Feedforward and feedback inhibition in neostriatal GABAergic spiny neurons

James M. Tepper, Charles J. Wilson, Tibor Koós

Research output: Contribution to journalReview articlepeer-review

146 Scopus citations

Abstract

There are two distinct inhibitory GABAergic circuits in the neostriatum. The feedforward circuit consists of a relatively small population of GABAergic interneurons that receives excitatory input from the neocortex and exerts monosynaptic inhibition onto striatal spiny projection neurons. The feedback circuit comprises the numerous spiny projection neurons and their interconnections via local axon collaterals. This network has long been assumed to provide the majority of striatal GABAergic inhibition and to sharpen and shape striatal output through lateral inhibition, producing increased activity in the most strongly excited spiny cells at the expense of their less strongly excited neighbors. Recent results, mostly from recording experiments of synaptically connected pairs of neurons, have revealed that the two GABAergic circuits differ markedly in terms of the total number of synapses made by each, the strength of the postsynaptic response detected at the soma, the extent of presynaptic convergence and divergence and the net effect of the activation of each circuit on the postsynaptic activity of the spiny neuron. These data have revealed that the feedforward inhibition is powerful and widespread, with spiking in a single interneuron being capable of significantly delaying or even blocking the generation of spikes in a large number of postsynaptic spiny neurons. In contrast, the postsynaptic effects of spiking in a single presynaptic spiny neuron on postsynaptic spiny neurons are weak when measured at the soma, and unable to significantly affect spike timing or generation. Further, reciprocity of synaptic connections between spiny neurons is only rarely observed. These results suggest that the bulk of the fast inhibition that has the strongest effects on spiny neuron spike timing comes from the feedforward interneuronal system whereas the axon collateral feedback system acts principally at the dendrites to control local excitability as well as the overall level of activity of the spiny neuron.

Original languageEnglish (US)
Pages (from-to)272-281
Number of pages10
JournalBrain Research Reviews
Volume58
Issue number2
DOIs
StatePublished - Aug 2008
Externally publishedYes

All Science Journal Classification (ASJC) codes

  • Neuroscience(all)
  • Clinical Neurology

Keywords

  • GABA
  • IPSC
  • IPSP
  • Interneuron
  • Local axon collaterals
  • Neostriatum
  • Paired recording

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