No CrossRef data available.
Article contents
Heightened fearfulness in infants is not adaptive
Published online by Cambridge University Press: 08 May 2023
Abstract
Grossmann proposes the “fearful ape hypothesis,” suggesting that heightened fearfulness in early life is evolutionarily adaptive. We question this claim with evidence that (1) perceived fearfulness in children is associated with negative, not positive long-term outcomes; (2) caregivers are responsive to all affective behaviors, not just those perceived as fearful; and (3) caregiver responsiveness serves to reduce perceived fearfulness.
- Type
- Open Peer Commentary
- Information
- Copyright
- Copyright © The Author(s), 2023. Published by Cambridge University Press
References
Barrett, L. F., Adolphs, R., Marsella, S., Martinez, A. M., & Pollak, S. D. (2019). Emotional expressions reconsidered: Challenges to inferring emotion from human facial movements. Psychological Science in the Public Interest, 20, 1–68. doi: 10.1177/1529100619832930CrossRefGoogle ScholarPubMed
Bennett, D. S., Bendersky, M., & Lewis, M. (2002). Facial expressivity at 4 months: A context by expression analysis. Infancy, 1, 97–113. doi: 10.1207/S15327078IN0301_5CrossRefGoogle Scholar
Bornstein, M. H., Putnick, D. L., Rigo, P., Esposito, G., Swain, J. E., Suwalsky, J. T. D., … Venuti, P. (2017). Neurobiology of culturally common maternal responses to infant cry. Proceedings of the National Academy of Sciences, 114, E9465–E9473. doi: 10.1073/pnas.1712022114CrossRefGoogle ScholarPubMed
Bornstein, M. H., Tamis-LeMonda, C. S., Tal, J., Ludemann, P., Toda, S., Rahn, C. W., … Vardi, D. (1992). Maternal responsiveness to infants in three societies: The United States, France, and Japan. Child Development, 63, 808–821. doi: 10.1111/j.1467-8624.1992.tb01663.xCrossRefGoogle ScholarPubMed
Buss, K. A., & McDoniel, M. E. (2016). Improving the prediction of risk for anxiety development in temperamentally fearful children. Current Directions in Psychological Science, 25, 14–20. doi: 10.1177/0963721415611601CrossRefGoogle ScholarPubMed
Callaghan, B., Meyer, H., Opendak, M., Van Tieghem, M., Harmon, C., Li, A., … Tottenham, N. (2019). Using a developmental ecology framework to align fear neurobiology across species. Annual Reviews of Clinical Psychology, 15, 345–369. doi: 10.1146/annurev-clinpsy-050718-095727CrossRefGoogle ScholarPubMed
Camras, L. A., Oster, H., Bakeman, R., Meng, Z., Ujiie, T., & Campos, J. J. (2007). Do infants show distinct negative facial expressions for fear and anger? Emotional expression in 11-month-old European American, Chinese, and Japanese infants. Infancy, 11, 131–155. doi: 10.1111/j.1532-7078.2007.tb00219.xCrossRefGoogle Scholar
Chóliz, M., Fernández-Abascal, E. G., & Martínez-Sánchez, F. (2013). Infant crying: Pattern of weeping, recognition of emotion and affective reactions in observers. The Spanish Journal of Psychology, 15, 978–988. doi: 10.5209/rev_SJOP.2012.v15.n3.39389CrossRefGoogle Scholar
Chronis-Tuscano, A., Dengan, K. A., Pine, D. S., Perez-Edgar, K., Henderson, H. A., Diaz, Y., … Fox, N. A. (2009). Stable early maternal report of behavioral inhibition predicts lifetime social anxiety disorders in adolescence. Journal of the American Academy of Child & Adolescent Psychiatry, 48, 928–935. doi: 10.1097/CHI.0b013e3181ae09dfCrossRefGoogle ScholarPubMed
Clauss, J. A., & Blackford, J. U. (2012). Behavioral inhibition and risk for developing social anxiety disorder: A meta-analytic study. Journal of the American Academy of Child & Adolescent Psychiatry, 51, 1066–1075. doi: 10.1016/j.jaac.2012.08.002CrossRefGoogle ScholarPubMed
Coplan, R. J., Wilson, J., Frohlick, S. L., & Zelenski, J. (2006). A person-oriented analysis of behavioral inhibition and behavioral activation in children. Personality and Individual Differences, 41, 917–927. doi: 10.1016/j.paid.2006.02.019CrossRefGoogle Scholar
Fox, N. A., Barker, T. V., White, L. K., Suway, J. G., & Pine, D. S. (2013). Commentary: To intervene or not? Appreciating or treating individual differences in childhood temperament – Remarks on Rapee. Journal of Child Psychology and Psychiatry, 54, 789–790.CrossRefGoogle ScholarPubMed
