Removal of perineuronal nets in the medial prefrontal cortex impairs the acquisition and reconsolidation of a cocaine-induced conditioned place preference memory

Megan Slaker, Lynn Churchill, Ryan P. Todd, Jordan M. Blacktop, Damian G. Zuloaga, Jacob Raber, Rebecca A. Darling, Travis E. Brown, Barbara A. Sorg

Research output: Contribution to journalArticle

64 Citations (Scopus)

Abstract

Pyramidal neurons in the medial prefrontal cortex (mPFC) critically contribute to cocaine-seeking behavior in humans and rodents. Activity of these neurons is significantly modulated by GABAergic, parvalbumin-containing, fast-spiking interneurons, the majority of which are enveloped by specialized structures of extracellular matrix called perineuronal nets (PNNs), which are integral to the mainte-nanceofmany types ofplasticity. Using a conditioned place preference (CPP) procedure,we found that removal of PNNs primarily from the prelimbic region of the mPFCofadult, male, Sprague Dawley rats impaired the acquisition and reconsolidation ofa cocaine-induced CPP memory. This impairment was accompanied by a decrease in the number of c-Fos-positive cells surrounded by PNNs. Following removal of PNNs, the frequency of inhibitory currents in mPFC pyramidal neurons was decreased; but following cocaine-induced CPP, both frequency and amplitudeof inhibitory currents were decreased. Our findings suggest that cocaine-induced plasticity isimpaired by removal of prelimbic mPFC PNNs and that PNNs may be a therapeutic target for disruption of cocaine CPP memories.

Original languageEnglish (US)
Pages (from-to)4190-4202
Number of pages13
JournalJournal of Neuroscience
Volume35
Issue number10
DOIs
StatePublished - 2015

Fingerprint

Prefrontal Cortex
Cocaine
Pyramidal Cells
Parvalbumins
Interneurons
Extracellular Matrix
Sprague Dawley Rats
Rodentia
Neurons
Therapeutics

Keywords

  • Cocaine
  • Conditioned place preference
  • Memory
  • Perineuronal net

ASJC Scopus subject areas

  • Neuroscience(all)

Cite this

Removal of perineuronal nets in the medial prefrontal cortex impairs the acquisition and reconsolidation of a cocaine-induced conditioned place preference memory. / Slaker, Megan; Churchill, Lynn; Todd, Ryan P.; Blacktop, Jordan M.; Zuloaga, Damian G.; Raber, Jacob; Darling, Rebecca A.; Brown, Travis E.; Sorg, Barbara A.

In: Journal of Neuroscience, Vol. 35, No. 10, 2015, p. 4190-4202.

Research output: Contribution to journalArticle

Slaker, Megan ; Churchill, Lynn ; Todd, Ryan P. ; Blacktop, Jordan M. ; Zuloaga, Damian G. ; Raber, Jacob ; Darling, Rebecca A. ; Brown, Travis E. ; Sorg, Barbara A. / Removal of perineuronal nets in the medial prefrontal cortex impairs the acquisition and reconsolidation of a cocaine-induced conditioned place preference memory. In: Journal of Neuroscience. 2015 ; Vol. 35, No. 10. pp. 4190-4202.
@article{58f2046afae44aa9bb7d7368f391898c,
title = "Removal of perineuronal nets in the medial prefrontal cortex impairs the acquisition and reconsolidation of a cocaine-induced conditioned place preference memory",
abstract = "Pyramidal neurons in the medial prefrontal cortex (mPFC) critically contribute to cocaine-seeking behavior in humans and rodents. Activity of these neurons is significantly modulated by GABAergic, parvalbumin-containing, fast-spiking interneurons, the majority of which are enveloped by specialized structures of extracellular matrix called perineuronal nets (PNNs), which are integral to the mainte-nanceofmany types ofplasticity. Using a conditioned place preference (CPP) procedure,we found that removal of PNNs primarily from the prelimbic region of the mPFCofadult, male, Sprague Dawley rats impaired the acquisition and reconsolidation ofa cocaine-induced CPP memory. This impairment was accompanied by a decrease in the number of c-Fos-positive cells surrounded by PNNs. Following removal of PNNs, the frequency of inhibitory currents in mPFC pyramidal neurons was decreased; but following cocaine-induced CPP, both frequency and amplitudeof inhibitory currents were decreased. Our findings suggest that cocaine-induced plasticity isimpaired by removal of prelimbic mPFC PNNs and that PNNs may be a therapeutic target for disruption of cocaine CPP memories.",
keywords = "Cocaine, Conditioned place preference, Memory, Perineuronal net",
author = "Megan Slaker and Lynn Churchill and Todd, {Ryan P.} and Blacktop, {Jordan M.} and Zuloaga, {Damian G.} and Jacob Raber and Darling, {Rebecca A.} and Brown, {Travis E.} and Sorg, {Barbara A.}",
year = "2015",
doi = "10.1523/JNEUROSCI.3592-14.2015",
language = "English (US)",
volume = "35",
pages = "4190--4202",
journal = "Journal of Neuroscience",
issn = "0270-6474",
publisher = "Society for Neuroscience",
number = "10",

