Electrical Transmission: A Functional Analysis and Comparison to Chemical Transmission

Bennett, Michael V. L.

doi:10.1002/cphy.cp010111

Cited by 123 publications

(136 citation statements)

References 322 publications

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“…Certain aspects of the tracer coupling method are unsatisfactory when compared to simultaneous electrophysiological recording from coupled cell pairs (Connors, 2009; see also Bennett, 1966Bennett, , 1977 for an historical perspective). First, although the presence of tracer or dye coupling in general correlates well with the presence of electrical coupling, the two can be dissociated from each other, at least under certain circumstances (Eckert, 2006;Ek-Vitorin et al, 2006;Ek-Vitorin and Burt, 2012).…”

Section: Evidence From Electrophysiological Recording Of Coupled Cellmentioning

confidence: 99%

“…The recordings demonstrated bidirectional, non-rectifying electrical coupling between these cells, with an average junctional conductance (G j ) of ~700 pS (range from about 300 to about 1500 pS). The coupling displayed low-pass transmission characteristics, typical of electrical synapses (Bennett, 1966(Bennett, , 1977Connors and Long, 2004). The conductance was large enough that action potentials in one AII cell could evoke distinct responses (electrical postsynaptic potentials; electrical PSPs) in coupled cells.…”

Section: Evidence From Electrophysiological Recording Of Coupled Cellmentioning

confidence: 99%

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Electrical synapses between AII amacrine cells in the retina: Function and modulation

Hartveit

Veruki

2012

Brain Research

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Adaptation enables the visual system to operate across a large range of background light intensities. There is evidence that one component of this adaptation is mediated by modulation of gap junctions functioning as electrical synapses, thereby tuning and functionally optimizing specific retinal microcircuits and pathways. The AII amacrine cell is an interneuron found in most mammalian retinas and plays a crucial role for processing visual signals in starlight, twilight and daylight. AII amacrine cells are connected to each other by gap junctions, potentially serving as a substrate for signal averaging and noise reduction, and there is evidence that the strength of electrical coupling is modulated by the level of background light. Whereas there is extensive knowledge concerning the retinal microcircuits that involve the AII amacrine cell, it is less clear which signaling pathways and intracellular transduction mechanisms are involved in modulating the junctional conductance between electrically coupled AII amacrine cells. Here we review the current state of knowledge, with a focus on recent evidence that suggests that the modulatory control involves activity-dependent changes in the phosphorylation of the gap junction channels between AII amacrine cells, potentially linked to their intracellular Ca 2+ dynamics.

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Section: Evidence From Electrophysiological Recording Of Coupled Cellmentioning

confidence: 99%

Section: Evidence From Electrophysiological Recording Of Coupled Cellmentioning

confidence: 99%

Electrical synapses between AII amacrine cells in the retina: Function and modulation

Hartveit

Veruki

2012

Brain Research

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“…For example, it is unknown how much of the total input conductance of a single cell the junctional and nonjunctional conductances account for. This question can be addressed experimentally for a pair of electrically coupled cells, using a two-cell circuit model (Bennett 1966(Bennett , 1977, but in the case of the network of AII amacrine cells, this model ignores the fact that a single cell is connected by electrical synapses to several other AII amacrine cells and ON-cone bipolar cells. There are few agents that block gap junction channels, and several of these have nonspecific effects on other channel types.…”

mentioning

confidence: 99%

Electrical Coupling and Passive Membrane Properties of AII Amacrine Cells

Veruki

Oltedal

Hartveit

2010

Journal of Neurophysiology

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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...

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“…This enhancement of electrical coupling could be due indirectly to a change in the input resistance (R i ) of these neurons and/or to a specific alteration in the junctional resistance of their connecting pathways (Bennett 1977). Although our data do not allow us to distinguish between these two possibilities, the experimental procedure used for coupling measurements under the different training conditions did reveal associated changes in membrane R i (Fig.…”

Section: Contingent-dependent Da Release Increases Electrical Couplinmentioning

confidence: 67%

Implication of dopaminergic modulation in operant reward learning and the induction of compulsive-like feeding behavior inAplysia

et al. 2013

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Feeding in Aplysia provides an amenable model system for analyzing the neuronal substrates of motivated behavior and its adaptability by associative reward learning and neuromodulation. Among such learning processes, appetitive operant conditioning that leads to a compulsive-like expression of feeding actions is known to be associated with changes in the membrane properties and electrical coupling of essential action-initiating B63 neurons in the buccal central pattern generator (CPG). Moreover, the food-reward signal for this learning is conveyed in the esophageal nerve (En), an input nerve rich in dopamine-containing fibers. Here, to investigate whether dopamine (DA) is involved in this learning-induced plasticity, we used an in vitro analog of operant conditioning in which electrical stimulation of En substituted the contingent reinforcement of biting movements in vivo. Our data indicate that contingent En stimulation does, indeed, replicate the operant learning-induced changes in CPG output and the underlying membrane and synaptic properties of B63. Significantly, moreover, this network and cellular plasticity was blocked when the input nerve was stimulated in the presence of the DA receptor antagonist cis-flupenthixol. These results therefore suggest that En-derived dopaminergic modulation of CPG circuitry contributes to the operant reward-dependent emergence of a compulsive-like expression of Aplysia's feeding behavior.

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Electrical Transmission: A Functional Analysis and Comparison to Chemical Transmission

Cited by 123 publications

References 322 publications

Electrical synapses between AII amacrine cells in the retina: Function and modulation

Electrical synapses between AII amacrine cells in the retina: Function and modulation

Electrical Coupling and Passive Membrane Properties of AII Amacrine Cells

Implication of dopaminergic modulation in operant reward learning and the induction of compulsive-like feeding behavior inAplysia

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