Fox, N. A., Buzzell, G. A., Morales, S., Valadez, E. A., Wilson, M., & Henderson, H. A. (2021). Understanding the emergence of social anxiety in children with behavioral inhibition. Biological Psychiatry, 89, 681–689. doi: 10.1016/j.biopsych.2020.10.004CrossRefGoogle ScholarPubMed
Gee, D. G., Gabard-Durnam, L., Telzer, E. H., Humphreys, K. L., Goff, B., Shapiro, M., … Tottenham, N. (2014). Psychological Science, 25, 2067–2078. doi: 10.1002/dev.20531CrossRefGoogle Scholar
Howard, M., Muris, P., Loxton, H., & Wege, A. (2017). Anxiety-proneness, anxiety symptoms, and the role of parental overprotection in young South African children. Journal of Child and Family Studies, 26, 262–270. doi: 10.1007/s10826-016-0545-zCrossRefGoogle Scholar
Kivijarvi, M., Voeten, M. J. M., Niemela, P., Raiha, H., Lertola, K., & Piha, J. (2001). Maternal sensitivity behavior and infant behavior in early interaction. Infant Mental Health Journal, 22, 627–640. doi: 10.1002/imhj.1023CrossRefGoogle Scholar
Mesman, J., Oster, H., & Camras, L. (2012). Parental sensitivity to infant distress: What do discrete negative emotions have to do with it? Attachment & Human Development, 14, 337–348. doi: 10.1080/14616734.2012.691649CrossRefGoogle Scholar
Sandstrom, A., Uher, R., & Pavlova, B. (2020). Prospective association between childhood behavioral inhibition and anxiety: A meta-analysis. Journal of Abnormal Child Psychology, 48, 57–66. doi: 10.1007/s10802-019-00588-5Google ScholarPubMed
Sears, M. S., Repetti, R. L., Reynolds, B. M., & Sperling, J. B. (2014). A naturalistic observational study of children's expressions of anger in the family context. Emotion, 14, 272–283. doi: 10.1037/a0034753CrossRefGoogle ScholarPubMed
Thompson-Booth, C., Viding, E., Mayes, L. C., Rutherford, H. J. V., Hodsoll, S., & McCrory, E. J. (2013). Here's looking at you, kid: Attention to infant emotional faces in mothers and non-mothers. Developmental Science, 17, 35–46. doi: 10.1111/desc.12090CrossRefGoogle ScholarPubMed
Tottenham, N. (2012). Human amygdala development in the absence of species-expected caregiving. Developmental Psychobiology, 54, 598–611. doi: 10.1002/dev.20531CrossRefGoogle ScholarPubMed
Van Brakel, A. M. L., Muris, P., Bogels, S. M., & Thomassen, C. (2006). A multifactorial model for the etiology of anxiety in non-clinical adolescents: Main and interactive effects of behavioral inhibition, attachment, and parental rearing. Journal of Child and Family Studies, 15, 568–578. doi: 10.1007/s10826-006-9061-xCrossRefGoogle Scholar
Van Rooij, S. J. H., Cross, D., Stevens, J. S., Vance, L. A., Kim, Y. J., Bradley, B., … Jovanovic, T. (2017). Maternal buffering of fear-potentiated startle in children and adolescents with trauma exposure. Social Neuroscience, 12, 22–31. doi: 10.1080/17470919.2016.1164244CrossRefGoogle ScholarPubMed
Vreeke, L. J., Muris, P., Mayer, B., Huijding, J., & Rapee, R. M. (2013). Skittish, shielded, and scared: Relations among behavioral inhibition, overprotective parenting, and anxiety in native and non-native Dutch preschool children. Journal of Anxiety Disorders, 27, 703–710. doi: 10.1016/j.janxdis.2013.09.006CrossRefGoogle ScholarPubMed
Williams, L. R., Degnan, K., Perez-Edgar, K., Henderson, H. A., Rubin, K. H., Pine, D. S., … Fox, N. A. (2009). Impact of behavioral inhibition and parenting style on internalizing and externalizing problems from early childhood through adolescence. Journal of Abnormal Child Psychology, 37, 1063–1075. doi: 10.1007/s10802-009-9331-3CrossRefGoogle ScholarPubMed
You have
Access
As affective scientists, we appreciate the target article's focus on how emotions emerge within early social development and are influenced by aspects of social functioning, including cooperation. The basic premise of the article should be called into question, however, when viewed through the lens of published, empirical evidence that was underemphasized, overlooked, or misinterpreted in the article's discussion of fearfulness in early childhood.
