title: Dendritic spikes amplify the synaptic signal to enhance detection of motion in a simulation of the direction-selective ganglion cell.
abstract: The On-Off direction-selective ganglion cell (DSGC) in mammalian retinas responds most strongly to a stimulus moving in a specific direction. The DSGC initiates spikes in its dendritic tree, which are thought to propagate to the soma with high probability. Both dendritic and somatic spikes in the DSGC display strong directional tuning, whereas somatic PSPs (postsynaptic potentials) are only weakly directional, indicating that spike generation includes marked enhancement of the directional signal. We used a realistic computational model based on anatomical and physiological measurements to determine the source of the enhancement. Our results indicate that the DSGC dendritic tree is partitioned into separate electrotonic regions, each summing its local excitatory and inhibitory synaptic inputs to initiate spikes. Within each local region the local spike threshold nonlinearly amplifies the preferred response over the null response on the basis of PSP amplitude. Using inhibitory conductances previously measured in DSGCs, the simulation results showed that inhibition is only sufficient to prevent spike initiation and cannot affect spike propagation. Therefore, inhibition will only act locally within the dendritic arbor. We identified the role of three mechanisms that generate directional selectivity (DS) in the local dendritic regions. First, a mechanism for DS intrinsic to the dendritic structure of the DSGC enhances DS on the null side of the cell's dendritic tree and weakens it on the preferred side. Second, spatially offset postsynaptic inhibition generates robust DS in the isolated dendritic tips but weak DS near the soma. Third, presynaptic DS is apparently necessary because it is more robust across the dendritic tree. The pre- and postsynaptic mechanisms together can overcome the local intrinsic DS. These local dendritic mechanisms can perform independent nonlinear computations to make a decision, and there could be analogous mechanisms within cortical circuitry.
authors.affiliation: Department of Neuroscience, University of Pennsylvania, Philadelphia, Pennsylvania, United States of America.
authors.forename: Michael J
authors.initials: MJ
authors.lastname: Schachter
authors.forename: Nicholas
authors.initials: N
authors.lastname: Oesch
authors.forename: Robert G
authors.initials: RG
authors.lastname: Smith
authors.forename: W Rowland
authors.initials: WR
authors.lastname: Taylor
mesh_terms: D000818:Animals; D003198:Computer Simulation; D003712:Dendrites / Q000502:physiology*; D051379:Mice; D008959:Models, Neurological; D009039:Motion Perception / Q000502:physiology*; D062557:NAV1.6 Voltage-Gated Sodium Channel; D009419:Nerve Tissue Proteins / Q000502:physiology; D011817:Rabbits; D012160:Retina / Q000033:anatomy & histology; D012165:Retinal Ganglion Cells / Q000502:physiology*; D015222:Sodium Channels / Q000502:physiology; D055366:Synaptic Potentials / Q000502:physiology*
chemical_list: D062557:NAV1.6 Voltage-Gated Sodium Channel; D009419:Nerve Tissue Proteins; C491046:Scn8a protein, mouse; D015222:Sodium Channels
references.citation: J Neurophysiol. 1993 Jun;69(6):2174-87
references.pmid: 8350137
references.citation: Neuron. 2005 Apr 7;46(1):117-27
references.pmid: 15820698
references.citation: J Neurophysiol. 1997 Oct;78(4):1935-47
references.pmid: 9325362
references.citation: Neuroscience. 1998 Jul;85(1):239-47
references.pmid: 9607715
references.citation: Vis Neurosci. 2003 Mar-Apr;20(2):141-52
references.pmid: 12916736
references.citation: J Comp Neurol. 2002 Jul 22;449(2):195-205
references.pmid: 12115689
references.citation: J Neurosci. 1999 May 15;19(10):3657-64
references.pmid: 10233997
references.citation: Nature. 2002 Aug 22;418(6900):845-52
references.pmid: 12192402
references.citation: Neuron. 2007 Jul 19;55(2):179-86
references.pmid: 17640521
references.citation: Proc Natl Acad Sci U S A. 1983 May;80(9):2799-802
references.pmid: 6573680
references.citation: J Neurophysiol. 1985 May;53(5):1266-86
references.pmid: 3998809
references.citation: Jpn J Physiol. 1991;41(1):35-48
references.pmid: 1713278
references.citation: PLoS Comput Biol. 2009 Sep;5(9):e1000500
references.pmid: 19750211
references.citation: Vis Neurosci. 1994 Sep-Oct;11(5):1019-25
