The Spatial Dimensions of Electrically Coupled Networks of Interneurons in the Neocortex

Yael Amitai, Jay R. Gibson, Michael Beierlein, Saundra L. Patrick, Alice M. Ho, Barry W. Connors, David Golomb

Research output: Contribution to journalArticle

181 Citations (Scopus)

Abstract

Inhibitory interneurons of the neocortex are electrically coupled to cells of the same type through gap junctions. We studied the spatial organization of two types of interneurons in the rat somatosensory cortex: fast-spiking (FS) parvalbumin-immunoreactive (PV+) cells, and low threshold-spiking (LTS) somatostatin-immunoreactive (SS+) cells. Paired recordings in layer 4 demonstrated that both the probability of coupling and the coupling coefficient drop steeply with intersomatic distance, reaching zero beyond 200 μm. The dendritic arbors of FS and LTS cells were reconstructed from electrophysiologically characterized, biocytin-filled cells; the two cell types had only minor differences in the number and span of their dendrites. However, there was a markedly higher density of PV+ cells than SS+ cells. PV+ cells were densest in layer 4, while SS+ cell density peaked in the subgranular layers. From these data we estimate that there is measurable electrical coupling (directly or indirectly via intermediary cells) between each interneuron and 20-50 others. The large number of electrical synapses implies that each interneuron participates in a large, continuous syncytium. To evaluate the functional significance of these findings, we examined several simple architectures of coupled networks analytically. We present a mathematical method to estimate the average summated coupling conductance that each cell receives from all of its neighbors, and the average leak conductance of individual cells, and we suggest that these have the same order of magnitude. These quantitative results have important implications for the effects of electrical coupling on the dynamic behavior of interneuron networks.

Original languageEnglish (US)
Pages (from-to)4142-4152
Number of pages11
JournalJournal of Neuroscience
Volume22
Issue number10
StatePublished - May 15 2002

Fingerprint

Neocortex
Interneurons
Cell Count
Electrical Synapses
Parvalbumins
Somatosensory Cortex
Gap Junctions
Giant Cells
Dendrites
Somatostatin

Keywords

  • Coupling coefficient
  • Coupling conductance
  • Dendritic fields
  • FS cells
  • Gap junctions
  • Inhibitory interneurons
  • LTS cells
  • Network architecture

ASJC Scopus subject areas

  • Neuroscience(all)

Cite this

Amitai, Y., Gibson, J. R., Beierlein, M., Patrick, S. L., Ho, A. M., Connors, B. W., & Golomb, D. (2002). The Spatial Dimensions of Electrically Coupled Networks of Interneurons in the Neocortex. Journal of Neuroscience, 22(10), 4142-4152.

The Spatial Dimensions of Electrically Coupled Networks of Interneurons in the Neocortex. / Amitai, Yael; Gibson, Jay R.; Beierlein, Michael; Patrick, Saundra L.; Ho, Alice M.; Connors, Barry W.; Golomb, David.

In: Journal of Neuroscience, Vol. 22, No. 10, 15.05.2002, p. 4142-4152.

Research output: Contribution to journalArticle

Amitai, Y, Gibson, JR, Beierlein, M, Patrick, SL, Ho, AM, Connors, BW & Golomb, D 2002, 'The Spatial Dimensions of Electrically Coupled Networks of Interneurons in the Neocortex', Journal of Neuroscience, vol. 22, no. 10, pp. 4142-4152.
Amitai Y, Gibson JR, Beierlein M, Patrick SL, Ho AM, Connors BW et al. The Spatial Dimensions of Electrically Coupled Networks of Interneurons in the Neocortex. Journal of Neuroscience. 2002 May 15;22(10):4142-4152.
Amitai, Yael ; Gibson, Jay R. ; Beierlein, Michael ; Patrick, Saundra L. ; Ho, Alice M. ; Connors, Barry W. ; Golomb, David. / The Spatial Dimensions of Electrically Coupled Networks of Interneurons in the Neocortex. In: Journal of Neuroscience. 2002 ; Vol. 22, No. 10. pp. 4142-4152.
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