First, there is a robust and growing literature demonstrating that heightened fearfulness in children is not an adaptive trait, and is instead an important predictor of negative behavioral outcomes. The abundance of research on the relation between fearful behavior and mental health problems was greatly minimized in the target article, even though some of it was mentioned (e.g., Fox et al., Reference Fox, Buzzell, Morales, Valadez, Wilson and Henderson2021; Sandstrom, Uher, & Pavlova, Reference Sandstrom, Uher and Pavlova2020). In fact, a large body of research indicates that perceived fearfulness in children is associated with a variety of long-term negative outcomes (e.g., Buss & McDoniel, Reference Buss and McDoniel2016; Coplan, Wilson, Frohlick, & Zelenski, Reference Coplan, Wilson, Frohlick and Zelenski2006; Van Brakel, Muris, Bogels, & Thomassen, Reference Van Brakel, Muris, Bogels and Thomassen2006), contrary to the author's claims regarding the benefits of early fearfulness. It has been known for some time that the extent to which infants and young children demonstrate a fearful temperament (commonly defined as behavioral inhibition, or children's tendency to excessively avoid or withdraw from novel situations) prospectively predicts internalizing behaviors and adverse social and mental health outcomes (e.g., Chronis-Tuscano et al., Reference Chronis-Tuscano, Dengan, Pine, Perez-Edgar, Henderson, Diaz and Fox2009; Williams et al., Reference Williams, Degnan, Perez-Edgar, Henderson, Rubin, Pine and Fox2009). In fact, fearful temperament is the strongest predictor of social anxiety in later childhood, with approximately 40% of behaviorally inhibited children going on to develop anxiety disorders compared to roughly 12% in children with other temperaments (Clauss & Blackford, Reference Clauss and Blackford2012; Fox, Barker, White, Suway, & Pine, Reference Fox, Barker, White, Suway and Pine2013). Importantly, the link between fearful temperament and anxiety disorders has also been documented cross-culturally (Howard, Muris, Loxton, & Wege, Reference Howard, Muris, Loxton and Wege2017; Vreeke, Muris, Mayer, Huijding, & Rapee, Reference Vreeke, Muris, Mayer, Huijding and Rapee2013), suggesting that this relation is unlikely to be the function of an evolutionary mismatch with Western culture as suggested by the author.
Second, research suggests that parents are unlikely to differentiate between negative emotions in their infants, and contrary to the author's claim that parental responses to fear are uniquely beneficial, parents are responsive to the intensity of both positive and negative affective behaviors. Many (if not all) evocative behaviors in infants capture caregiver attention, regardless of valence or perceived emotion category (e.g., Thompson-Booth et al., Reference Thompson-Booth, Viding, Mayes, Rutherford, Hodsoll and McCrory2013). For example, caregivers are highly sensitive to behaviors that suggest positive affect in infants (Kivijarvi et al., Reference Kivijarvi, Voeten, Niemela, Raiha, Lertola and Piha2001). Additionally, caregiver sensitivity to infant distress relies more on integrating information about context and the intensity of infant distress than on making inferences about whether an infant is fearful, sad, angry, and so on (Mesman, Oster, & Camras, Reference Mesman, Oster and Camras2012). This makes sense given evidence that, across both Western and non-Western cultures, infants do not show distinct facial configurations in fear- and anger-eliciting situations (Camras et al., Reference Camras, Oster, Bakeman, Meng, Ujiie and Campos2007) and that caregivers respond similarly to bouts of child distress cross-culturally (Bornstein et al., Reference Bornstein, Tamis-LeMonda, Tal, Ludemann, Toda, Rahn and Vardi1992, Reference Bornstein, Putnick, Rigo, Esposito, Swain, Suwalsky and Venuti2017). More generally, many of the arguments offered in the target article about the adaptiveness of fear in infants and young children would also hold for caregivers' perceptions of other emotions, such as sadness or happiness, or intense affective experiences.
