More than fear: Contributions of biobehavioral synchrony and infants' reactivity to cooperative care

Abstract

We present two challenges to the fearful ape hypothesis: (1) biobehavioral synchrony precedes and moderates the effects of fear on cooperative care, and (2) cooperative care emerges in a more bidirectional manner than Grossmann acknowledges. We present evidence demonstrating how dyadic differences in co-regulation and individual differences in infants' reactivity shape caregivers' responses to infant affect.

Expressing and recognizing fear in conspecifics is critical to survival. In the fearful ape hypothesis, Grossmann thoughtfully integrates evidence from comparative, developmental, and neuroscience research to explain how fear developed differently in humans compared to our primate relatives. By focusing exclusively on fear, however, some of the most complex dynamic factors contributing to the development of cooperative care are neglected. We present two challenges to the fearful ape hypothesis: (1) biobehavioral synchrony is a precursor to cooperative care that precedes the development of fear and varies as a function of a multitude of factors, and (2) cooperative care emerges in a more bidirectional manner than implied by this target article.

First, most accounts, including Grossmann's, suggest that fear does not develop until the latter half of the first year. Yet, infants are already engaging in biobehavioral synchrony with their caregivers in the first few months of life (e.g., Feldman, 2007). Synchrony is highly associated with early cooperative behavior and contributes to the development of infants' emotion regulation (Feldman, Greenbaum, & Yirmiya, 1999), including their negative affect in novel or stressful situations such as the still-face paradigm (Tronick, Als, Adamson, Wise, & Brazelton, 1978). For example, infants often exhibit distress when mothers withdraw interactive cues during the still-face episode because it violates their expectations about parental responsiveness (Jones-Mason, Alkon, Coccia, & Bush, 2018). Critically, synchrony is not present all the time even when the mother is contingently responsive, because successful affective communication between mother and infant involves a series of mismatched states that are repeatedly repaired through the dynamic and reciprocal interaction of the mother and child (Tronick & Beeghly, 2011). Recent work from our laboratory points to physiological synchrony as a key moderator of infants' affect regulation. We found that once mothers resume engagement following the still-face stressor, there is a significant reduction of negative affect for those infants who displayed positive physiological synchrony with their mothers during the initial face-to-face episode, but only among infants with less developed autonomic nervous systems (Abney, DaSilva, & Bertenthal, 2021). Mothers also dynamically alter their behaviors, including their gaze, facial expressions, vocalizations, and movements, to match those of their infants (e.g., Chong, Werker, Russell, & Carroll, 2003; MacLean et al., 2014). Moreover, high values on a composite measure of maternal prosody are associated with a reduction of infant negative affect following the still face, with larger reductions observed among infants with lower capacity for self-regulation (Kolacz, DaSilva, Lewis, Bertenthal, & Porges, 2022). These results are important because they demonstrate that biobehavioral synchrony changes as a function of the characteristics of the dyad as well as infants' developmental status.

The fearful ape hypothesis focuses too narrowly on fear as a trigger of cooperative care without sufficient acknowledgement of the many other affective factors that contribute to effective parenting. Over time, repeated interactions with responsive caregivers provide predictability and safety for the infant, which in turn fosters the development of secure attachment with caregivers (Gee & Cohodes, 2021). Importantly, good parenting develops both through responding to infants' distress, but also through responding to other emotions, including positive emotions such as joy (Leerkes, Blankson, & O'Brien, 2009; Lohaus, Keller, Ball, Elben, & Voelker, 2001) and interest (Hammond & Drummond, 2019). The sharing of positive experiences is foundational to healthy caregiver–child interactions (e.g., Brown & Fredrickson, 2021; Ramsey & Gentzler, 2015). By focusing exclusively on fear, Grossmann overlooks how maternal responsiveness to other emotions, and early, recurring experiences with parental co-regulation more broadly, lead to positive socioemotional development and cooperative care.

Second, the fearful ape hypothesis presents fearfulness as a state of helplessness that the caregiver must respond to without considering bidirectional pathways through which the infant has the agency to dynamically influence the interaction. In three well-known paradigms for infant research – still face, strange situation, and visual cliff – infants are faced with a challenge that violates their expectations. Yet, it is not the case that all infants exhibit negative affect and wait for their caregivers to soothe them. Rather, many infants actively solicit responses from their caregivers or look for cues signaling how to behave. For example, some infants as young as 2–3 months will attempt to re-engage their still-faced mother through social bids – looking at her while smiling or vocalizing (Bigelow & Power, 2016). Infants will also use social referencing by attending to adults' facial expressions to gauge how to respond to their uncertain situation, such as whether to traverse the deep side of the visual cliff (Sorce, Emde, Campos, & Klinnert, 1985), or what to do when presented with an unfamiliar toy (Klinnert, Emde, Butterfield, & Campos, 1986). Over the course of the first year, infant–caregiver interactions become more interactive and bidirectional, such that infants initiate and actively elicit responses from their caregivers just as caregivers are responding to their infants (Beebe et al., 2016; Chow, Haltigan, & Messinger, 2010; Tronick & Gianino, 1986). These changes in communicative pathways are further influenced by infants' temperament because differences in reactivity interact with maternal sensitivity and responsiveness to the child's needs. Notably, infants with negative temperaments receive less responsive parenting, including reduced parental co-regulation, compared to their less fussy peers (Bridgett et al., 2009; Mills-Koonce et al., 2007). In sum, infants' own behaviors influence and elicit responses from their caregivers, suggesting that cooperative care involves more than the caregivers' response to the child.

In conclusion, the relation between the emergence of fear and cooperative care is more complex and multifaceted than implied by the fearful ape hypothesis. The reviewed evidence supporting how fear contributes to cooperative care is incomplete because it neglects the emergence of cooperative care in the broader context of infant–parent affect regulation, particularly early experiences with caregivers co-regulating both negative and positive emotions. Children's fearful responses may be adaptive in eliciting cooperative care, but not all the time and not for all individuals. This hypothesis overlooks many of the complex interactions between emotion, temperament, and biobehavioral synchrony that shape good parenting and cooperative care. As we discussed, cooperative care emerges from co-regulation, and as such it is a co-created experience that depends jointly on the caregiver as well as the child.