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J Neurophysiol. 2016 Oct 1;116(4):1752-1764. doi: 10.1152/jn.00511.2016. Epub 2016 Jul 20.

The ionic mechanism of membrane potential oscillations and membrane resonance in striatal LTS interneurons.

Author information

1
Department of Biology, The University of Texas at San Antonio, San Antonio, Texas; and.
2
Department of Biology, The University of Texas at San Antonio, San Antonio, Texas; and Department of Physiology, Michigan State University, East Lansing, Michigan.
3
Department of Biology, The University of Texas at San Antonio, San Antonio, Texas; and charles.wilson@utsa.edu.

Abstract

Striatal low-threshold spiking (LTS) interneurons spontaneously transition to a depolarized, oscillating state similar to that seen after sodium channels are blocked. In the depolarized state, whether spontaneous or induced by sodium channel blockade, the neurons express a 3- to 7-Hz oscillation and membrane impedance resonance in the same frequency range. The membrane potential oscillation and membrane resonance are expressed in the same voltage range (greater than -40 mV). We identified and recorded from LTS interneurons in striatal slices from a mouse that expressed green fluorescent protein under the control of the neuropeptide Y promoter. The membrane potential oscillation depended on voltage-gated calcium channels. Antagonism of L-type calcium currents (CaV1) reduced the amplitude of the oscillation, whereas blockade of N-type calcium currents (CaV2.2) reduced the frequency. Both calcium sources activate a calcium-activated chloride current (CaCC), the blockade of which abolished the oscillation. The blocking of any of these three channels abolished the membrane resonance. Immunohistochemical staining indicated anoctamin 2 (ANO2), and not ANO1, as the CaCC source. Biophysical modeling showed that CaV1, CaV2.2, and ANO2 are sufficient to generate a membrane potential oscillation and membrane resonance, similar to that in LTS interneurons. LTS interneurons exhibit a membrane potential oscillation and membrane resonance that are both generated by CaV1 and CaV2.2 activating ANO2. They can spontaneously enter a state in which the membrane potential oscillation dominates the physiological properties of the neuron.

KEYWORDS:

LTS interneuron; calcium-activated chloride current; oscillation; resonance; striatum

PMID:
27440246
PMCID:
PMC5144687
DOI:
10.1152/jn.00511.2016
[Indexed for MEDLINE]
Free PMC Article

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