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Role of perineuronal nets in the anterior dorsal lateral hypothalamic area in the acquisition of cocaine-induced conditioned place preference and self-administration

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Blacktop, Jordan M., Todd, Ryan P., Sorg, Barbara A.·2017·Neuropharmacology
DOI 10.1016/j.neuropharm.2017.03.018PMC PMC5492967
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Abstract

Addiction involves drug-induced neuroplasticity in the circuitry of motivated behavior, which includes the medial forebrain bundle and the lateral hypothalamic area. Emerging at the forefront of neuroplasticity regulation are specialized extracellular matrix (ECM) structures that form perineuronal nets (PNNs) around certain neurons, mainly parvalbumin positive (PV+), fast-spiking interneurons (FSINs), making them a promising target for the regulation of drug-induced neuroplasticity. Despite the emerging significance of PNNs in drug-induced neuroplasticity and the well-established role of the lateral hypothalamic area (LHA) in reward, reinforcement, and motivation, very little is known about how PNN-expressing neurons control drug-seeking behavior. We found that a discrete region of the anterior dorsal LHA (LHAad) exhibited robust PNN and dense ECM expression. Approximately 87% of parvalbumin positive (PV+) neurons co-expressed the PNN marker Wisteria floribunda agglutinin (WFA), while 62% of WFA positive (WFA+) neurons co-expressed PV in the LHAad of drug naïve rats. Removal of PNNs within this brain region via chrondroitinase ABC (Ch-ABC) administration abolished acquisition of cocaine-induced CPP and significantly attenuated the acquisition of cocaine self-administration (SA). Removal of LHAad PNNs did not affect locomotor activity, sucrose intake, sucrose-induced CPP, or acquisition of sucrose SA in separate groups of cocaine naïve animals. These data suggest that PNN-dependent neuroplasticity within the LHAad is critical for the acquisition of both cocaine-induced CPP and SA but is not general to all rewards, and that PNN degradation may have utility for the management of drug-associated behavioral plasticity and memory in cocaine addicts.

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  • Removal of PNNs with ChABC alters behavioural responses to drugs.

    “Several studies have demonstrated that removal of PNNs with ChABC alters behavioural responses to drugs.”

    From The extracellular matrix and perineuronal nets in memory (2022) · cites this paper as [159]

  • Removal of PNNs with ChABC in the mPFC or lateral hypothalamus prior to CPP training attenuates acquisition of the CPP memory, and removal after CPP training attenuates memory reconsolidation.

    “For example, removal of PNNs with ChABC in the mPFC or lateral hypothalamus prior to training for conditioned place preference (CPP) attenuates acquisition of the CPP memory [117, 159], and removal after CPP training also attenuates memory reconsolidation [117].”

    From The extracellular matrix and perineuronal nets in memory (2022) · cites this paper as [159]

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Authors
Blacktop, J. M., Todd, R. P., & Sorg, B. A.
Affiliations
Washington State University Vancouver (US)
Corresponding author
Blacktop, Jordan M.
ORCID
Venue
Neuropharmacology
Publisher
Elsevier BV
Published
2017-05
Volume
118
Pages
124-136
ISSN
0028-3908 (ISSN-L)
DOI
10.1016/j.neuropharm.2017.03.018
PMC
PMC5492967
OpenAlex
W2596554716
Cited by
43
References
10
Citations by year
2026: 1 · 2025: 4 · 2024: 5 · 2023: 3 · 2022: 4 · 2021: 6 · 2020: 7 · 2019: 2 · 2018: 7 · 2017: 4
FWCI
2.68
Type
journal article
Language
en
Open access
Licence
www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations
  • Neuropharmacology (publishedVersion)
  • PubMed (publishedVersion)
  • Europe PMC (PubMed Central) (acceptedVersion)
  • PubMed Central (acceptedVersion)
Funders
  • National Institute of Health (NIH) (DA033404)
  • Washington State Initiative 171 (Washington State University Alcohol
  • Drug Abuse Research Program (124777)
Topics
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
Keywords
perineuronal nets, cocaine, conditioned place preference, cocaine self-administration, extracellular matrix, parvalbumin interneurons, Wisteria floribunda agglutinin, drug-seeking behavior, addiction, reward
MeSH terms
Anesthetics, Local, Animals, Cocaine, Conditioning, Operant, Cues, Extinction, Psychological, Extracellular Matrix, Feeding Behavior, Hypothalamic Area, Lateral, Male, Neurons, Parvalbumins, Chondroitin Sulfate Proteoglycans, Reinforcement, Psychology, Self Administration, Time Factors, Rats, Sprague-Dawley, Chondroitin ABC Lyase, Receptors, N-Acetylglucosamine, Plant Lectins, Rats

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