Electrical Coupling and Passive Membrane Properties of AII Amacrine Cells

Abstract

Veruki ML, Oltedal L, Hartveit E. Electrical coupling and passive membrane properties of AII amacrine cells. J Neurophysiol 103: 1456-1466, 2010. First published January 20, 2010 doi:10.1152/jn.01105.2009. AII amacrine cells in the mammalian retina are connected via electrical synapses to ON-cone bipolar cells and to other AII amacrine cells. To understand synaptic integration in these interneurons, we need information about the junctional conductance (g j ), the membrane resistance (r m ), the membrane capacitance (C m ), and the cytoplasmic resistivity (R i ). Due to the extensive electrical coupling, it is difficult to obtain estimates of r m , as well as the relative contribution of the junctional and nonjunctional conductances to the total input resistance of an AII amacrine cell. Here we used dual voltage-clamp recording of pairs of electrically coupled AII amacrine cells in an in vitro slice preparation from rat retina and applied meclofenamic acid (MFA) to block the electrical coupling and isolate single AII amacrines electrically. In the control condition, the input resistance (R in ) was ϳ620 M⍀ and the apparent r m was ϳ760 M⍀. After block of electrical coupling, determined by estimating g j in the dual recordings, R in and r m were ϳ4,400 M⍀, suggesting that the nongap junctional conductance of an AII amacrine cell is ϳ16% of the total input conductance. Control experiments with nucleated patches from AII amacrine cells suggested that MFA had no effect on the nongap junctional membrane of these cells. From morphological reconstructions of AII amacrine cells filled with biocytin, we obtained a surface area of ϳ900 m 2 which, with a standard value for C m of 0.01 pF/m 2 , corresponds to an average capacitance of ϳ9 pF and a specific membrane resistance of ϳ41 k⍀ cm 2 . Together with information concerning synaptic connectivity, these data will be important for developing realistic compartmental models of the network of AII amacrine cells. Strettoi et al. 1992Strettoi et al. , 1994Veruki et al. 2003). They are presynaptic to and transmit their signals to OFF-cone bipolar cells via glycinergic, inhibitory synapses (Pourcho and Goebel 1985;Sassoè-Pognetto et al. 1994;Strettoi et al. 1992Strettoi et al. , 1994. In addition, AII amacrine cells are connected via gap junctions to ON-cone bipolar cells (heterologous connections) and to other AII amacrine cells (homologous connections) (Chun et al. 1993;Kolb 1979;Kolb and Famiglietti 1974;McGuire et al. 1984;Strettoi et al. 1992Strettoi et al. , 1994. Functionally, both types of gap junctions correspond to electrical synapses (Trexler et al. 2005; Veruki and Hartveit 2002a,b).While the electrical synapses between AII amacrine cells and ON-cone bipolar cells are considered to play a role in the direct transmission of scotopic visual signals, the electrical synapses between AII amacrine cells are thought to be important for removing noise from the visual signal (Smith and Vardi 1995;Vardi and Smith 1996). The magnitude of the junctional conductance (g j ) betwe...

NMDA Receptor Activation Strengthens Weak Electrical Coupling in Mammalian Brain

“…G j between IO neurons is only 50–200 pS (Figure S4) which is remarkably weak compared to the G j in other systems, such as retina AII amacrine cells (400 pS; Veruki et al, 2010), mesencephalic trigeminal neurons (4.8 nS; Curti et al, 2012), and crayfish septate axons (10 µS; Campos de Carvalho et al, 1984). A tonic NMDAR current mediating Ca 2+ influx at DVs and GJs may increase G j between weaklycoupled neurons to a level sufficient to permit continuous STOs to emerge within an ensemble.…”

AII amacrine cells: quantitative reconstruction and morphometric analysis of electrophysiologically identified cells in live rat retinal slices imaged with multi-photon excitation microscopy

“…The range of input resistances can most likely be explained by differences in the extent and conductance of gap junction coupling (cf. Veruki et al 2010). …”

“…These tracers cannot be visualized during recording, but must be visualized following the binding to streptavidin (or avidin) which can be linked to either a fluorescent dye (for visualization by fluorescence microscopy) or HRP (for visualization after developing an insoluble reaction product). In a previous study from our laboratory (Veruki et al 2010), we filled AII amacrines in rat retinal slices with biocytin from patch pipettes and reconstructed the morphology after histochemical detection. Because AII amacrines are connected to other AIIs and ON-cone bipolar cells via gap junctions (Kolb and Famiglietti 1974; Famiglietti and Kolb 1975; Kolb 1979; Strettoi et al 1992; Chun et al 1993) and because biocytin and Neurobiotin can diffuse into neighboring cells through gap junctions (Vaney 1991), we limited the recording time to 5–10 min.…”

Light adaptation alters inner retinal inhibition to shape OFF retinal pathway signaling

“…One way this could be achieved is through electrical gap junction coupling between amacrine cells that could increase their excitatory spread. AII amacrine cells, which give input to most OFF bipolar cells (OFF1,2,4) (Mazade and Eggers 2013;Tsukamoto et al 2001) are highly coupled in the very dim light conditions shown from labeling studies Bloomfield 1999a, 1997), which mediated signal spread through the network (Veruki et al 2010). This glycinergic signal spread has been shown to extend far beyond the dimensions of the dendritic arbor further suggesting the use of gap junctions in narrow-field amacrine cell networks (Chen et al 2011).…”