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Voltage-gated potassium channels control extended access cocaine seeking: a role for nucleus accumbens astrocytes

Neuropsychopharmacology volume 49, pages 551–560 (2024)Cite this article

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Abstract

Dopaminergic signaling in the nucleus accumbens shell (NAc) regulates neuronal activity relevant to reward-related learning, including cocaine-associated behaviors. Although astrocytes respond to dopamine and cocaine with structural changes, the impact of dopamine and cocaine on astrocyte functional plasticity has not been widely studied. Specifically, behavioral implications of voltage-gated channel activity in the canonically non-excitable astrocytes are not known. We characterized potassium channel function in NAc astrocytes following exposure to exogenous dopamine or cocaine self-administration training under short (2 h/day) and extended (6 h/day) access schedules. Electrophysiological, Ca2+ imaging, mRNA, and mass spectrometry tools were used for molecular characterization. Behavioral effects were examined after NAc-targeted microinjections of channel antagonists and astroglial toxins. Exogenous dopamine increased activity of currents mediated by voltage-gated (Kv7) channels in NAc astrocytes. This was associated with a ~5-fold increase in expression of Kcnq2 transcript level in homogenized NAc micropunches. Matrix-assisted laser desorption/ionization mass spectrometry revealed increased NAc dopamine levels in extended access, relative to short access, rats. Kv7 inhibition selectively increased frequency and amplitude of astrocyte intracellular Ca2+ transients in NAc of extended access rats. Inhibition of Kv7 channels in the NAc attenuated cocaine-seeking in extended access rats only, an effect that was occluded by microinjection of the astrocyte metabolic poison, fluorocitrate. These results suggest that voltage-gated K+ channel signaling in NAc astrocytes is behaviorally relevant, support Kv7-mediated regulation of astrocyte Ca2+ signals, and propose novel mechanisms of neuroglial interactions relevant to drug use.

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Fig. 1: Dopamine decreases astrocyte sensitivity to 4-AP.
Fig. 2: Dopamine upregulates Kcnq transcript levels and astrocyte Kv7 activity.
Fig. 3: NAc dopamine metabolism differences after short and extended access cocaine.
Fig. 4: Kv7 regulates astrocyte Ca2+ after short- and extended-access cocaine.
Fig. 5: NAc astrocytes are required for XE 991-mediated attenuation of cocaine seeking after extended access to cocaine.

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Funding

The authors would like to acknowledge the following sources of grant support: R01DA041513 (PIO), R01DA053070 (PIO, JRT), R01DA044311 (JRT), T32 DA035200 (TAA), R01AG066653, R01CA266004, R01AG078702 (RCS).

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Authors and Affiliations

  1. Department of Neuroscience, University of Kentucky, Lexington, KY, USA

    Mengfan Xia, Tanner L. Anderson & Pavel I. Ortinski

  2. Department of Pharmacology and Nutritional Sciences, University of Kentucky, Lexington, KY, USA

    Mengfan Xia

  3. Department of Pharmaceutical Sciences, University of Kentucky, Lexington, KY, USA

    Emily R. Prantzalos & Jill R. Turner

  4. Department of Biochemistry and Molecular Biology, University of Florida, Gainesville, FL, USA

    Tara R. Hawkinson, Harrison A. Clarke, Shannon B. Keohane & Ramon C. Sun

  5. Center for Advanced Spatial Biomolecule Research, University of Florida, Gainesville, FL, USA

    Ramon C. Sun

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Contributions

MX, PIO – conception and design of the work. MX, ERP, TRH, HAC, and SBK – data acquisition and analysis. MX, TLA, and PIO – data interpretation, manuscript drafting, and manuscript revisions. PIO, JRT, and RCS – data interpretation, manuscript revisions, and final approval.

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Correspondence to Pavel I. Ortinski.

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Xia, M., Anderson, T.L., Prantzalos, E.R. et al. Voltage-gated potassium channels control extended access cocaine seeking: a role for nucleus accumbens astrocytes. Neuropsychopharmacol. 49, 551–560 (2024). https://doi.org/10.1038/s41386-023-01718-w

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