How Do Expectant Fathers Respond to Infant Cry?

Examining Brain and Behavioral Responses and the Moderating Role of Testosterone

Hannah Khoddam; Diane Goldenberg; Sarah A. Stoycos; Katelyn Taline Horton; Narcis Marshall; Sofia I. Cárdenas; Jonas Kaplan; Darby Saxbe

Disclosures

Soc Cogn Affect Neurosci. 2020;15(4):437-446. 

In This Article

Abstract and Introduction

Abstract

Expectant parents' responses to infant cry may indicate future risk and resiliency in the parent-child relationship. Most studies of parental reactivity to infant cry have focused on mothers, and few studies have focused on expectant fathers, although fathers make important contributions to parenting. Additionally, although different responses to infant cry (behavioral, psychological and neural) are hypothesized to track together, few studies have analyzed them concurrently. The current investigation aimed to address these gaps by characterizing multimodal responses to infant cry within expectant fathers and testing whether prenatal testosterone moderates these responses. Expectant fathers responded to infant cry vs frequency-matched white noise with increased activation in bilateral areas of the temporal lobe involved in processing speech sounds and social and emotional stimuli. Handgrip force, which has been used to measure parents' reactivity to cry sounds in previous studies, did not differentiate cry from white noise within this sample. Expectant fathers with higher prenatal testosterone showed greater activation in the supramarginal gyrus, left occipital lobe and precuneus cortex to cry sounds. Expectant fathers appear to interpret and process infant cry as a meaningful speech sound and social cue, and testosterone may play a role in expectant fathers' response to infant cry.

Introduction

An infant's survival depends on the caregiving relationship. Caregivers who respond sensitively to their infant's needs can facilitate their child's healthy development (Ainsworth, 1979; Malmberg et al., 2016). An infant's primary form of communication, crying, may arouse the parent to respond and attend to an infant's distress (Brosch et al., 2007). Researchers have studied endocrine, behavioral and, more recently, neural responses to infant cry, finding that hormone levels, handgrip strength and patterns of brain activation may vary while listening to infant cries (Fleming et al., 2002; Crouch et al., 2008; Kim et al., 2010). Previous studies have suggested that calm parental responses to cry may be linked with approach-oriented, sensitive responses to infants (e.g. Joosen et al., 2013), whereas irritated or hyperreactive responses may be linked with risk for aggression or neglect (Reijman et al., 2014; Zeifman and St James-Roberts, 2017).

Despite these intriguing findings, the literature on reactivity to infant cry has several notable gaps. Surprisingly, given that fathers often participate in infant caregiving, few studies have investigated responses to infant cry sounds in fathers and even fewer have included expectant fathers (Thijssen et al., 2018; Alyousefi-Van Dijk et al., 2019). Interventions have targeted parents' possible responses to infant cry as a marker of aggressive responses to a crying infant (Barr et al., 2009; Coster, 2017). However, it is imperative to thoroughly study expectant fathers' responses to infant cry in order to best tailor these interventions specifically before the baby even arrives. Men's hormones prior to the birth of their child (e.g. their testosterone levels during their partner's pregnancy) may also reflect their preparation for parenting (Saxbe et al., 2017a) and also warrant examination in conjunction with expectant fathers' responses to infant cry. Lastly, although responses across different measurement domains, such as brain and behavioral responses, are assumed to relate to one another (Messina et al., 2016), few studies have measured multiple responses to cry sounds within the same population and analyzed them concurrently (e.g. Riem et al., 2012). Understanding how behavior works in tandem with the brain will help to clarify an overarching theory of the biological response to infant cry and identify where this system may go awry in aggressive or abusive parenting responses.

The current investigation aims to address these gaps by characterizing behavioral, psychological and neural responses to infant cry compared to frequency-matched white noise within expectant fathers and by testing whether paternal prenatal testosterone, a hormone that may reflect paternal investment, affects reactivity to infant cry.

