title: Dynamic tuning of electrical and chemical synaptic transmission in a network of motion coding retinal neurons.
abstract: Recently, we demonstrated that gap junction coupling in the population of superior coding ON-OFF directionally selective ganglion cells (DSGCs) genetically labeled in the Hb9::eGFP mouse retina allows the passage of lateral anticipatory signals that help track moving stimuli. Here, we examine the properties of gap junctions in the DSGC network, and address how interactions between electrical and chemical synapses and intrinsic membrane properties contribute to the dynamic tuning of lateral anticipatory signals. When DSGC subtypes coding all four cardinal directions were individually loaded with the gap junction-permeable tracer Neurobiotin, only superior coding DSGCs exhibited homologous coupling. Consistent with these anatomical findings, gap junction-dependent feedback spikelets were only observed in Hb9(+) DSGCs. Recordings from pairs of neighboring Hb9(+) DSGCs revealed that coupling was reciprocal, non-inactivating, and relatively weak, and provided a substrate for an extensive subthreshold excitatory receptive field around each cell. This subthreshold activity appeared to boost coincident light-driven chemical synaptic responses. However, during responses to moving stimuli, gap junction-mediated boosting appeared to be dynamically modulated such that upstream DSGCs primed downstream cells, but not vice versa, giving rise to highly skewed responses in individual cells. We show that the asymmetry in priming arises from a combination of spatially offset GABAergic inhibition and activity-dependent changes in intrinsic membrane properties of DSGCs. Thus, dynamic interactions between electrical and chemical synapses and intrinsic membrane properties allow the network of DSGCs to propagate anticipatory responses most effectively along their preferred direction without leading to runaway excitation.
authors.affiliation: Biology Department, University of Victoria, Victoria, British Columbia V8W 3N5, Canada, and Department of Physics, Princeton University, Princeton, New Jersey 08544.
authors.forename: Stuart
authors.initials: S
authors.lastname: Trenholm
authors.forename: Amanda J
authors.initials: AJ
authors.lastname: McLaughlin
authors.forename: David J
authors.initials: DJ
authors.lastname: Schwab
authors.forename: Gautam B
authors.initials: GB
authors.lastname: Awatramani
mesh_terms: D000200:Action Potentials / Q000502:physiology; D000818:Animals; D001703:Biophysics; D001710:Biotin / Q000031:analogs & derivatives / Q000378:metabolism; D004558:Electric Stimulation; D005260:Female; D017629:Gap Junctions / Q000502:physiology; D049452:Green Fluorescent Proteins / Q000235:genetics; D018398:Homeodomain Proteins / Q000235:genetics / Q000378:metabolism; D066298:In Vitro Techniques; D008297:Male; D051379:Mice; D008822:Mice, Transgenic; D009038:Motion; D009433:Neural Inhibition; D009474:Neurons / Q000502:physiology*; D017711:Nonlinear Dynamics; D010775:Photic Stimulation; D012160:Retina / Q000166:cytology*; D013569:Synapses / Q000145:classification / Q000502:physiology*; D014157:Transcription Factors / Q000235:genetics / Q000378:metabolism; D014795:Visual Pathways / Q000166:cytology / Q000502:physiology*
chemical_list: D018398:Homeodomain Proteins; D014157:Transcription Factors; C485184:enhanced green fluorescent protein; C070614:neurobiotin; C084059:Hb9 protein, mouse; D049452:Green Fluorescent Proteins; D001710:Biotin
references.citation: Nature. 1999 Mar 25;398(6725):334-8
references.pmid: 10192333
references.citation: Science. 2011 Oct 21;334(6054):389-93
references.pmid: 22021860
references.citation: J Physiol. 1970 Aug;209(3):647-67
references.pmid: 5499801
references.citation: J Physiol. 1959 Mar 3;145(2):289-325
references.pmid: 13642302
references.citation: J Theor Biol. 2006 Jun 7;240(3):501-10
references.pmid: 16318857
references.citation: J Neurosci. 2008 Sep 24;28(39):9769-89
references.pmid: 18815262
references.citation: Neuron. 2005 Sep 1;47(5):739-50
references.pmid: 16129402
references.citation: Circ Res. 1994 Sep;75(3):483-90
references.pmid: 7520372
references.citation: J Comp Neurol. 2005 Sep 12;490(1):29-39
references.pmid: 16041717