}

TY - JOUR

T1 - Removal of perineuronal nets in the medial prefrontal cortex impairs the acquisition and reconsolidation of a cocaine-induced conditioned place preference memory

AU - Slaker, Megan

AU - Churchill, Lynn

AU - Todd, Ryan P.

AU - Blacktop, Jordan M.

AU - Zuloaga, Damian G.

AU - Raber, Jacob

AU - Darling, Rebecca A.

AU - Brown, Travis E.

AU - Sorg, Barbara A.

PY - 2015

Y1 - 2015

N2 - Pyramidal neurons in the medial prefrontal cortex (mPFC) critically contribute to cocaine-seeking behavior in humans and rodents. Activity of these neurons is significantly modulated by GABAergic, parvalbumin-containing, fast-spiking interneurons, the majority of which are enveloped by specialized structures of extracellular matrix called perineuronal nets (PNNs), which are integral to the mainte-nanceofmany types ofplasticity. Using a conditioned place preference (CPP) procedure,we found that removal of PNNs primarily from the prelimbic region of the mPFCofadult, male, Sprague Dawley rats impaired the acquisition and reconsolidation ofa cocaine-induced CPP memory. This impairment was accompanied by a decrease in the number of c-Fos-positive cells surrounded by PNNs. Following removal of PNNs, the frequency of inhibitory currents in mPFC pyramidal neurons was decreased; but following cocaine-induced CPP, both frequency and amplitudeof inhibitory currents were decreased. Our findings suggest that cocaine-induced plasticity isimpaired by removal of prelimbic mPFC PNNs and that PNNs may be a therapeutic target for disruption of cocaine CPP memories.

AB - Pyramidal neurons in the medial prefrontal cortex (mPFC) critically contribute to cocaine-seeking behavior in humans and rodents. Activity of these neurons is significantly modulated by GABAergic, parvalbumin-containing, fast-spiking interneurons, the majority of which are enveloped by specialized structures of extracellular matrix called perineuronal nets (PNNs), which are integral to the mainte-nanceofmany types ofplasticity. Using a conditioned place preference (CPP) procedure,we found that removal of PNNs primarily from the prelimbic region of the mPFCofadult, male, Sprague Dawley rats impaired the acquisition and reconsolidation ofa cocaine-induced CPP memory. This impairment was accompanied by a decrease in the number of c-Fos-positive cells surrounded by PNNs. Following removal of PNNs, the frequency of inhibitory currents in mPFC pyramidal neurons was decreased; but following cocaine-induced CPP, both frequency and amplitudeof inhibitory currents were decreased. Our findings suggest that cocaine-induced plasticity isimpaired by removal of prelimbic mPFC PNNs and that PNNs may be a therapeutic target for disruption of cocaine CPP memories.

KW - Cocaine

KW - Conditioned place preference

KW - Memory

KW - Perineuronal net

UR - http://www.scopus.com/inward/record.url?scp=84924439938&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84924439938&partnerID=8YFLogxK

U2 - 10.1523/JNEUROSCI.3592-14.2015

DO - 10.1523/JNEUROSCI.3592-14.2015

M3 - Article

C2 - 25762666

AN - SCOPUS:84924439938

VL - 35

SP - 4190

EP - 4202

JO - Journal of Neuroscience

JF - Journal of Neuroscience

SN - 0270-6474

IS - 10

ER -