Fear signals vulnerability and appeasement, not threat

Abstract

Humans are not only fearful apes, but we also communicate our fear using social cues. Social fear displays typically elicit care and assistance in the real world and the lab. But in the psychology and neuroscience literature fearful expressions are commonly interpreted as “threat cues.” The fearful ape hypothesis suggests that fearful expressions should be instead considered appeasement and vulnerability cues.

Social displays of fearfulness – that is, fearful facial, vocal, or body expressions – are commonly interpreted by psychologists and neuroscientists as “threat cues”; that is, cues that primarily serve to signal that the perceiver may be in danger. Fearful expressions have been variously described as cues that “trigger an automatic response to potential danger” (Morris et al., 1996), “implicit signals of broad environmental threat” (e.g., Farber, Kim, Knodt, & Hariri, 2019), a “cue of potential threat” (Powers & Casey, 2015), and, “threatening” (Imbriano, Sussman, Jin, & Mohanty, 2020).

Grossmann's compelling synthesis of the social functions of fear in humans may fundamentally change this practice.

The idea that decontextualized fearful expressions primarily represent threat cues can be traced back at least to the early days of human functional brain imaging research, when several seminal studies investigated patterns of brain activation when participants viewed various types of facial expressions (Breiter et al., 1996; Morris et al., 1996; Phillips et al., 1997). All found increased recruitment of the amygdala when participants saw faces expressing fear relative to other emotions (happiness, disgust, or anger) or no emotion (neutral expressions) – a pattern that largely held up in subsequent research (Fusar-Poli et al., 2009).

The interpretation of these effects was strongly influenced by Morris et al. (1996), who surmised that, because “integrated responses to threat or danger … can be mediated by the amygdala,” one could infer that, “perceiving an expression of fear in a conspecific may trigger an automatic response to potential danger that accounts for the observed amygdala activation in response to fearful faces” (p. 814). But problems soon became apparent with the reverse inference that an amygdala response to a face means the face signals threat. For example, it was discovered that the amygdala responds more strongly to fearful expressions than to angry expressions (Fusar-Poli et al., 2009; Whalen et al., 2001), the latter of which clearly signal a direct interpersonal threat (Blair, 2012). In an effort to resolve this discrepancy, it was suggested that perhaps fear is the most alarming expression of all because it represents an ambiguous threat (Whalen et al., 2001) – that is, the expresser is not themselves the threat but is responding to an unspecified threat elsewhere in the environment. This remains a common interpretation of the social function of fear in psychology and neuroscience to this day (e.g., Farber et al., 2019; Imbriano et al., 2020).

But this interpretation has flaws. One is that if someone is looking at you in fear, an obvious potential reason – absent any other contextual cues – is that they are afraid of you (Rhoads et al., 2020). Another is that, as Grossmann's review makes clear, the “threat cue” interpretation of fear does not account for how perceivers actually respond to others' fear in the social world, which is often with care and the inhibition of aggression.

The care-eliciting effects of fear have been observed both in various social settings, as Grossmann describes, and in the laboratory. For example, even subliminally presented fearful expressions reliably elicit increased self-reported care and concern (Brethel-Haurwitz et al., 2017; Marsh & Ambady, 2007). Consistent with this, expressions of fear also reliably elicit behavioral approach in perceivers, as measured using a lever task (Hammer & Marsh, 2015; Marsh, Ambady, & Kleck, 2005b). This is the opposite response one would expect if perceivers primarily interpreted fearful expressions as threats. Thus, it appears that fear functions more reliably as a cue that conveys vulnerability and appeasement, similar to the bared-teeth displays other primates use to signal submission and appeasement (Vlaeyen et al., 2022), and to the submission and fear displays used in other alloparenting mammals like wolves (Schenkel, 1967). Human fearful expressions may elicit caring responses particularly effectively when displayed by children, consistent with Grossmann's hypothesis. But they may also succeed in eliciting care among adults in part because the components of a fearful expression – widened eyes, raised brows, and a rounded lower face – cause the expresser's face to appear more babyish (Marsh, Adams, & Kleck, 2005a) – which may stimulate human adults' alloparental tendencies.

How, then, should observed neural responses to fear cues be understood? Why does the amygdala respond so robustly to fearful expressions? One logical conclusion stemming from Grossmann's hypothesis is that amygdala responses to others' fear are empathic (Marsh, 2016). Just as the regions involved in coordinating the personal experience of pain are recruited when observing another's pain in order to interpret their experience and respond to them adaptively (Lamm et al., 2019), so the regions involved in coordinating the personal experience of fear (including the amygdala) may be recruited in response to others' fear in order to interpret their experience and respond adaptively. In many cases, the appropriate response to another's fear is protection and care. That unusually caring adults recruit the amygdala more than typical adults when viewing others' fear supports this conclusion (Marsh et al., 2014). Of course, in some contexts the most appropriate response to others' fear might be social fear learning (Olsson & Phelps, 2007) or marshaling one's own fearful response.

But fundamentally, if humans are indeed not only fearful apes, but apes endowed with a multitude of social cues to convey our fear to each other, it supports the idea that we are also caring apes who can generally be trusted to respond to others' displays of fear with the help they are seeking rather than selfishly fleeing or exploiting their vulnerability.

Both our fearfulness and our readiness to signal fear to one another can thus be interpreted as evidence of our species' prosocial nature.