Cognitive rigidity and BDNF-mediated frontostriatal glutamate neuroadaptations during spontaneous nicotine withdrawal.
Adaptation, Physiological
/ drug effects
Animals
Behavior, Animal
Brain-Derived Neurotrophic Factor
/ metabolism
Cognition
/ drug effects
Conditioning, Operant
/ drug effects
Corpus Striatum
/ drug effects
Discrimination, Psychological
/ drug effects
Frontal Lobe
/ drug effects
Glutamic Acid
/ metabolism
Male
Mice, Inbred C57BL
Nicotine
/ administration & dosage
Nicotinic Agonists
/ administration & dosage
Substance Withdrawal Syndrome
/ metabolism
Synaptic Transmission
/ drug effects
Journal
Neuropsychopharmacology : official publication of the American College of Neuropsychopharmacology
ISSN: 1740-634X
Titre abrégé: Neuropsychopharmacology
Pays: England
ID NLM: 8904907
Informations de publication
Date de publication:
04 2020
04 2020
Historique:
received:
14
07
2019
accepted:
14
11
2019
revised:
13
10
2019
pubmed:
22
11
2019
medline:
31
3
2021
entrez:
22
11
2019
Statut:
ppublish
Résumé
Cognitive flexibility is the ability to switch strategic responses adaptively in changing environments. Cognitive rigidity imposed by neural circuit adaptations during nicotine abstinence may foster maladaptive nicotine taking in addicts. We systematically examined the effects of spontaneous withdrawal in mice exposed to either nicotine (6.3 or 18 mg/kg/day) or saline for 14 days on cognitive flexibility using an operant strategy set-shifting task. Because frontostriatal circuits are critical for cognitive flexibility and brain-derived neurotrophic factor (BDNF) modulates glutamate plasticity in these circuits, we also explored the effects of nicotine withdrawal on these neurochemical substrates. Mice undergoing nicotine withdrawal required more trials to attain strategy-switching criterion. Error analysis show that animals withdrawn from both nicotine doses committed higher perseverative errors, which correlated with measures of anxiety. However, animals treated with the higher nicotine dose also displayed more strategy maintenance errors that remained independent of negative affect. BDNF mRNA expression increased in the medial prefrontal cortex (mPFC) following nicotine withdrawal. Surprisingly, BDNF protein declined in mPFC but was elevated in dorsal striatum (DS). DS BDNF protein positively correlated with perseverative and maintenance errors, suggesting mPFC-DS overflow of BDNF during withdrawal. BDNF-evoked glutamate release and synapsin phosphorylation was attenuated within DS synapses, but enhanced in the nucleus accumbens, suggesting a dichotomous role of BDNF signaling in striatal regions. Taken together, these data suggest that spontaneous nicotine withdrawal impairs distinct components of cognitive set-shifting and these deficits may be linked to BDNF-mediated alterations in glutamate signaling dynamics in discrete frontostriatal circuits.
Identifiants
pubmed: 31752015
doi: 10.1038/s41386-019-0574-6
pii: 10.1038/s41386-019-0574-6
pmc: PMC7075915
doi:
Substances chimiques
Bdnf protein, mouse
0
Brain-Derived Neurotrophic Factor
0
Nicotinic Agonists
0
Glutamic Acid
3KX376GY7L
Nicotine
6M3C89ZY6R
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Langues
eng
Sous-ensembles de citation
IM
Pagination
866-876Subventions
Organisme : NIDA NIH HHS
ID : R03 DA037421
Pays : United States
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