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Stress-induced brain activation: buffering role of social behavior and neuronal nicotinic receptors

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Abstract

Social behavior and stress responses both rely on activity in the prefrontal cortex (PFC) and amygdala. We previously reported that acute stress exposure impoverishes social repertoire and triggers behavioral rigidity, and that both effects are modulated by β2-containing nicotinic receptors. We, therefore, hypothesized that the activity of brain regions associated with the integration of social cues will be modulated by stress exposure. We mapped the expression of c-fos protein in all subregions of the PFC and basolateral (BLA) and central (Ce) areas of the amygdala in C57BL/6J (B6) and β2−/− mice. We show altered brain activity and differences in functional connectivity between the two genotypes after stress: the PFC and BLA were hyperactivated in B6 and hypo-activated in β2−/− mice, showing that the impact of stress on brain activity and functional organization depends on the nicotinic system. We also show that the effects of the opportunity to explore a novel environment or interact socially after acute stress depended on genotype: exploration induced only marginal PFC activation in both genotypes relative to stress alone, excluding a major role for β2 receptors in this process. However, social interaction following stress only activated the rostral and caudolateral areas of the PFC in B6 mice, while it induced a kindling of activation in all PFC and amygdalar areas in β2−/− mice. These results indicate that acute stress triggers important PFC-amygdala plasticity, social interaction has a buffering role during stress-induced brain activation, and β2 receptors contribute to the effects of social interaction under stress.

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Acknowledgements

This work was supported by the Centre National de la Recherche Scientifique (CNRS, UMR 9197), by the ANR-FLEXNEURIM and ANR-10-INBS-04 FranceBioImaging Grants. We thank Layla Veleanu for help with some behavioral and immunohistochemical experiments.

Funding

This work was supported by the Centre National de la Recherche Scientifique (CNRS, UMR 9197), by the ANR (FLEXNEURIM 09-BLAN-034002) and ANR (10-INBS-04 FranceBioImaging).

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Authors and Affiliations

  1. Neuroscience Paris-Saclay Institute (Neuro-PSI), UMR CNRS 9197, Université Paris-Sud, Bâtiment 446, 15 Bd Clémenceau, 91405, Orsay Cedex, France

    Anne Nosjean & Sylvie Granon

  2. Institut Pasteur, Unité d’Analyse d’Images Biologiques, CNRS UMR 3691, Paris, France

    Fabrice de Chaumont & Jean-Christophe Olivo-Marin

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  1. Anne Nosjean
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  2. Fabrice de Chaumont
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Correspondence to Anne Nosjean.

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This article does not contain any studies with human participants performed by any of the authors. This research involves only animals.

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All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. All procedures performed in studies involving animals were in accordance with the ethical standards of the institution or practice at which the studies were conducted. All experimental procedures were carried out in accordance with the EU Directive 2010/63/EU, Decree N 2013-118 of February 1st, 2013, and the French National Committee (87/848).

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Supplementary Fig. 1

. The number (top) and the total time (bottom) of social events statistically correlated with brain area activation in B6 or β2-/- dyads (see Figure 6 and Supplementary Table 4) during the 8 minute social interaction task. Only host mice were submitted to acute stress. Data are expressed as means ± SEM. Histograms show similar quantitative data in the two genotypes. (TIF 2686 KB)

Supplementary Fig. 2

. Plasma corticosterone levels (µg/dl) in different experimental conditions in B6 and β2-/- mice (stressed or not). Blood samples were collected in 3 different experimental conditions: A. 60 min after exit from animal facility. B. after the 45 min of restraint stress. C. after the exploration period. Values are means ± SEM. All comparisons were performed using Kruskal-Wallis one-way ANOVA followed by Mann-Whitney U-tests. Effect of exploration in not stressed mice: *p = 0.01; **p = 0.006. Effect of stress: †† p = 0.01. Effects of stress and exploration: ‡ ‡ p ≤ 0.007. Effect of exploration in stressed mice §p = 0.029. For each experimental procedure, the genotype effect was not significant (0.132 ≤ ps ≤ 0.686). Not Stress mice: n = 4 for each genotype. Stressed mice: n = 6 for each genotype. Mice submitted to exploration with no stress: n = 6 (B6) and n = 7 (β2-/-). Mice submitted to exploration and stress: n = 7 (B6) and n = 9 (β2-/-). (TIF 2876 KB)

Supplementary Table 1

. Statistical comparison between B6 and β2-/- mice with their respective controls (S vs Cnt) and between genotypes (β2-/- vs B6) in not stressed mice (Cnt) and in mice submitted to acute stress (S). Comparisons were performed on 4 independent groups with Kruskal-Wallis one-way ANOVA on Ranks (p) in the Global PFC and in the amygdala (a) and in the rostral, median and caudal PFC (b). When normality passed, data were subsequently analyzed with the Holm-Sidak method test (HS) and when data did not follow a Gaussian distribution it was tested with Mann-Whitney U-tests (MW). p of each test is indicated. Gray areas showed not significant comparisons. (DOCX 23 KB)

Supplementary Table 2

. Statistical analyses in B6 and β2-/- mice submitted to stress with no behavioral procedure (S), to stress followed by exploration of a novel environment (SE), and to stress followed by exploration and social interaction (SESI). Comparisons were performed on six independent groups using Kruskal-Wallis one-way ANOVA on Ranks (p) in the Global PFC and in the amygdala (a) and in the rostral, median and caudal PFC (b). When normality passed, data were subsequently analyzed with the Holm-Sidak method test (HS) and when data did not follow a Gaussian distribution it was tested with Mann-Whitney U-tests (MW). p of each test is indicated. Gray areas showed not significant comparisons. (DOCX 24 KB)

Supplementary Table 3

. Statistical analyses between B6 and β2-/- mice submitted to stress with no behavioral procedure (S), to stress followed by exploration of a novel environment (SE), and to stress followed by exploration of a novel exploration and social interaction (SESI). Statistical analyses were performed on six independent groups using Kruskal-Wallis one-way ANOVA on Ranks (p) in the Global PFC and in the amygdala (a) and in the rostral, median and caudal PFC (b). When normality passed, data were subsequently analyzed with the Holm-Sidak method test (HS) and when data did not follow a Gaussian distribution it was tested with Mann-Whitney U-tests (MW). p of each test is indicated. Gray areas showed not significant comparisons. (DOCX 22 KB)

Supplementary Table 4

. Social behaviors correlated with c-fos protein expression in specific brain areas. Categories and sub-categories of behavioral events during social interaction between an isolated host mouse (IH, black) and a social visitor mouse (SV, white) are extracted from MiceProfiler software (de Chaumont et al. 2012). Only events that correlated with brain structures (see Fig. 6) are represented, i.e., 12 events over the 27 events analyzed. These events are: contact events (close contacts, oral-genital and side-by-side contacts, categories 1 to 3), relative position events (defined by the position of one mouse with regard to the other one, SV mouse is behind IH mouse, category 4), dynamic events initiated by the SV mouse (categories 5 to 7) or by the IH mouse (categories 8 to 11) and IH stop events (category 12). Aggressiveness defined by cumulated numbers of tail rattling exhibited by IH mice and battles defined by cumulated numbers of fight between IH and SV mice, as well as dominance were also analyzed. (DOCX 56 KB)

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Nosjean, A., de Chaumont, F., Olivo-Marin, JC. et al. Stress-induced brain activation: buffering role of social behavior and neuronal nicotinic receptors. Brain Struct Funct 223, 4259–4274 (2018). https://doi.org/10.1007/s00429-018-1745-7

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