Between-subject transfer of emotional information evokes specific pattern of amygdala activation

Abstract

Emotional states displayed by an animal or a human can seriously affect behavior of their conspecifics. The amygdala plays a crucial role in the processing of emotions. In this study, we describe an experimental rat model of between-subject transfer of emotional information and its effects on activation of the amygdala. The rats were kept in pairs, and one animal (designated as "demonstrator") was treated to specific behavioral training of either foot-shock-reinforced context conditioning or just exposure to a novel context. We next examined the influence of the demonstrators on the exploratory behavior of their cagemates (called "observers") and the observers' performance of the acoustic startle response. We report that we can distinguish both groups of observers from the control animals (as shown by startle-response measure) and distinguish between observers (by means of indexing the exploration), with respect to whether they were paired with demonstrators treated to different experimental conditions. Furthermore, we show that the observers have most of their amygdala activated (as revealed by c-Fos mapping) to the same level as the demonstrators and, in the case of the central amygdala, to an even higher level. Moreover, the level of c-Fos expression in the observers reflected the specific behavioral treatment of the demonstrators with whom they were paired. Thus, in this study, we have shown that undefined emotional information transferred by a cohabitant rat can be evaluated and measured and that it evokes very strong and information-specific activation of the amygdala.

Fig. 1.

Schematic representation of the experimental procedures used.

Fig. 2.

Behavioral measures allowing investigation of the between-subject transfer of emotional information. (A) Mean ASR amplitudes ± SEM in the observer rats that were paired with demonstrator rats either receiving foot-shock (S-o), or not (NS-o) and H groups in five consecutive blocks of trials (four trials each). The three-way ANOVA revealed the following interactions: (i) subgroup × block of trials (F_(4,168) = 6.94, P < 0.0001) and (ii) the group × subgroup × block of trials (F_(8,168) = 2.28, P < 0.02). The effect of block of trials (F_(4,168) = 17.36, P < 0.0001) was also seen. The differences in temporal characteristics of the startle-response magnitude between the S-o, NS-o, and H groups were confirmed by two-way ANOVA, which revealed group × block of trials interaction (F_(8,84) = 2.79, P < 0.01). Further Duncan post hoc tests showed differences in ASR amplitudes between the N and NS groups in comparison with the H group in the first block (∗∗, P < 0.01) and between the S and H groups in the third block (○○, P < 0.01) of trials. Similar two-way ANOVA for demonstrators yielded neither group and block effects nor interaction. (B) The magnitude of exploration factor in the observers from the S-o, NS-o, and H groups. The exploration factor was calculated as a difference between the head movements made in the first 2 min after reunion of the demonstrators and the observers in the testing session and the head movements during the first 2 min of the preceding session. The three-way ANOVA was used to compare mean distances of head movements in the observers from the S-o, NS-o, and H groups in pretesting and testing sessions and two 2-min time intervals. Clear differences between groups were seen. Either group × session (F_(2,21) = 4.52, P < 0.02) or group × time intervals interactions (F_(2,21) = 4.13, P < 0.03) and the effect of time intervals (F_(1,21) = 43.47, P < 0.0001) were yielded. Bars denote ± SEM. ∗, P < 0.05.

Fig. 3.

c-Fos expression in the amygdala. (A) c-Fos immunoreactivity (black dots) observed in the amygdala of demonstrators and observers from the S group. (B) Mean number of c-Fos-immunopositive cell nuclei ± SEM; Ce, central nucleus; Me, medial nucleus; Co, cortical nuclei; L, lateral nucleus; B, basal nucleus; BM, basomedial nucleus. Three-way ANOVAs that were independently performed for each amygdalar nucleus revealed group effects (P < 0.0001). The subgroup effect was yielded only in the Ce nucleus (P < 0.0001). Neither the brain-slices effect nor double or triple interactions were seen. The levels of significance (Duncan tests) between groups and subgroups are shown. ∗∗, P < 0.01; ∗∗∗, P < 0.001.