references.pmid: 7947395
references.citation: J Neurophysiol. 2003 May;89(5):2406-19
references.pmid: 12740401
references.citation: Nat Neurosci. 2009 Aug;12(8):996-1002
references.pmid: 19633666
references.citation: J Neurosci. 1988 Jul;8(7):2303-20
references.pmid: 3249227
references.citation: J Neurosci. 2002 Sep 1;22(17):7712-20
references.pmid: 12196594
references.citation: Trends Neurosci. 2003 Jul;26(7):379-85
references.pmid: 12850434
references.citation: Biophys J. 1991 Dec;60(6):1511-33
references.pmid: 1663796
references.citation: J Physiol. 2005 May 1;564(Pt 3):803-15
references.pmid: 15760941
references.citation: Exp Neurol. 1959 Nov;1:491-527
references.pmid: 14435979
references.citation: J Neurosci. 1990 Jun;10(6):1728-44
references.pmid: 2355247
references.citation: J Gen Physiol. 1998 Apr;111(4):565-81
references.pmid: 9524139
references.citation: J Physiol. 1989 Nov;418:379-96
references.pmid: 2559971
references.citation: J Neurochem. 1981 Oct;37(4):867-77
references.pmid: 7320727
references.citation: J Comp Neurol. 2008 May 1;508(1):175-83
references.pmid: 18306383
references.citation: Physiol Rev. 1992 Oct;72(4 Suppl):S159-86
references.pmid: 1438585
references.citation: Vision Res. 1993 Mar-Apr;33(5-6):579-608
references.pmid: 8351833
references.citation: Biophys J. 1974 Oct;14(10):759-90
references.pmid: 4424185
references.citation: J Neurophysiol. 1998 Jan;79(1):151-8
references.pmid: 9425186
references.citation: Neurosci Res. 1991 Sep;11(4):261-75
references.pmid: 1661876
references.citation: Science. 2000 Sep 29;289(5488):2347-50
references.pmid: 11009420
references.citation: Science. 2000 Oct 27;290(5492):739-44
references.pmid: 11052929
references.citation: Neuron. 2009 Mar 26;61(6):906-16
references.pmid: 19323999
references.citation: Bull Math Biol. 1992 Nov;54(6):905-28
references.pmid: 1515871
references.citation: J Neurophysiol. 1967 Sep;30(5):1138-68
references.pmid: 6055351
references.citation: Neuron. 2005 Sep 1;47(5):739-50
references.pmid: 16129402
references.citation: J Physiol. 1964 Oct;173:377-407
references.pmid: 14220259
references.citation: Cold Spring Harb Symp Quant Biol. 1990;55:69-80
references.pmid: 1966772
references.citation: J Physiol. 1965 Jun;178(3):477-504
references.pmid: 5827909
references.citation: J Neurosci. 1998 Oct 1;18(19):7613-24
references.pmid: 9742133
references.citation: J Physiol. 1995 Sep 15;487 ( Pt 3):711-25
references.pmid: 8544133
references.citation: Brain Res. 2009 Nov 3;1296:225-33
references.pmid: 19596283
references.citation: J Neurophysiol. 1995 Feb;73(2):703-12
references.pmid: 7760129
references.citation: J Neurophysiol. 1999 Mar;81(3):1412-7
references.pmid: 10085366
references.citation: J Neurophysiol. 1997 Nov;78(5):2772-89
references.pmid: 9356425
references.citation: Vis Neurosci. 2004 Jul-Aug;21(4):611-25
references.pmid: 15579224
references.citation: J Physiol. 1993 Dec;472:615-63
references.pmid: 7908327
references.citation: J Neurophysiol. 1975 May;38(3):613-26
references.pmid: 1127460
references.citation: J Neurosci. 2003 Mar 15;23(6):2306-13
references.pmid: 12657689
references.citation: Biophys J. 2001 Feb;80(2):729-37
references.pmid: 11159440
references.citation: Nat Neurosci. 2001 Feb;4(2):176-83
references.pmid: 11175879
references.citation: J Neurophysiol. 1999 Apr;81(4):1685-98
references.pmid: 10200204
references.citation: Philos Trans R Soc Lond B Biol Sci. 1982 Jul 27;298(1090):227-63
references.pmid: 6127730
references.citation: J Neurosci. 2006 Jul 5;26(27):7172-80
references.pmid: 16822974
references.citation: J Neurosci. 1994 Sep;14(9):5267-80
references.pmid: 8083735
references.citation: Nat Neurosci. 2004 Sep;7(9):961-7
references.pmid: 15322550
references.citation: J Neurophysiol. 2002 Aug;88(2):1026-39
references.pmid: 12163551
references.citation: J Neurophysiol. 2001 Feb;85(2):926-37
references.pmid: 11160523
references.citation: J Neurophysiol. 2010 Mar;103(3):1357-74
references.pmid: 20053849
references.citation: J Neurophysiol. 1997 Oct;78(4):1948-64
references.pmid: 9325363
references.citation: J Neurosci. 1999 Sep 15;19(18):8049-56
references.pmid: 10479705
references.citation: J Neurosci. 1994 Nov;14(11 Pt 1):6301-16
references.pmid: 7965037
references.citation: J Neurosci Methods. 1992 Jul;43(2-3):83-108
references.pmid: 1405746
references.citation: J Comp Neurol. 2007 Jan 10;500(2):339-52
references.pmid: 17111377