Social Fear Learning: from Animal Models to Human Function

Abstract

Learning about potential threats is critical for survival. Learned fear responses are acquired either through direct experiences or indirectly through social transmission. Social fear learning (SFL), also known as vicarious fear learning, is a paradigm successfully used for studying the transmission of threat information between individuals. Animal and human studies have begun to elucidate the behavioral, neural and molecular mechanisms of SFL. Recent research suggests that social learning mechanisms underlie a wide range of adaptive and maladaptive phenomena, from supporting flexible avoidance in dynamic environments to intergenerational transmission of trauma and anxiety disorders. This review discusses recent advances in SFL studies and their implications for basic, social and clinical sciences.

Keywords: emotional contagion; empathy; fear contagion; fear learning by proxy; intergenerational transmission; observational fear learning; vicarious fear learning.

Figure 1. Observational fear learning procedure used in human studies

During the training phase (left), an observer learns to fear a CS (blue rectangle) through watching on a screen a demonstrator receiving FC (electric shocks to the wrist paired with the CS). During the testing phase (right), the observer expresses fear during an exposure to the CS. (A white lightning bolt denotes an electric shock and red lightning bolts denote fear response).

Figure 2. Behavioral paradigms used in SFL studies in rodents

This figure depicts SFL behavioral paradigms used in rodent studies, with the left column showing the training and the right column showing the testing phase. In the most commonly used paradigm, during the training phase the observer (right) is placed together with a frightened demonstrator (left) and exposed to the CS (a shining light bulb for all experiments in our figure, although, various sensory modalities may be used) (A). In one variant of the SFL paradigm, the observer (right) and the demonstrator are physically isolated during training but are able to maintain a visual contact (B). In another variant of the SFL paradigm, the observer (right) is exposed to the prerecorded (or streamed life) vocalizations produced by the frightened demonstrator (C). In SFL studies relying on chemosignaling, the observer (right) and demonstrator (left) are physically isolated and the observer is exposed to the air delivered from the box with the frightened demonstrator (D).

Figure 3. A model of neural systems of SFL

The arrows describe the hypothetical flow of information between different functional brain regions that are most relevant to SFL. As in FC, the information about the CS and social cues signaling threat that is projected from the thalamus, hippocampus and cortical sites (or directly to the amygdala as in the case of olfactory cues) converges in the lateral nucleus of the amygdala (LA). The LA projects to the central nucleus of the amygdala (CE) that sends outputs to sites and systems directly controlling threat responses. Some information (e.g. about the context where learning occurs) reaches the LA through the basal nucleus of the amygdala (B) and some other cue representations project to the CE without the LA being involved. The medial nucleus of the amygdala (Me) mediates social behaviors and has bidirectional connections with the LA. The affective pain processing system, including midline nuclei of the thalamus (the ‘limbic’ thalamus), the anterior cingulate cortex (ACC) and the anterior insula (AI) are believed to process information about social cues signaling fear. The ACC-amygdala projections appear critical for the delivery of the information about social cues signaling threat to the amygdala. SFL is modified by medial prefrontal cortex (MPFC) which is responsible for interpretation of the other’s mental state and temporal-parietal junction (TPJ) that controls attention processes during learning. The dotted line represents a hypothetical alarm chemosignaling pathway that has been characterized in rodents but is mostly unknown in humans.