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Gap junctional coupling between retinal amacrine and ganglion cells underlies coherent activity integral to global object perception

  1. Stewart A. Bloomfielda,1
  1. aDepartment of Biological and Vision Sciences, State University of New York College of Optometry, New York, NY 10036
  1. Edited by John E. Dowling, Harvard University, Cambridge, MA, and approved October 11, 2017 (received for review May 18, 2017)

Significance

Neuron ensembles in the brain visual system often show correlated responses, but the sensory information encoded by this activity remains unclear. Here, we show that widely separated ganglion cells in the mouse retina show correlated activity when presented with a large, contiguous object, but not when the object is disjointed. We show that these long-range correlations are produced by electrical coupling via gap junctions made with polyaxonal amacrine cells, which can span distances greater than a millimeter. Blockade or ablation of these gap junctions eliminates correlations between distant ganglion cells and, moreover, diminishes an animal’s ability to discriminate large, solid objects from disjointed ones. Our findings indicate that long-range correlated activity in the retina encodes visual information critical for global object perception.

Abstract

Coherent spike activity occurs between widely separated retinal ganglion cells (RGCs) in response to a large, contiguous object, but not to disjointed objects. Since the large spatial separation between the RGCs precludes common excitatory inputs from bipolar cells, the mechanism underlying this long-range coherence remains unclear. Here, we show that electrical coupling between RGCs and polyaxonal amacrine cells in mouse retina forms the synaptic mechanism responsible for long-range coherent activity in the retina. Pharmacological blockade of gap junctions or genetic ablation of connexin 36 (Cx36) subunits eliminates the long-range correlated spiking between RGCs. Moreover, we find that blockade of gap junctions or ablation of Cx36 significantly reduces the ability of mice to discriminate large, global objects from small, disjointed stimuli. Our results indicate that synchronous activity of RGCs, derived from electrical coupling with amacrine cells, encodes information critical to global object perception.

Footnotes

  • ?1To whom correspondence should be addressed. Email: sbloomfield{at}sunyopt.edu.
  • Author contributions: K.R. and S.A.B. designed research; K.R., S.K., and S.A.B. performed research; K.R., S.K., and S.A.B. analyzed data; and K.R., S.K., and S.A.B. wrote the paper.

  • The authors declare no conflict of interest.

  • This article is a PNAS Direct Submission.

  • This article contains supporting information online at www.danielhellerman.com/lookup/suppl/doi:10.1073/pnas.1708261114/-/DCSupplemental.

Published under the PNAS license.

Online Impact

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