Neural Substrates of Automatic Social Perception

III.2.1. Amygdala

The original description of amygdala function related to emotion perception was established

more than seventy years ago by Kluver and Bucy [107]. By performing temporal lobectomies in

rhesus monkeys, these authors observed reduced fear-responses, increased exploratory behavior,

and hyper-sexualism in the lesioned animals [108], all constituting important alterations of

fundamental social behaviors (today also known as Kluver-Bucy syndrome). In humans, evidence

for amygdala involvement in social emotional processes became only available from the 1990ies,

when lesion studies showed impairments in negative emotion recognition from the face in general,

and fear in particular [25]. Such findings were later extended by a large body of research using

functional neuro-imaging, which demonstrated a key role for the amygdala in a range of emotional

and social domains, including recognition of facial [34] and vocal [66] emotions, discrimination of

mutual gaze contact [47, 48], but also personal relevance [69], as well as processing and learning

of various emotional stimuli [108]. Amygdala dysfunction has also been found in various disorders

with emotional and social disturbances, including autism [109], sociopathy [110], depression [111], or neuro-genetic syndromes such as the 22q11.2 deletion syndrome (see Figure M9 below; [112]).

Figure M9: Abnormal response to fearful faces in amygdala for subjects with 22q11.2 deletion syndrome (reproduced from [112]). A response to fearful faces on first presentation with subsequent repetition effect suppression for fearful faces in the amygdala is observed only in healthy control subjects (blue) but not in patients (purple). No such effect is present in both populations for neutral faces.

Behavioral animal as well as human functional investigations of amygdala function have particularly revealed its implication in the encoding and storage of memories acquired through fear conditioning, and thus implicit negative emotional learning and memory [113]. Subsequently, the amygdala was also attributed an important role in the modulation of explicit memory consolidation as a function of arousal, by “… favoring stimuli that are predisposed to lead to an emotional reaction …” [108]. By demonstrating that amygdala activation to fearful (versus neutral) faces could be found even if such faces were not attended consciously [114], and that enhanced activation in visual brain areas to fearful faces was absent in patients with amygdala damage [115], a more general function subserving the preferential processing of emotional and potentially threatening information was proposed for the amygdala. Further, the amygdala has been conceptualized as a

“relevance detector” [69], involved in the appraisal of a wide variety of negative as well as positive

[116] and even neutral [117] stimuli according to their significance for the goals, needs and

well-being of an organism at a specific moment in time.

More specifically related to social perception, the amygdala has been shown to contribute to the formation of first impressions about people based on subjective preference [118]. Such research was fuelled by findings that amygdala activity reflects social inferences based on trustworthiness [119] and implicit attitudes in the context of racial prejudice [55] and other social stigmas [58, 59].

Because such inferences not only involve information about others but also depend on the self – which is presumably stored as automatically accessible knowledge in the form of strong self-schemas –, the amygdala has also been found to be activated during self-descriptiveness judgments [120].

Therefore, besides mediating basic emotion recognition and implicit as well as explicit emotional memory formation and retrieval, the amygdala is thought to play an important role in automatic social evaluations, by means of evolutionary determined biological mechanisms or representations stored from previous experience.

III.2.2. Basal Ganglia

The basal ganglia are an assembly of nuclei including the putamen, caudate, globus pallidus, and nucleus accumbens. Generally, these structures are activated during implicit and probabilistic learning, motor skill acquisition, as well as the evaluation and prediction of both negative and positive outcomes, but their ventral division is most prominently described to represent reward-related signals during positive motivational events, such as addictive drug-administration or monetary gains [24].

Regarding social perception, increased activity in the basal ganglia has been found during the exposure to pictures of a romantic partner or own child [63], consistent with a role in coding for the positive hedonic valence of romantic and maternal love, as well as during presentation of unknown happy faces [121], thus representing social reward in general. Moreover, the same brain regions have been found activated in response to cooperative partners or cooperative play, thereby representing fairness and trust [79], also measurable through altruistic punishment [122]. Finally, basal ganglia activation has been observed as a function of social hierarchy, either when increasing social status [123], or when winning more money than somebody referred to for social comparison [124].

In sum, the basal ganglia seem to code for the rewarding value of various positive social

interactions and scenarios. These include intimate social cues such as romantic and maternal love,

fairness and trust during cooperation, as well as more general social rewards as conveyed by happy facial expressions or increases in social rank.

III.2.3. Lateral Temporal Cortex

The lateral temporal cortex includes two areas important for social perception, namely the posterior superior temporal sulcus (pSTS) and the anterior temporal pole (ATP).

The pSTS has been ascribed an important role in the detection of biological motion and is thus thought to contribute to the decoding of perceived action in others [71], which is crucial for subsequent higher-order theory of mind processes.

The ATP has been found activated during the exposure to a variety of familiar stimuli, including faces, names and landscapes, implying these areas in the retrieval of autobiographical or episodic memory information [33]. In addition, the (superior) ATP has been linked with the representation of abstract conceptual knowledge of social behaviors [125].

Together, the pSTS and ATP therefore importantly contribute to familiar face perception, theory of mind, and flexible evaluation of social behavior.

III.2.4. Dorsal Anterior Cingulate Cortex

The dorsal anterior cingulate cortex (dACC) is located in the posterior region of the rostral medial frontal cortex (prMFC), comprising Brodmann areas 8, 9, 24 and 32, and has been associated with cognitive tasks related to action representation, such as attention and error/conflict monitoring [88, 126, 127], but also implicated in the so-called pain-matrix and affective responses during nociception [52].

Accordingly, social neuroscience paradigms have found dACC activation in situations of social separation and rejection, presumably coding for both the cognitive conflict caused by expectancy violation [65], as well as subjective distress (or “pain”) experienced during social exclusion [128, 129]. Moreover, the dACC has been implicated in affective processes related to empathy, especially in paradigms using the observation of another person feeling physical pain [52, 130].

Such results led to the hypothesis that “… mammalian social pain may have evolved out of the

existing system for physical pain …” [6, 64].

III.2.5. Ventro-medial Prefrontal Cortex

The only cortical prefrontal area – ventromedial prefrontal cortex (VMPFC) – listed as part of the automatic x-system lies at the intersection between Brodmann areas 10 and 11, and also include areas in the orbital medial frontal cortex (oMFC; [126]).

Originally, the VMPFC has been implicated in monitoring of rewards and punishments [131]. More recently, its function has been extended to the guidance of behavior in terms of updating the value of possible outcomes and the monitoring of externally guided actions [126], particularly through reinforcement-guided decision making and in terms of context-sensitive stimulus evaluation [127].

In social neuroscience paradigms, VMPFC activity has been found during the formation of implicit attitudes and behavioral preferences [132], as well as counterfactual judgments and regret [133].

Similarly, VMPFC damage was linked with empathic deficits [134] because VMPFC activity is thought to “… contribute to the additional processes involved by empathy over direct feeling …” [6], which is probably related to the fact that VMPFC is strongly connected to sensory association areas (see below – Chapter III.2.6. – and [126, 127]).

In sum, the VMPFC is thought to represent “… certain aspects of over-learned associated social

knowledge …” [135] and might thus automatically guide social behavior through rapid evaluations

of social emotional contextual cues.