A novel(ty) perspective of fear bias

Abstract

Grossmann presents an exciting and interesting theory on the function of fearfulness. In this commentary it is argued that fearfulness may be a byproduct of a larger executive functioning network and these early regulatory skills considered more broadly may be key building blocks for later cooperative behaviors.

Grossmann introduces the “fearful ape hypothesis,” an exciting perspective on the function and evolution of fearfulness. The author outlines associations between maternal sensitivity, early recognition and response to fearful expressions, and later prosocial outcomes. However, there may be a more comprehensive explanation, as a heightened response to fearfulness in infancy is not conclusive evidence for a highly specialized and evolved fear system. Here, we put forth an alternative perspective following three levels of evidence outlined in the target article: ontogeny, adaptive value, and mechanism. We argue that fearfulness in infancy may not be the root of future cooperation but rather fearfulness is a byproduct of a larger executive functioning/regulatory network (i.e., cognitive processes [e.g., visual working memory, inhibitory control] that aid in the regulation of thoughts, actions, and emotions).

The ontogeny of executive functioning abilities begins in infancy and one aspect of executive functioning development that is nicely outlined in the target article is fear bias (Blankenship et al., 2019). Fearful faces are less common in positive emoting moms, and thus infants would obtain less exposure to fearful faces compared to other emotions such as happiness (Downes, Bathelt, & De Haan, 2017; Ruba & Repacholi, 2020). Given the relatively minimal exposure to fear, the assessment of fear bias, or the enhanced attention to fearful compared to happy (and sometimes other target faces) indexed from emotion discrimination tasks (e.g., habituation and preferential looking), is thought to index novelty detection, a key precursor for executive functioning. Moreover, positive associations exist between infant fear bias and maternal positive emotionality providing further evidence for fear bias indexing novelty detection (de Haan, Belsky, Reid, Volein, & Johnson, 2004). Critically, attentional biases to fearful faces, novel objects, and other social stimuli are all linked to executive functioning outcomes, providing evidence for fear bias being just one behavior of a larger suite of behaviors encompassed in executive functioning (Blankenship et al., 2019).

One of the key brain regions introduced in the target article as mechanistic evidence for the fearful ape hypothesis is the dorsolateral prefrontal cortex. The dorsolateral prefrontal cortex is not typically considered in emotion perception, but rather experimental and correlational evidence has characterized the dorsolateral prefrontal cortex in supporting executive functions (Kelsey, Krol, Kret, & Grossmann, 2019; Nejati, Salehinejad, & Nitsche, 2018; Panikratova et al., 2020). Remarkably, these associations between dorsolateral prefrontal cortex connectivity and regulatory behaviors, such as increased orienting to stimuli, are seen very early in development (Kelsey, Farris, & Grossmann, 2021). In the target article, key mechanistic evidence for the fearful ape hypothesis is derived from a study finding a negative association between dorsolateral prefrontal cortex response to fearful faces at 7 months and instrumental helping at 14 months (Grossmann, Missana, & Krol, 2018). Here, it is important to note that this study also found an association between dorsolateral prefrontal cortex response and fear bias (an approximation for novelty), but not fearful behaviors assessed using a temperament questionnaire. This hints at the possibility that the dorsolateral prefrontal cortex response to fear may be an index of general executive functioning rather than a specific marker for fearful emotions and behaviors.

In support of the alternative hypothesis for a larger executive functioning network being the root of cooperation and the adaptive value of executive functioning, mothers with a high level of executive functioning are more responsive caregivers and raise children with greater executive functioning abilities, likely because of both genetic and environmental contributions (Ribner, Devine, Blair, Hughes, & Investigators, 2022). Critically, young children with greater executive functioning abilities go on to be more prosocial humans (Aguilar-Pardo, Martínez-Arias, & Colmenares, 2013; Traverso, Viterbori, & Usai, 2020).

Given the confounding between fearfulness and executive functioning, it is essential for future work to better isolate the unique contributions of fearfulness. More specifically, work testing components of the fearful ape hypothesis should include measures of executive functioning (e.g., visual working memory task, effortful control temperament assessments, etc.) to better understand the unique contributions. In addition, when assessing links between attentional and neural responses to fear similar to Grossmann et al. (2018), it is imperative to include a nonsocial novelty control condition. These additions will allow for a richer understanding of how fearfulness and general executive functioning abilities contribute to later prosocial development.

Overall, Grossmann presents exciting and innovative ideas that I think raise critical questions for the field. This commentary offers an alternative explanation for the ontogenetic and brain evidence of the “fearful ape hypothesis” in hopes of providing a roadmap for future research needed to disentangle these two accounts.