Cocaine Exposure Modulates Perineuronal Nets and Synaptic Excitability of Fast-Spiking Interneurons in the Medial Prefrontal Cortex

Megan L. Slaker, Emily T. Jorgensen, Deborah M. Hegarty, Xinyue Liu, Yan Kong, Fuming Zhang, Robert J. Linhardt, Travis E. Brown, Sue Aicher, Barbara A. Sorg

Research output: Contribution to journalArticle

2 Citations (Scopus)

Abstract

We previously reported that perineuronal nets (PNNs) are required for cocaine-associated memories. Perineuronal nets are extracellular matrix that primarily surrounds parvalbumin (PV)-containing, GABAergic fast-spiking interneurons (FSIs) in the medial prefrontal cortex (mPFC). Here we measured the impact of acute (1 d) or repeated (5 d) cocaine exposure on PNNs and PV cells within the prelimbic and infralimbic regions of the mPFC. Adult rats were exposed to 1 or 5 d of cocaine and stained for PNNs (using Wisteria floribunda agglutinin) and PV intensity 2 or 24 h later. In the prelimbic and infralimbic PFC, PNN staining intensity decreased 2 h after 1 d of cocaine exposure but increased after 5 d of cocaine exposure. Cocaine also produced changes in PV intensity, which generally lagged behind that of PNNs. In the prelimbic PFC, both 1 and 5 d of cocaine exposure increased GAD65/67 puncta near PNN-surrounded PV cells, with an increase in the GAD65/67-to-VGluT1 puncta ratio after 5 d of cocaine exposure. In the prelimbic PFC, slice electrophysiology studies in FSIs surrounded by PNNs revealed that both 1 and 5 d of cocaine exposure reduced the number of action potentials 2 h later. Synaptic changes demonstrated that 5 d of cocaine exposure increased the inhibition of FSIs, potentially reducing the inhibition of pyramidal neurons and contributing to their hyperexcitability during relapse behavior. These early and rapid responses to cocaine may alter the network stability of PV FSIs that partially mediate the persistent and chronic nature of drug addiction.

Original languageEnglish (US)
JournaleNeuro
Volume5
Issue number5
DOIs
StatePublished - Sep 1 2018

Fingerprint

Interneurons
Prefrontal Cortex
Cocaine
Parvalbumins
Pyramidal Cells
Electrophysiology
Action Potentials
Substance-Related Disorders
Extracellular Matrix
Staining and Labeling
Recurrence

Keywords

  • cocaine
  • interneurons
  • parvalbumin
  • perineuronal nets
  • prefrontal cortex

ASJC Scopus subject areas

  • Neuroscience(all)

Cite this

Cocaine Exposure Modulates Perineuronal Nets and Synaptic Excitability of Fast-Spiking Interneurons in the Medial Prefrontal Cortex. / Slaker, Megan L.; Jorgensen, Emily T.; Hegarty, Deborah M.; Liu, Xinyue; Kong, Yan; Zhang, Fuming; Linhardt, Robert J.; Brown, Travis E.; Aicher, Sue; Sorg, Barbara A.

In: eNeuro, Vol. 5, No. 5, 01.09.2018.

Research output: Contribution to journalArticle

Slaker, ML, Jorgensen, ET, Hegarty, DM, Liu, X, Kong, Y, Zhang, F, Linhardt, RJ, Brown, TE, Aicher, S & Sorg, BA 2018, 'Cocaine Exposure Modulates Perineuronal Nets and Synaptic Excitability of Fast-Spiking Interneurons in the Medial Prefrontal Cortex', eNeuro, vol. 5, no. 5. https://doi.org/10.1523/ENEURO.0221-18.2018
Slaker, Megan L. ; Jorgensen, Emily T. ; Hegarty, Deborah M. ; Liu, Xinyue ; Kong, Yan ; Zhang, Fuming ; Linhardt, Robert J. ; Brown, Travis E. ; Aicher, Sue ; Sorg, Barbara A. / Cocaine Exposure Modulates Perineuronal Nets and Synaptic Excitability of Fast-Spiking Interneurons in the Medial Prefrontal Cortex. In: eNeuro. 2018 ; Vol. 5, No. 5.
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AU - Kong, Yan

AU - Zhang, Fuming

AU - Linhardt, Robert J.

AU - Brown, Travis E.

AU - Aicher, Sue

AU - Sorg, Barbara A.

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