Gap Junctional Coupling Between Retinal Amacrine and Ganglion Cells Underlies Coherent Activity Integral to Global Object Perception

Overview

Journal Proc Natl Acad Sci U S A

Specialty Science

Date 2017 Nov 15

PMID 29133423

Citations 25

Authors

Kaushambi Roy

Sandeep Kumar

Stewart A Bloomfield

Affiliations

Soon will be listed here.

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.

Citing Articles

Retinal ganglion cells encode the direction of motion outside their classical receptive field.

Riccitelli S, Yaakov H, Heukamp A, Ankri L, Rivlin-Etzion M Proc Natl Acad Sci U S A. 2025; 122(1):e2415223122.

PMID: 39793063 PMC: 11725840. DOI: 10.1073/pnas.2415223122.

Gap junctions fine-tune ganglion cell signals to equalize response kinetics within a given electrically coupled array.

Szarka G, Ganczer A, Balogh M, Tengolics A, Futacsi A, Kenyon G iScience. 2024; 27(6):110099.

PMID: 38947503 PMC: 11214328. DOI: 10.1016/j.isci.2024.110099.

Connexins Biology in the Pathophysiology of Retinal Diseases.

Ponce-Mora A, Yuste A, Perini-Villanueva G, Miranda M, Bejarano E Adv Exp Med Biol. 2023; 1415:229-234.

PMID: 37440038 DOI: 10.1007/978-3-031-27681-1_33.

On the Functional Role of Gamma Synchronization in the Retinogeniculate System of the Cat.

Neuenschwander S, Rosso G, Branco N, Freitag F, Tehovnik E, Schmidt K J Neurosci. 2023; 43(28):5204-5220.

PMID: 37328291 PMC: 10342227. DOI: 10.1523/JNEUROSCI.1550-22.2023.

Analytical methods for assessing retinal cell coupling using cut-loading.

Myles W, McFadden S PLoS One. 2022; 17(7):e0271744.

PMID: 35853039 PMC: 9295955. DOI: 10.1371/journal.pone.0271744.

References

Hu E, Bloomfield S . Gap junctional coupling underlies the short-latency spike synchrony of retinal alpha ganglion cells. J Neurosci. 2003; 23(17):6768-77. PMC: 6740719. View

Kenyon G, Travis B, Theiler J, George J, Stephens G, Marshak D . Stimulus-specific oscillations in a retinal model. IEEE Trans Neural Netw. 2004; 15(5):1083-91. DOI: 10.1109/TNN.2004.832722. View

Prusky G, West P, Douglas R . Behavioral assessment of visual acuity in mice and rats. Vision Res. 2000; 40(16):2201-9. DOI: 10.1016/s0042-6989(00)00081-x. View

Marc R, Jones B . Molecular phenotyping of retinal ganglion cells. J Neurosci. 2002; 22(2):413-27. PMC: 6758675. View

Roelfsema P, Singer W . Detecting connectedness. Cereb Cortex. 1998; 8(5):385-96. DOI: 10.1093/cercor/8.5.385. View

van Wyk M, Wassle H, Taylor W . Receptive field properties of ON- and OFF-ganglion cells in the mouse retina. Vis Neurosci. 2009; 26(3):297-308. PMC: 2874828. DOI: 10.1017/S0952523809990137. View

Singer W, Gray C . Visual feature integration and the temporal correlation hypothesis. Annu Rev Neurosci. 1995; 18:555-86. DOI: 10.1146/annurev.ne.18.030195.003011. View

Mastronarde D . Correlated firing of cat retinal ganglion cells. II. Responses of X- and Y-cells to single quantal events. J Neurophysiol. 1983; 49(2):325-49. DOI: 10.1152/jn.1983.49.2.325. View

Steriade M . Grouping of brain rhythms in corticothalamic systems. Neuroscience. 2005; 137(4):1087-106. DOI: 10.1016/j.neuroscience.2005.10.029. View

10.

Pang J, Paul D, Wu S . Survey on amacrine cells coupling to retrograde-identified ganglion cells in the mouse retina. Invest Ophthalmol Vis Sci. 2013; 54(8):5151-62. PMC: 3732024. DOI: 10.1167/iovs.13-11774. View

11.

Brainard D . The Psychophysics Toolbox. Spat Vis. 1997; 10(4):433-6. View

12.

Sohl G, Maxeiner S, Willecke K . Expression and functions of neuronal gap junctions. Nat Rev Neurosci. 2005; 6(3):191-200. DOI: 10.1038/nrn1627. View

13.

Wright L, Vaney D . The type 1 polyaxonal amacrine cells of the rabbit retina: a tracer-coupling study. Vis Neurosci. 2004; 21(2):145-55. DOI: 10.1017/s0952523804042063. View

14.

Deans M, Volgyi B, Goodenough D, Bloomfield S, Paul D . Connexin36 is essential for transmission of rod-mediated visual signals in the mammalian retina. Neuron. 2002; 36(4):703-12. PMC: 2834592. DOI: 10.1016/s0896-6273(02)01046-2. View

15.

Ainsworth M, Lee S, Cunningham M, Traub R, Kopell N, Whittington M . Rates and rhythms: a synergistic view of frequency and temporal coding in neuronal networks. Neuron. 2012; 75(4):572-83. DOI: 10.1016/j.neuron.2012.08.004. View

16.

Kenyon G, Moore B, Jeffs J, Denning K, Stephens G, Travis B . A model of high-frequency oscillatory potentials in retinal ganglion cells. Vis Neurosci. 2004; 20(5):465-80. PMC: 3348786. DOI: 10.1017/s0952523803205010. View

17.

Trenholm S, McLaughlin A, Schwab D, Turner M, Smith R, Rieke F . Nonlinear dendritic integration of electrical and chemical synaptic inputs drives fine-scale correlations. Nat Neurosci. 2014; 17(12):1759-66. PMC: 4265022. DOI: 10.1038/nn.3851. View

18.

DeVries S . Correlated firing in rabbit retinal ganglion cells. J Neurophysiol. 1999; 81(2):908-20. DOI: 10.1152/jn.1999.81.2.908. View

19.

Volgyi B, Abrams J, Paul D, Bloomfield S . Morphology and tracer coupling pattern of alpha ganglion cells in the mouse retina. J Comp Neurol. 2005; 492(1):66-77. PMC: 2834591. DOI: 10.1002/cne.20700. View

20.

Hu E, Pan F, Volgyi B, Bloomfield S . Light increases the gap junctional coupling of retinal ganglion cells. J Physiol. 2010; 588(Pt 21):4145-63. PMC: 3002447. DOI: 10.1113/jphysiol.2010.193268. View