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Differential modulation of excitatory and inhibitory striatal synaptic transmission by histamine.
J Neurosci 2011; 31(43):15340-51JN

Abstract

Information processing in the striatum is critical for basal ganglia function and strongly influenced by neuromodulators (e.g., dopamine). The striatum also receives modulatory afferents from the histaminergic neurons in the hypothalamus which exhibit a distinct diurnal rhythm with high activity during wakefulness, and little or no activity during sleep. In view of the fact that the striatum also expresses a high density of histamine receptors, we hypothesized that released histamine will affect striatal function. We studied the role of histamine on striatal microcircuit function by performing whole-cell patch-clamp recordings of neurochemically identified striatal neurons combined with electrical and optogenetic stimulation of striatal afferents in mouse brain slices. Bath applied histamine had many effects on striatal microcircuits. Histamine, acting at H(2) receptors, depolarized both the direct and indirect pathway medium spiny projection neurons (MSNs). Excitatory, glutamatergic input to both classes of MSNs from both the cortex and thalamus was negatively modulated by histamine acting at presynaptic H(3) receptors. The dynamics of thalamostriatal, but not corticostriatal, synapses were modulated by histamine leading to a facilitation of thalamic input. Furthermore, local inhibitory input to both classes of MSNs was negatively modulated by histamine. Subsequent dual whole-cell patch-clamp recordings of connected pairs of striatal neurons revealed that only lateral inhibition between MSNs is negatively modulated, whereas feedforward inhibition from fast-spiking GABAergic interneurons onto MSNs is unaffected by histamine. These findings suggest that the diurnal rhythm of histamine release entrains striatal function which, during wakefulness, is dominated by feedforward inhibition and a suppression of excitatory drive.

Authors+Show Affiliations

MRC Anatomical Neuropharmacology Unit, Department of Pharmacology, University of Oxford, OX1 3TH, Oxford, United Kingdom. tommas.ellender@pharm.ox.ac.ukNo affiliation info availableNo affiliation info availableNo affiliation info availableNo affiliation info available

Pub Type(s)

Journal Article
Research Support, Non-U.S. Gov't

Language

eng

PubMed ID

22031880

Citation

Ellender, Tommas J., et al. "Differential Modulation of Excitatory and Inhibitory Striatal Synaptic Transmission By Histamine." The Journal of Neuroscience : the Official Journal of the Society for Neuroscience, vol. 31, no. 43, 2011, pp. 15340-51.
Ellender TJ, Huerta-Ocampo I, Deisseroth K, et al. Differential modulation of excitatory and inhibitory striatal synaptic transmission by histamine. J Neurosci. 2011;31(43):15340-51.
Ellender, T. J., Huerta-Ocampo, I., Deisseroth, K., Capogna, M., & Bolam, J. P. (2011). Differential modulation of excitatory and inhibitory striatal synaptic transmission by histamine. The Journal of Neuroscience : the Official Journal of the Society for Neuroscience, 31(43), pp. 15340-51. doi:10.1523/JNEUROSCI.3144-11.2011.
Ellender TJ, et al. Differential Modulation of Excitatory and Inhibitory Striatal Synaptic Transmission By Histamine. J Neurosci. 2011 Oct 26;31(43):15340-51. PubMed PMID: 22031880.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Differential modulation of excitatory and inhibitory striatal synaptic transmission by histamine. AU - Ellender,Tommas J, AU - Huerta-Ocampo,Icnelia, AU - Deisseroth,Karl, AU - Capogna,Marco, AU - Bolam,J Paul, PY - 2011/10/28/entrez PY - 2011/10/28/pubmed PY - 2011/12/20/medline SP - 15340 EP - 51 JF - The Journal of neuroscience : the official journal of the Society for Neuroscience JO - J. Neurosci. VL - 31 IS - 43 N2 - Information processing in the striatum is critical for basal ganglia function and strongly influenced by neuromodulators (e.g., dopamine). The striatum also receives modulatory afferents from the histaminergic neurons in the hypothalamus which exhibit a distinct diurnal rhythm with high activity during wakefulness, and little or no activity during sleep. In view of the fact that the striatum also expresses a high density of histamine receptors, we hypothesized that released histamine will affect striatal function. We studied the role of histamine on striatal microcircuit function by performing whole-cell patch-clamp recordings of neurochemically identified striatal neurons combined with electrical and optogenetic stimulation of striatal afferents in mouse brain slices. Bath applied histamine had many effects on striatal microcircuits. Histamine, acting at H(2) receptors, depolarized both the direct and indirect pathway medium spiny projection neurons (MSNs). Excitatory, glutamatergic input to both classes of MSNs from both the cortex and thalamus was negatively modulated by histamine acting at presynaptic H(3) receptors. The dynamics of thalamostriatal, but not corticostriatal, synapses were modulated by histamine leading to a facilitation of thalamic input. Furthermore, local inhibitory input to both classes of MSNs was negatively modulated by histamine. Subsequent dual whole-cell patch-clamp recordings of connected pairs of striatal neurons revealed that only lateral inhibition between MSNs is negatively modulated, whereas feedforward inhibition from fast-spiking GABAergic interneurons onto MSNs is unaffected by histamine. These findings suggest that the diurnal rhythm of histamine release entrains striatal function which, during wakefulness, is dominated by feedforward inhibition and a suppression of excitatory drive. SN - 1529-2401 UR - https://www.unboundmedicine.com/medline/citation/22031880/Differential_modulation_of_excitatory_and_inhibitory_striatal_synaptic_transmission_by_histamine_ L2 - http://www.jneurosci.org/cgi/pmidlookup?view=long&pmid=22031880 DB - PRIME DP - Unbound Medicine ER -