  4. Máté Lengyel
(2015)
Dendritic nonlinearities are tuned for efficient spike-based computations in cortical circuits
eLife 4:e10056.
https://doi.org/10.7554/eLife.10056

Share this article

https://doi.org/10.7554/eLife.10056

Further reading

    1. Neuroscience
    Songyao Zhang, Tuo Zhang ... Tianming Liu
    Research Article

    Cortical folding is an important feature of primate brains that plays a crucial role in various cognitive and behavioral processes. Extensive research has revealed both similarities and differences in folding morphology and brain function among primates including macaque and human. The folding morphology is the basis of brain function, making cross-species studies on folding morphology important for understanding brain function and species evolution. However, prior studies on cross-species folding morphology mainly focused on partial regions of the cortex instead of the entire brain. Previously, our research defined a whole-brain landmark based on folding morphology: the gyral peak. It was found to exist stably across individuals and ages in both human and macaque brains. Shared and unique gyral peaks in human and macaque are identified in this study, and their similarities and differences in spatial distribution, anatomical morphology, and functional connectivity were also dicussed.

    1. Neuroscience
    Avani Koparkar, Timothy L Warren ... Lena Veit
    Research Article

    Complex skills like speech and dance are composed of ordered sequences of simpler elements, but the neuronal basis for the syntactic ordering of actions is poorly understood. Birdsong is a learned vocal behavior composed of syntactically ordered syllables, controlled in part by the songbird premotor nucleus HVC (proper name). Here, we test whether one of HVC’s recurrent inputs, mMAN (medial magnocellular nucleus of the anterior nidopallium), contributes to sequencing in adult male Bengalese finches (Lonchura striata domestica). Bengalese finch song includes several patterns: (1) chunks, comprising stereotyped syllable sequences; (2) branch points, where a given syllable can be followed probabilistically by multiple syllables; and (3) repeat phrases, where individual syllables are repeated variable numbers of times. We found that following bilateral lesions of mMAN, acoustic structure of syllables remained largely intact, but sequencing became more variable, as evidenced by ‘breaks’ in previously stereotyped chunks, increased uncertainty at branch points, and increased variability in repeat numbers. Our results show that mMAN contributes to the variable sequencing of vocal elements in Bengalese finch song and demonstrate the influence of recurrent projections to HVC. Furthermore, they highlight the utility of species with complex syntax in investigating neuronal control of ordered sequences.