Further, throughout the target article, the description of infant behavior is not clearly distinguished from inferences about its cause. Infant behaviors were frequently described as “fearful” without clearly demonstrating that the situations were reasonably likely to evoke fear. Indeed, instances of a given emotion category are situationally expressed with a variety of facial configurations and behaviors (e.g., in anger, infants and adults furrow their brows in a scowl less than 30% of the time; Barrett, Adolphs, Marsella, Martinez, & Pollak, Reference Barrett, Adolphs, Marsella, Martinez and Pollak2019; Bennett, Bendersky, & Lewis, Reference Bennett, Bendersky and Lewis2002; Sears, Repetti, Reynolds, & Sperling, Reference Sears, Repetti, Reynolds and Sperling2014). Given this situated variation in expressive behaviors, some infant behaviors (such as crying) will be interpreted by adults in more than one way, depending on the context (Chóliz, Fernández-Abascal, & Martínez-Sánchez, Reference Chóliz, Fernández-Abascal and Martínez-Sánchez2013). Scientists must take care to separate their descriptions of physical actions (e.g., facial movements such as widened eyes and gasping mouth) from their inferences about the causes of such actions (such as an inference that the movements are an expression of emotion, or an expression of fear more specifically). Thus, in line with our second point it is more scientifically accurate to conclude that intense or affectively evocative behaviors, rather than fearful behaviors per se, elicit caregiving responses.
Third, parental presence reduces perceived fearfulness early in life at both the behavioral and neural levels; it does not support perceived fearfulness as one would expect if this were, indeed, adaptive. Recent developmental research suggests that a caregiver's presence reduces the development of behaviors commonly associated with perceived fearfulness, such as startle responses (e.g., Van Rooij et al., Reference Van Rooij, Cross, Stevens, Vance, Kim, Bradley and Jovanovic2017). There is also evidence in both human and nonhuman animals that the presence of a caregiver promotes exploration and learning in children, buffering against behaviors that are perceived as fearful (e.g., Callaghan et al., Reference Callaghan, Meyer, Opendak, Van Tieghem, Harmon, Li and Tottenham2019). Although the original article proposes the role of amygdala activity in supporting fearfulness, caregiver presence typically functions to buffer rapid amygdala development and premature amygdala engagement (Tottenham, Reference Tottenham2012). Further, maternal presence allows child amygdala-prefrontal circuitry to function more similarly to adolescent connectivity, thereby allowing for more mature regulatory behavior (Gee et al., Reference Gee, Gabard-Durnam, Telzer, Humphreys, Goff, Shapiro and Tottenham2014). These findings suggest that exploration, and not fearful behavior, is what is most adaptive for infants.
In our view, the target article falls short of demonstrating that heightened fearfulness in infants and young children is evolutionarily adaptive. This hypothesis is called into serious doubt by several hidden inferences that are not supported by existing research, specifically that which demonstrates long-term mental health outcomes of perceived fearfulness as well as parental buffering. Instead, intense affect more generally elicits responses from caregivers. These affective behaviors, and not fearfulness per se, may be what elicits responsive caregiving, ultimately leading to improved functionality within the lifespan of an individual human and improved adaptation of the species.
Financial support
This paper was supported by funding from the National Institutes of Health (F32HD105316 to MO), National Science Foundation (BCS 1947972 to LFB), the National Institute of Mental Health (R21MH129902 to LFB), the US Army Research Institute for the Behavioral and Social Sciences (W911NF-16-1-019 to LFB), the Elizabeth R. Koch Foundation (through its Unlikely Collaborators Fund to LFB), a Marie Skłodowska–Curie Individual Fellowship from the European Commission (892379 to KH) under the European Union's Horizon 2020 research and innovation program, and a James McDonnell Foundation Scholar Award for Understanding Human Cognition (to VL). This paper reflects only the authors' views; the European Commission is not liable for any use that may be made of the contained information. The views, opinions, and/or findings contained in this review are those of the authors and shall not be construed as an official Department of the Army position, policy, or decision, unless so designated by other documents; nor do they necessarily reflect the views of the Elizabeth R. Koch Foundation.
Competing interest
None.