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Review
. 2015 Sep;26(6):580-94.
doi: 10.1097/FBP.0000000000000167.

Dyadic social interaction inhibits cocaine-conditioned place preference and the associated activation of the accumbens corridor

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Review

Dyadic social interaction inhibits cocaine-conditioned place preference and the associated activation of the accumbens corridor

Gerald Zernig et al. Behav Pharmacol. 2015 Sep.

Abstract

Impaired social interaction is a hallmark symptom of many psychiatric disorders. In substance use disorders, impaired social interaction is triply harmful (a) because addicts increasingly prefer the drug of abuse to the natural reward of drug-free social interaction, thus worsening the progression of the disease by increasing their drug consumption, (b) because treatment adherence and, consequently, treatment success itself depends on the ability of the recovering addict to maintain social interaction and adhere to treatment, and (c) because socially interacting with an individual suffering from a substance use disorder may be harmful for others. Helping the addict reorient his/her behavior away from the drug of abuse toward social interaction would therefore be of considerable therapeutic benefit. This article reviews our work on the neural basis of such a reorientation from cocaine, as a prototypical drug of abuse, toward dyadic (i.e. one-to-one) social interaction and compares our findings with the effects of other potentially beneficial interventions, that is, environmental enrichment or paired housing, on the activation of the accumbens and other brain regions involved in behavior motivated by drugs of abuse or nondrug stimuli. Our experimental models are based on the conditioned place preference paradigm. As the therapeutically most promising finding, only four 15 min episodes of dyadic social interaction were able to inhibit both the subsequent reacquisition/re-expression of preference for cocaine and the neural activation associated with this behavior, that is, an increase in the expression of the immediate early gene Early Growth Response protein 1 (EGR1, Zif268) in the nucleus accumbens, basolateral and central amygdala, and the ventral tegmental area. The time spent in the cocaine-associated conditioning compartment was correlated with the density of EGR1-activated neurons not only in the medial core (AcbCm) and medial shell (AcbShm) of the nucleus accumbens, but was observed in all regions medial to the anterior commissure ('accumbens corridor'), including (from medial to lateral), the vertical limb of the diagonal band and the medial septum (VDB+MS), the major island of Calleja and the intermediate nucleus of the lateral septum (ICjM+LSI), the AcbShm, and the AcbCm. All effects were limited to GABAergic projection neurons (called 'medium spiny neurons', in the accumbens), encompassing both dopamine D1 receptor-expressing and D2 receptor-expressing medium spiny neuron subtypes. Our EGR1 expression findings were mirrored in multielectrode array recordings. Finally, we have validated our paradigm in C57BL/6 mice to make use of the plethora of transgenic models available in this genus.

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Figures

Fig. 1
Fig. 1
Timelines of the three experimental models used by our group. Details of the three experimental models are provided in the text. Red fields: place preference conditioning with cocaine (intraperitoneal injections, cocaine dissolved in saline in a volume of 1 ml/kg for rats, 10 ml/kg for mice). Tan field: extinction of cocaine conditioning by pairing the previously cocaine-associated conditioned place preference (CPP) compartment with i.p. saline injections. Green fields: conditioning to dyadic social interaction (preceded by an i.p. saline injection). Pretests (to quantify pre-CPP compartment bias) and CPP tests are not indicated here for the sake of clarity.
Fig. 2
Fig. 2
Times spent in the compartment associated with dyadic social interaction or cocaine: mouse versus rat comparison. Solid symbols show the time spent in the compartment associated with the stimulus of interest [(a), dyadic social interaction, int, green symbols; (b), 15 mg/kg i.p. cocaine, coc, red symbols] during the conditioned place preference (CPP) test (total test duration, 900 s). Each symbol represents the behavior of one individual animal. M, C57BL/6N mouse, square. R, Sprague–Dawley rat, triangle. All animals were male and weight matched (rats, 150–250 g; mice, 22–23 g). Open symbols represent transformed data, that is show the time spent in the compartment associated with the stimulus of interest minus the time spent in the saline-associated compartment. Black lines show the mean of the experimental group. The following numbers of animals and experimenters (given in parentheses) contributed toward each experimental group: M int, 42 mice (seven experimenters); R int, 27 rats (four experimenters); M coc, eight mice (two experimenters); and R coc, 26 rats (three experimenters). All groups except for the rat cocaine (R coc) and rat cocaine-saline (R coc-sal) groups passed all three normality tests used (Kolmogorov–Smirnov, D’Agostino–Pearson, Shapiro–Wilk; Prism 5; http://www.graphpad.com). After removing one visible outlier (time spent in the coc-associated compartment, 716 s) in the R coc group, the also R coc and R coc-sal group passed all normality tests too. i.p., intraperitoneally.
Fig. 3
Fig. 3
Accumbens corridor activation associated with the reacquisition/re-expression of cocaine CPP and its inhibition by dyadic social interaction. The correlations of EGR1 expression per mm2 versus the time spent in the cocaine compartment during the cocaine CPP reacquisition/re-expression test are shown for animals that had undergone cocaine conditioning, followed by extinction with saline (red triangles, filled) and for animals that were counterconditioned with social interaction after an initial cocaine conditioning (green circles, filled) before being subjected to a final cocaine challenge and tested for the reacquisition/re-expression of cocaine 24 h later. The diagram in the lower right corner was taken from the rat brain atlas of Paxinos and Watson (2007) and shows the following subregions of the accumbens corridor: aca, anterior commissure; AcbCm, medial accumbens core; AcbShm, medial accumbens shell; ICjM+LSI, major island of Calleja and intermediate nucleus of the lateral septum; VDB+MS, vertical limb of the diagonal band and medial septum. Solid lines show the correlation of data pooled from saline-extinguished (filled red triangles) and DSI-counterconditioned (filled green circles) animals. The respective correlation coefficients, r, and P values were for the VDB+MS: r=0.86, P<0.0001; ICjM+LSI: r=0.89, P<0.0001; AcbShm: r=0.87, P<0.0001; AcbCm: r=0.9, P<0.0001; AcbCl: r=0.33, P=0.12; CPu: r=0.41, P=0.07; and Cg1: r=−0.16, P=0. 29. There was no statistically significant correlation (shown as a dashed line) between the EGR1 expression per mm2 and the time spent in the cocaine compartment for animals injected noncontingently with cocaine (unfilled red triangles). This figure is an extraction and combination of the data presented in figures 6 and 8 of Prast et al. (2014b).

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