references.citation: Curr Opin Neurobiol. 2002 Aug;12(4):405-10
references.pmid: 12139988
references.citation: Nat Rev Neurosci. 2012 Feb 08;13(3):194-208
references.pmid: 22314444
references.citation: J Theor Biol. 2001 May 21;210(2):187-99
references.pmid: 11371174
references.citation: Neuron. 2010 Dec 22;68(6):1159-72
references.pmid: 21172616
references.citation: Biochim Biophys Acta. 2013 Jan;1828(1):134-46
references.pmid: 22659675
references.citation: J Comp Neurol. 2010 Mar 15;518(6):911-27
references.pmid: 20058323
references.citation: J Physiol. 2010 Nov 1;588(Pt 21):4145-63
references.pmid: 20819943
references.citation: J Physiol. 1953 Jan;119(1):69-88
references.pmid: 13035718
references.citation: J Neurosci. 2012 Mar 28;32(13):4341-59
references.pmid: 22457486
references.citation: Neuron. 2011 Sep 22;71(6):974-94
references.pmid: 21943597
references.citation: J Physiol. 1978 Mar;276:277-98
references.pmid: 650450
references.citation: J Neurophysiol. 1974 May;37(3):560-71
references.pmid: 4827022
references.citation: Annu Rev Neurosci. 2004;27:393-418
references.pmid: 15217338
references.citation: Science. 1967 Feb 17;155(3764):841-2
references.pmid: 6019094
references.citation: Vis Neurosci. 2010 Jul;27(3-4):91-101
references.pmid: 20537217
references.citation: J Neurosci. 2004 Nov 17;24(46):10553-67
references.pmid: 15548670
references.citation: J Neurophysiol. 1998 Jan;79(1):151-8
references.pmid: 9425186
references.citation: J Comp Physiol A. 1993;172(6):715-32
references.pmid: 8350285
references.citation: Biophys J. 1997 Aug;73(2):757-69
references.pmid: 9251792
references.citation: Science. 1995 Aug 18;269(5226):981-5
references.pmid: 7638624
references.citation: J Comp Neurol. 2009 Feb 10;512(5):664-87
references.pmid: 19051243
references.citation: Neuron. 2011 Aug 25;71(4):683-94
references.pmid: 21867884
references.citation: J Neurosci. 2008 Feb 20;28(8):1804-15
references.pmid: 18287497
references.citation: Nature. 2002 Nov 28;420(6914):411-4
references.pmid: 12459782
references.citation: Nature. 2008 Aug 21;454(7207):995-9
references.pmid: 18650810
references.citation: J Neurophysiol. 1983 Feb;49(2):350-65
references.pmid: 6300342
references.citation: Nature. 2004 Mar 25;428(6981):423-6
references.pmid: 15042090
references.citation: J Neurosci. 2003 Jul 30;23(17):6768-77
references.pmid: 12890770
references.citation: Science. 1999 Jan 29;283(5402):695-9
references.pmid: 9924031
references.citation: Science. 2008 Feb 22;319(5866):1108-11
references.pmid: 18292344
references.citation: Science. 2012 Mar 30;335(6076):1624-8
references.pmid: 22403180
references.citation: J Neurosci. 2003 Feb 15;23(4):1506-16
references.pmid: 12598639
references.citation: J Neurosci. 1994 Sep;14(9):5267-80
references.pmid: 8083735
references.citation: Vision Res. 1965 Dec;5(11):583-601
references.pmid: 5862581
references.citation: Spat Vis. 1997;10(4):433-6
references.pmid: 9176952
references.citation: Am J Physiol. 1995 Feb;268(2 Pt 1):C356-65
references.pmid: 7532358
references.citation: J Physiol. 2012 May 15;590(10):2501-17
references.pmid: 22393249
references.citation: J Neurosci. 2012 May 16;32(20):6747-59
references.pmid: 22593045
references.citation: J Neurosci. 1998 Nov 15;18(22):9517-28
references.pmid: 9801388
references.citation: J Neurosci. 2011 May 25;31(21):7753-62
references.pmid: 21613488
references.citation: J Neurosci. 1994 Nov;14(11 Pt 1):6301-16
references.pmid: 7965037
references.citation: J Neurophysiol. 1953 Jan;16(1):37-68
references.pmid: 13035466
references.citation: Nature. 2011 Jan 20;469(7330):402-6
references.pmid: 21131947
references.citation: J Physiol. 2005 Feb 1;562(Pt 3):915-23
references.pmid: 15564281
references.citation: J Neurosci. 2003 Dec 3;23(35):11167-77
references.pmid: 14657176
references.citation: Nature. 2011 Jan 20;469(7330):407-10
references.pmid: 21170022
references.citation: Neuron. 2004 Feb 19;41(4):495-511
references.pmid: 14980200
references.citation: J Neurosci. 1999 May 1;19(9):3298-306
references.pmid: 10212289
references.citation: J Neurosci. 1994 May;14(5 Pt 1):2545-68
references.pmid: 8182427
references.citation: J Physiol. 1969 Aug;203(3):591-609
references.pmid: 4319015
references.citation: Nat Neurosci. 2013 Feb;16(2):154-6
references.pmid: 23313908