Connexon connexions in the thalamocortical system

Academic Article

Abstract

  • Electrical synapses are composed of gap junction channels that interconnect neurons. They occur throughout the mammalian brain, although this has been appreciated only recently. Gap junction channels, which are made of proteins called connexins, allow ionic current and small organic molecules to pass directly between cells, usually with symmetrical ease. Here we review evidence that electrical synapses are a major feature of the inhibitory circuitry in the thalamocortical system. In the neocortex, pairs of neighboring inhibitory interneurons are often electrically coupled, and these electrical connections are remarkably specific. To date, there is evidence that five distinct subtypes of inhibitory interneurons in the cortex make electrical interconnections selectively with interneurons of the same subtype. Excitatory neurons (i.e., pyramidal and spiny stellate cells) of the mature cortex do not appear to make electrical synapses. Within the thalamus, electrical coupling is observed in the reticular nucleus, which is composed entirely of GABAergic neurons. Some pairs of inhibitory neurons in the cortex and reticular thalamus have mixed synaptic connections: chemical (GABAergic) inhibitory synapses operating in parallel with electrical synapses. Inhibitory neurons of the thalamus and cortex express the gap junction protein connexin36 (C×36), and knocking out its gene abolishes nearly all of their electrical synapses. The electrical synapses of the thalamocortical system are strong enough to mediate robust interactions between inhibitory neurons. When pairs or groups of electrically coupled cells are excited by synaptic input, receptor agonists, or injected current, they typically display strong synchrony of both subthreshold voltage fluctuations and spikes. For example, activating metabotropic glutamate receptors on coupled pairs of cortical interneurons or on thalamic reticular neurons can induce rhythmic action potentials that are synchronized with millisecond precision. Electrical synapses offer a uniquely fast, bidirectional mechanism for coordinating local neural activity. Their widespread distribution in the thalamocortical system suggests that they serve myriad functions. We are far from a complete understanding of those functions, but recent experiments suggest that electrical synapses help to coordinate the temporal and spatial features of various forms of neural activity. Copyright © 2005 Elsevier BV. All rights reserved.
  • Published In

    Digital Object Identifier (doi)

    Author List

  • Cruikshank SJ; Landisman CE; Mancilla JG; Connors BW
  • Start Page

  • 41
  • End Page

  • 57
  • Volume

  • 149