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-shockreinforced 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.c-Fos ͉ emotion ͉ social communication ͉ brain mapping ͉ empathy E motions coordinate homeostasis of an organism in a complex, dynamic environment and participate in regulation of social behaviors. Emotional states displayed by an animal or a human can seriously affect the behavior of conspecifics. This fact has been demonstrated in numerous studies involving simulated and real panic situations, in which the presence of a leader determines the time of achieving the goal of a safe exit (1, 2). The escape panic could happen in life-threatening situations, such as fires in crowded buildings, but sometimes, interestingly, it seems to emerge without any apparent cause. This kind of panic is probably provoked by the specific emotional behavior of some members of the crowd.It is well known that the elaborate emotional systems of social species, such as humans, allow the recognition of very subtle emotional signals. Most of the functional imaging studies in humans have used emotional facial expressions as social signals presented to a subject to associate differences in the social content of stimuli with differences in the activity of the neural structures engaged in the processing of such stimuli (3). The results of these studies clearly pointed to the amygdala being involved in the processing of negatively valenced stimuli of biological importance (4-6). The neuroimaging studies also revealed that fearful faces are especially effective in activa...

Intergenerational transmission of emotional trauma through amygdala-dependent mother-to-infant transfer of specific fear

“…Our data show robust infant amygdala activation during the social transmission of fear (2-DG, c-Fos) consistent with adult social fear learning data (18,25). To determine if the amygdala is causally involved in social transmission of fear in pups, PND 11-13 pups were bilaterally implanted with intra-LBA amygdala cannulae and 2-3 d later (14) had the amygdala suppressed (using GABA A receptor agonist muscimol) or received vehicle (control) infusion followed by the social transmission of fear procedure.…”

The effect of age on the dynamics and the level of c-Fos activation in response to acute restraint in Lewis rats

“…The former is in contrast to several studies showing no age-dependent differences in basal c-Fos expression [5,13,28,34,36,42]. This discrepancy might be explained by very recent results obtained by Knapska et al [22]. They showed that structures involved in higher processing of emotional stimuli can be activated by between-subject transfer of information (for example by ultrasound vocalisation or odours [22]).…”

“…This discrepancy might be explained by very recent results obtained by Knapska et al [22]. They showed that structures involved in higher processing of emotional stimuli can be activated by between-subject transfer of information (for example by ultrasound vocalisation or odours [22]). In our experiment rats were housed in groups of two to three per cage and the cages were located close to each other in one experimental room.…”

“…With this method it has been demonstrated that an increase in anxiety is associated with increased c-Fos expression in specific brain areas implicated in the regulation of emotional behavior including the amygdala, hypothalamus and hippocampus [8,9,22,29,31,35].…”

Insular Cortex Mediates Approach and Avoidance Responses to Social Affective Stimuli

“…Translational rodent models that capture aspects of social affective cognition include emotion contagion [50][51][52][53] , social buffering 41 and even helping 54,55 (for review of models see 56 ). However, interpreting the underlying cognitive mechanisms is challenging because some paradigms involve repeated conditioning, direct exposure to a conspecific in pain or receiving aversive stimulation [57][58][59][60] , making it difficult to rule out self-serving or socially rewarding motives 41,61 .…”