Neural Responses to Infant Cry

Studies of parental brain responses to infant cry have focused primarily on mothers, with few studies on fathers and even fewer investigating expectant fathers (for review see Lynch, 2003; Rilling and Young, 2014; Feldman, 2015; Abraham and Feldman, 2018; Thijssen et al., 2018; Witteman et al., 2019). These studies have investigated how parents respond to own infant cry vs unfamiliar infant cry or an unfamiliar infant cry compared to a control sound. Infant cry sounds, in comparison to video or picture stimuli of infants, have been linked with amygdala activation in mothers, but not fathers or non-parents (Feldman, 2015). Recruitment of the amygdala may underscore parental vigilance to infant distress cues (Abraham et al., 2014). Studies have found that mothers listening to an unknown infant compared to a frequency-matched white noise show activation in components of the midbrain dopamine system (i.e. substantia nigra and ventral tegmental area), anterior and posterior cingulate cortex, right fronto-insular cortex, dorsomedial pre-frontal cortex (dMPFC) (regions involved with emotional and cognitive empathy) and right lateralized auditory cortices extending to the temporal pole (Lorberbaum et al., 1998). A study of neural reactivity in first-time fathers listening to unknown infant cry compared to a white noise control found bilateral activations in the medial pre-frontal cortex, bilateral anterior insula and inferior frontal gyrus (IFG), bilateral striatum, bilateral thalamus, bilateral auditory cortex (including the planum temporale, Heschl's gyrus and supramarginal gyrus) bilateral posterior cingulate and bilateral midbrain structures (Li et al., 2018). No differences were found between own infant cry and unfamiliar infant cry in these first-time fathers. Similarly, a study of the effects of vasopressin on processing infant cry sounds in expectant fathers found that infant crying (vs control sounds) was associated with increased activation in the bilateral auditory cortex and posterior medial cortex (Thijssen et al., 2018). First-time fathers, similarly to first-time mothers, appear to engage five neural systems while listening to unknown infant cries: (i) auditory cortex (auditory perception), (ii) dMPFC (perspective-taking, theory of mind), (iii) fronto-insular cortex (emotional empathy), (iv) thalamocingulate circuits (parental caregiving) and (v) midbrain dopaminergic regions (approach motivation) (Feldman, 2015). A recent meta-analysis similarly confirmed involvement of the cingulate, the auditory system, the pre-supplementary motor area, the dorsal anterior insula, the dMPFC and the IFG in infant cry perception as well as larger activations in the right IFG, temporal pole and left angular gyrus in men in response to infant cry compared to women (Witteman et al., 2019).

Handgrip Modulation Response to Infant Cry

Modulation of handgrip force is interpreted as a behavioral indicator of motivation to respond to the distressed infant (Crouch et al., 2008; Riem et al., 2012; Zeifman and St James-Roberts, 2017). The ability to modulate handgrip force is measured by a dynamometer, which tracks grip strength while an individual listens to an infant crying. Studies have suggested that excessive handgrip force, referred to as 'poor modulation', may indicate risk for abuse or aggressive responding toward an infant (Bakermans-Kranenburg et al., 2012). Poorly modulated handgrip response to infant cry has been linked with neglectful and physically abusive mothers (Compier-de Block et al., 2015) and with parents at risk for child physical abuse (Crouch et al., 2008). Other studies suggest that poor modulation of handgrip may be an indicator of motivation to act or help while an infant is crying (Parsons et al., 2013). One study of expectant fathers failed to find a difference in handgrip modulation between infant cry and frequency-matched white noise control sounds (Alyousefi-Van Dijk et al., 2019). However, this study involved vasopressin administration and viewing pictures of infant faces while listening to infant cry. Earlier studies of infant cry and handgrip force also rarely utilized control sound stimuli, making it difficult to assess whether poor modulation is tied specifically to infant cry or more broadly to any distressing sound. The current study builds on previous studies in examining the response to infant cry in expectant fathers while also using a control condition of frequency-matched white noise.

Psychological Response to Infant Cry

In addition to neural and behavioral responses to infant cry, researchers have investigated individual differences in parents' self-reported interpretations of infant cry. Interpretations of a crying infant as intentionally hostile or reporting increased frustration and negative emotion while listening to infant cry have been associated with risk for aggressive or harsh parenting behaviors (Crouch et al., 2008; Rodriguez et al., 2015). However, the question of whether these interpretations are associated with neural or behavioral responses to cry sounds is underexplored. Parents who rate infant cry sounds as more hostile may show more excessive handgrip force while listening to infant cry (Crouch et al., 2008). Similarly, one study found that fathers who rated infant cry as more aversive exhibited greater neural activation in auditory cortices (Li et al., 2018). Li and authors interpreted this greater neural activation as reflecting a form of negative emotional overarousal in response to infant cry sounds. However, another study found no relationship between mothers' irritation with infant cry sounds and their neural responses to the same sounds (Riem et al., 2012). In sum, this literature is small and inconclusive and has generally not included expectant fathers.

