Memories of Opiate Withdrawal Emotional States Correlate with Specific Gamma Oscillations in the Nucleus Accumbens.

Cyril Dejean, Mathieu Sitko, Paul Girardeau, Amine Bennabi, Stéphanie Caillé, Martine Cador, Thomas Boraud, Catherine Le Moine
Neuropsychopharmacol. 2016-12-06; 42(5): 1157-1168
DOI: 10.1038/npp.2016.272

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Dejean C(1)(2), Sitko M(1)(2), Girardeau P(1)(2), Bennabi A(3)(4), Caillé S(1)(2), Cador M(1)(2), Boraud T(5)(6), Le Moine C(1)(2).

Author information:
(1)Université de Bordeaux, INCIA, UMR 5287, Bordeaux, France.
(2)CNRS, INCIA, UMR 5287, Bordeaux, France.
(3)Université de Bordeaux, I2M, UMR 5295, Bordeaux, France.
(4)CNRS, I2M, UMR 5295, Bordeaux, France.
(5)Université de Bordeaux, IMN, UMR 5293, Bordeaux, France.
(6)CNRS, IMN, UMR 5293, Bordeaux, France.

Affective memories associated with the negative emotional state experienced
during opiate withdrawal are central in maintaining drug taking, seeking, and
relapse. Nucleus accumbens (NAC) is a key structure for both acute withdrawal and
withdrawal memories reactivation, but the NAC neuron coding properties
underpinning the expression of these memories remain largely unknown. Here we
aimed at deciphering the role of NAC neurons in the encoding and retrieval of
opiate withdrawal memory. Chronic single neuron and local field potentials
recordings were performed in morphine-dependent rats and placebo controls.
Animals were subjected to an unbiased conditioned placed aversion protocol with
one compartment (CS+) paired with naloxone-precipitated withdrawal, a second
compartment with saline injection (CS-), and a third being neutral (no pairing).
After conditioning, animals displayed a typical place aversion for CS+ and
developed a preference for CS- characteristic of safety learning. We found that
distinct NAC neurons code for CS+ or CS-. Both populations also displayed highly
specific oscillatory dynamics, CS+ and CS- neurons, respectively, following 80 Hz
(G80) and 60 Hz (G60) local field potential gamma rhythms. Finally, we found that
the balance between G60 and G80 rhythms strongly correlated both with the ongoing
behavior of the animal and the strength of the conditioning. We demonstrate here
that the aversive and preferred environments are underpinned by distinct groups
of NAC neurons as well as specific oscillatory dynamics. This suggest that
G60/G80 interplay-established through the conditioning process-serves as a robust
and versatile mechanism for a fine coding of the environment emotional weight.

DOI: 10.1038/npp.2016.272
PMCID: PMC5506790
PMID: 27922595 [Indexed for MEDLINE]

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