Electrical and Calcium Signaling in Dendrites of Hippocampal Pyramidal Neurons

Magee, Jeffrey C.; Hoffman, Dax A.; Colbert, Costa M.; Johnston, Daniel

doi:10.1146/annurev.physiol.60.1.327

Cited by 269 publications

(170 citation statements)

References 76 publications

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“…However, chemical PSPs can be altered in shape and size by voltage-activated currents when the postsynaptic membrane potential is near or above spike threshold (Magee et al 1998;Stuart and Sakmann 1995). We observed distinctly nonlinear effects of electrical synaptic transmission under similar conditions.…”

Section: Nonlinear Effects Of Postsynaptic Membrane Potential On Epspsmentioning

confidence: 66%

Functional Properties of Electrical Synapses Between Inhibitory Interneurons of Neocortical Layer 4

Gibson¹,

Beierlein²,

Connors³

2005

Journal of Neurophysiology

216

168

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Gibson, Jay R., Michael Beierlein, and Barry W. Connors. Functional properties of electrical synapses between inhibitory interneurons of neocortical layer 4. J Neurophysiol 93: [467][468][469][470][471][472][473][474][475][476][477][478][479][480] 2005. First published August 18, 2004; doi:10.1152/jn.00520.2004. The existence of electrical synapses between GABAergic inhibitory interneurons in neocortex is well established, but their functional properties have not been described in detail. We made whole cell recordings from pairs of electrically coupled fast-spiking (FS) or low thresholdspiking (LTS) neurons, and filled some cells with biocytin for morphological reconstruction. Data were used to create compartmental cable models and to guide mathematical analysis. We analyzed the time course and amplitude of electrical postsynaptic potentials (ePSPs), the subthreshold events generated by presynaptic action potentials, in both FS and LTS neurons. The results imply that the generation of ePSPs is predominantly a linear process in both cell types for presynaptic firing of both single and repetitive spikes. Nonlinearities shape ePSPs near spike threshold, but our data suggest that the underlying synaptic current is still a linear process. Cell-tocell electrical signaling on longer timescales also appears to be linear. Cable models of electrically coupled FS and LTS neurons imply that the analyzed electrical synapses are, on average, within 50 m of the soma. Finally, we show that electrical coupling between 2 inhibitory cells promotes synchrony at all spiking frequencies. This contrasts with the effect of reciprocal inhibitory postsynaptic potentials (IPSPs) evoked by the same cells, which promote antisynchronous firing at frequencies less than about 100 Hz. Electrical coupling counteracts the antisynchronous behavior induced by IPSPs and facilitates spiking synchrony. Our results suggest that electrical synapses among inhibitory interneurons are most readily described as low-pass linear filters that promote firing synchrony. I N T R O D U C T I O NThere is strong anatomical and electrophysiological evidence for electrical synapses between GABAergic inhibitory interneurons in neocortex (Bozhilova Pastirova and Ovtscharoff 1995;Galarreta and Hestrin 1999;Gibson et al. 1999;Sloper and Powell 1978;Tamas et al. 2000). Electrical synapses mediate direct electrical communication between neurons. They are composed of clusters of ion channels that span the plasma membranes of 2 neurons, thereby directly connecting their cytoplasmic compartments. Each of these channel clusters is called a gap junction (Bennett 1977). Gap junctions between inhibitory neurons in neocortex tend to be dendrodendritic or dendrosomatic (Fukuda and Kosaka 2003;Szabadics et al. 2001;Tamas et al. 2000), and their channels require connexin36 (Cx36) subunits (Deans et al. 2001;Hormuzdi et al. 2001). Electrical synapses in neocortex mostly occur between cells whose somata are within 75 m of each other, they interconnect about 20 to 60 neighboring inhibito...

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Section: Nonlinear Effects Of Postsynaptic Membrane Potential On Epspsmentioning

confidence: 66%

Functional Properties of Electrical Synapses Between Inhibitory Interneurons of Neocortical Layer 4

Gibson¹,

Beierlein²,

Connors³

2005

Journal of Neurophysiology

216

168

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“…Third, the tonic excitatory inputs are likely to be more prominent in vivo than in an isolated in vitro slice that is constantly being perfused with ACSF. Fourth, there are populations of voltage-gated calcium channels activated at low voltages (Ϫ70 to Ϫ50 mV) comparable to those that elicit BDNF release that contribute to tonic intracellular calcium concentration (Magee et al, 1998). Fifth, GABA excitation itself can activate voltage-gated calcium channels (Ben-Ari, 2002) that could be the actual physiological stimulus that elicits BDNF release.…”

Section: Discussionmentioning

confidence: 99%

Single-Cell Characterization of Retrograde Signaling by Brain-Derived Neurotrophic Factor

Magby¹,

Bi²,

Chen³

et al. 2006

J. Neurosci.

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Brain-derived neurotrophic factor (BDNF) is a key regulator of hippocampal synaptic plasticity in the developing and adult nervous system. It can be released from pyramidal neuron dendrites in an activity-dependent manner and has therefore been suggested to serve as a signal that provides the retrograde intercellular communication necessary for Hebbian plasticity and hippocampal-dependent learning. Although much has been learned about BDNF function by field stimulation of hippocampal neurons, it is not known whether moderate action potential-independent depolarization of single cells is capable of releasing sufficient BDNF to influence transmission at individual synapses. In this study, we show directly at the single-cell level that such modulation can occur. By using K-252a, anti-BDNF antibody, and interruption of regulated release, we confirm a model in which postsynaptic depolarization elicits calcium-dependent release of BDNF that diffuses retrogradely and enhances presynaptic transmitter release.

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“…It should be noted, however, that our simulation methods do not discriminate between pre-and postsynaptic mechanisms of this potentiation. Another important issue is that active conductances on the dendrites may contribute to the nonlinear summation of unitary EPSPs (reviewed by Magee et al, 1998;Reyes, 2001) and complicate interpretation of EPSPs recorded at the soma. Dendritic active conductances have not been included in the current model due to a lack of knowledge of their distribution and properties in DG granule cells.…”

mentioning

confidence: 99%

Contribution of NMDA receptor channels to the expression of LTP in the hippocampal dentate gyrus

2002

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ABSTRACT:The role of glutamatergic NMDA receptor channels (NMDARs) in the induction of long-term potentiation (LTP) has been well established. In contrast, whether or not NMDARs contribute to the expression of LTP has been an issue of debate. In this study, we investigated the contribution of NMDARs to LTP expression in the hippocampal dentate gyrus (DG) by stimulating perforant path afferents with short bursts of pulses delivered at a moderate frequency (40 Hz), instead of using the traditional protocol of a single stimulus at a low frequency (<0.1 Hz).

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Electrical and Calcium Signaling in Dendrites of Hippocampal Pyramidal Neurons

Cited by 269 publications

References 76 publications

Functional Properties of Electrical Synapses Between Inhibitory Interneurons of Neocortical Layer 4

Functional Properties of Electrical Synapses Between Inhibitory Interneurons of Neocortical Layer 4

Single-Cell Characterization of Retrograde Signaling by Brain-Derived Neurotrophic Factor

Contribution of NMDA receptor channels to the expression of LTP in the hippocampal dentate gyrus

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