The Role of Testosterone

Many recent studies have investigated the neuroendocrine underpinnings of parenting (Bos et al., 2010; Bos, 2017). Testosterone appears to decline across the transition to parenthood in men and may be associated with paternal sensitivity and involvement in childcare (Gettler et al., 2011; Storey and Ziegler, 2016; Saxbe et al., 2017b). Infant cry can elicit sensitive caregiving (Murray, 1985) or frustration and annoyance (Frodi, 1985; Barr et al., 2006; Del Vecchio et al., 2009). Some parents may be physiologically overly responsive to noxious child stimuli, such as infant cry (Knutson, 1978). This hyperreactivity can lead to an increase in 'irritable aggression,' which may reflect heightened parenting stress and compromised parent-child bonding.

Higher levels of T around the transition to parenthood may indicate the potential for harsh or insensitive parenting, particularly when coupled with this hyperreactivity to infant cry. The role of testosterone in modulating paternal responses to infant cry, however, has received little attention, with most studies focusing on T reactivity to infant stimuli rather than baseline levels of T across the transition to parenthood. One of the only studies to investigate baseline levels of T in first-time fathers (post-partum) failed to find a relationship between baseline T levels and neural activation differences in response to infant cry vs frequency-matched white noise (Li et al., 2018). In studies investigating T reactivity to infant cry, it has been found that men with higher T reactivity (non-fathers and new fathers) in response to unfamiliar infant cries show less sympathy for these infant cries (Fleming et al., 2002). Another study of reactivity to infant cry video stimuli found greater activation in the left caudate in fathers whose testosterone increased more after interacting with their child (Kuo et al., 2012). These authors suggest that increased testosterone and greater neural activation may indicate the body readying itself to protect the baby as signaled by the urgent cries (Kuo et al., 2012). Additionally, another study found that infant cries from a baby doll decreased T levels when the father was allowed to care for the infant but increased T levels when the father was blocked from nurturing the infant (Van Anders et al., 2012), while another found lower T after interacting with an infant in fathers with low cortisol levels (Bos et al., 2018). Therefore, context may be important for understanding the relationship between T and infant cry reactivity in fathers, and increased T levels (both baseline and reactivity) may indicate a physiological hyperreactivity to infant cry and be associated with other potential hyperactive responses to infant cry such as neural activity and handgrip modulation. Notably, testosterone level appears to be positively associated with handgrip strength in men (Gallup et al., 2010), but the relationship between testosterone and handgrip modulation has not been thoroughly tested in the context of infant cry. Few studies have investigated testosterone levels in expectant fathers before the birth of their child (prenatal T) and its potential role in reactivity to infant cry.

Current Study

Although neural, behavioral and psychological responses to infant cry have been examined separately in previous studies, multi-modal approaches are needed to characterize how and whether these responses are correlated across domains. Moreover, understanding how expectant fathers respond to infant cry, and the role of testosterone in shaping these responses, might elucidate how fathers transition to parenthood and prepare to care for their infants.

Within a sample of fathers expecting their first child, we tested four hypotheses:

  1. In response to infant cry sounds (vs white noise), we expected that expectant fathers would show greater neural activation in regions that have been associated with infant cry specifically (e.g. socio-cognitive areas such as the STG, insula, mPFC, dlPFC, auditory cortices and IFG). We planned to use whole-brain analyses to test this hypothesis and to supplement these analyses with an a priori ROI focused on the amygdala.

  2. We also expected fathers to show behavioral responses to infant cry sounds, specifically poor handgrip modulation when listening to infant cry sounds compared with white noise sounds.

  3. We expected that fathers' responses to infant cry would be consistent across neural, behavioral and self-report modalities. Specifically, given evidence that fathers who rated infant cry more negatively also showed heightened neural activation to cry (Li et al., 2018), we expected that fathers who showed greater neural activation to infant cry in hypothesized brain areas would also show poorer handgrip modulation, greater interpretation of the infant as more negative during infant cry and greater self-reported negative emotions after infant cry compared to white noise.

  4. Given that prenatal testosterone may reflect paternal investment in sensitive parenting, which requires the ability to modulate negative responses to aversive stimuli such as infant cry, we hypothesized that fathers with higher prenatal testosterone levels would show more reactivity to infant cry, including more negative ratings of the infant, more negative emotions after listening to infant cry, poorer handgrip modulation and more activation in hypothesized brain areas in response to infant cry.

Comments

3090D553-9492-4563-8681-AD288FA52ACE

processing....