Interneuron Diversity series: Circuit complexity and axon wiring economy of cortical interneurons

https://doi.org/10.1016/j.tins.2004.02.007Get rights and content

Abstract

The performance of the brain is constrained by wiring length and maintenance costs. The apparently inverse relationship between number of neurons in the various interneuron classes and the spatial extent of their axon trees suggests a mathematically definable organization, reminiscent of ‘small-world’ or scale-free networks observed in other complex systems. The wiring-economy-based classification of cortical inhibitory interneurons is supported by the distinct physiological patterns of class members in the intact brain. The complex wiring of diverse interneuron classes could represent an economic solution for supporting global synchrony and oscillations at multiple timescales with minimum axon length.

Section snippets

Building networks for multiple functions

The repertoire and complexity of network performance can be augmented in two fundamentally different ways. The first approach is to use relatively few constituents in large numbers. However, physical realization of this approach in growing networks is problematic. If the network is sparsely connected (e.g. feedforward ‘synfire’ chains of pyramidal cells across many layers [9]), signals become too long to propagate across the network owing to synaptic and conduction delays. However, if the

Scalable interneuronal clocks: connectivity is of the essence

Complex brains have developed specialized mechanisms for keeping time: inhibitory interneuron networks [23]. Oscillatory timing can transform unconnected principal cell groups into temporal coalitions, providing maximal flexibility and economic use of their spikes [24]. Various architectures of inhibitory and excitatory neurons can give rise to oscillations 25, 26, 27, 28. The simplest one consists of interneurons of the same type 26, 28, 29, 30, 31, 32, 33, 34. Let us illustrate the importance

Functional diversity of interneurons increases computational power at a low wiring cost

As already discussed, integrating functionally novel types of neurons into networks increases their computational diversity 12, 13. Functionality can be defined by the intrinsic, biophysical properties of interneurons 1, 3, 4, 6 and/or by their placement in the network [43]. In terms of their connectivity to the principal cells 2, 5, 13, 44, three major groups of cortical interneurons are recognized: (i) interneurons controlling principal cell output (by perisomatic inhibition), (ii)

Concluding remarks

This review has considered whether, and how, the diversity of cortical interneurons reflects optimization between computational performance of the cortex and its axonal wiring costs. In their relationship to principal cells, three major classes of interneurons are recognized: (i) interneurons controlling principal cell output, (ii) interneurons controlling dendritic inputs and (iii) long-range interneurons coordinating interneuron assemblies. Each class has several further divisions. The number

Acknowledgements

We thank A-L. Barabasi, T.F. Freund, A. Gulyas, K.D. Harris, K. Kaila, N. Logothetis, M. Raichle and the referees for comments and criticism. Our work is supported by NIH and NIMH.

References (60)

  • M.A. Whittington et al.

    Interneuron Diversity series: Inhibitory interneurons and network oscillations in vitro

    Trends Neurosci.

    (2003)
  • G. Buzsaki

    Hippocampal evoked potentials and EEG changes during classical conditioning in the rat

    Electroencephalogr. Clin. Neurophysiol.

    (1979)
  • T.F. Freund

    Interneuron Diversity series: Rhythm and mood in perisomatic inhibition

    Trends Neurosci.

    (2003)
  • R. Miles

    Differences between somatic and dendritic inhibition in the hippocampus

    Neuron

    (1996)
  • T.F. Freund et al.

    Interneurons of the hippocampus

    Hippocampus

    (1996)
  • A. Gupta

    Organizing principles for a diversity of GABAergic interneurons and synapses in the neocortex

    Science

    (2000)
  • C.J. McBain et al.

    Interneurons unbound

    Nat. Rev. Neurosci.

    (2001)
  • Y. Kawaguchi et al.

    GABAergic cell subtypes and their synaptic connections in rat frontal cortex

    Cereb. Cortex

    (1997)
  • M. Abeles

    Corticonics

    (1991)
  • R. Sarpeshkar

    Analog versus digital: extrapolating from electronics to neurobiology

    Neural Comput.

    (1998)
  • J.M. Allman

    Evolving Brains

    (1998)
  • M.A. Changizi

    The Brain from 25,000 feet: High Level Explorations of Brain Complexity, Perception, Induction and Vagueness

    (2003)
  • A.-L. Barabási

    Linked: the New Science of Networks

    (2002)
  • D.J. Watts et al.

    Collective dynamics of ‘small-world’ networks

    Nature

    (1998)
  • S.B. Laughlin et al.

    Communication in neuronal networks

    Science

    (2003)
  • O. Sporns

    Theoretical neuroanatomy: relating anatomical and functional connectivity in graphs and cortical connection matrices

    Cereb. Cortex

    (2000)
  • C. Koch et al.

    Complexity and the nervous system

    Science

    (1999)
  • G. Tamas

    Identified sources and targets of slow inhibition in the neocortex

    Science

    (2003)
  • X.J. Wang

    Division of labor among distinct subtypes of inhibitory neurons in a cortical microcircuit of working memory

    Proc. Natl. Acad. Sci. U. S. A.

    (2004)
  • N. Kopell et al.

    Symmetry and phase-locking in chains of weakly coupled oscillators

    Comm. Pure Appl. Math.

    (1986)
  • Cited by (397)

    • Explosive synchronization of weighted mobile oscillators

      2022, Physica A: Statistical Mechanics and its Applications
    View all citing articles on Scopus
    View full text