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

Discussion

This study sought to characterize neural, behavioral and psychological responses to infant cry sounds among expectant fathers and to examine whether their testosterone levels were associated with these responses to cry sounds. Our hypotheses were partially supported. As expected, infant cry (vs white noise sounds) elicited activation in regions including the superior temporal gyrus, IFG and insula, although we did not find expected differences in amygdala activation. Additionally, parts of the auditory cortices such as the planum temporale, Heschl's gyrus and supramarginal gyrus were additionally found to be more active during infant cry than a frequency-matched white noise, similarly to previous studies of first-time fathers and expectant fathers (Li et al., 2018; Thijssen et al., 2018). The planum temporale is situated posterior to the primary auditory cortex and has been found to be active during the processing of speech-related cues (Baars and Gage, 2010), locating sound in space (Hickok, 2009) and stimulus selection and auditory attention (Hirnstein et al., 2013). The supramarginal gyrus has been implicated in phonological processing (e.g. Saur et al., 2008; Church et al., 2011) and in social cognition (Silani et al., 2013; Singer and Klimecki, 2014). Our sample of expectant fathers appeared to recognize infant cry sounds as a meaningful speech signal over and above a frequency-matched white noise.

Additionally, areas of the brain associated with social cognition (i.e. insula, supramarginal gyrus) appear to be more active during cry than white noise. Previous research has suggested that, in contrast to biological mothers, who form a physical bond with the infant prior to birth, the paternal brain primarily comes 'online' after the birth of a child and in interacting with their newborn (Abraham et al., 2014). However, the current research suggests that infant cry is nevertheless a salient stimulus for expectant fathers, even though they have not yet participated in caregiving for their own infants. Fine-tuning of these processes may occur with socialization with the infant as has been previously hypothesized (Atzil et al., 2012; Abraham et al., 2014; Feldman, 2015). However, the current study suggests that expectant fathers show processing of infant cry that is similar to mothers and to fathers whose child is already born. Future studies would benefit from including expectant fathers at different stages of pregnancy or age-matched non-fathers to understand whether similar brain responses emerge in non-parents and if not, when and how these brain responses come 'online' during pregnancy.

Although we did not find a main effect for amygdala activation in response to infant cry vs white noise, we did find that fathers' negative views of infant cry predicted greater right amygdala activation during infant cry compared to white noise. This finding contradicts a previous study that found no relationship between amygdala activation and mothers' reported irritation during infant cry (Riem et al., 2012), suggesting that this finding may be specific to expectant fathers. However, this result should be interpreted with caution given that it did not reach the level of significance after controlling for multiple comparisons. Amygdala activation has been found to be greater during infant cry compared to other forms of infant stimuli (such as laughter), and activation in these areas has been purported to underlie parental vigilance to infant distress cues (Abraham et al., 2014). Amygdala activation may also represent the hub of the emotion-processing sub-network of the parenting brain (Feldman, 2015; Abraham and Feldman, 2018).

Counter to hypotheses, no difference in handgrip modulation was found during infant cry compared to frequency-matched white noise. Several reasons may explain these null results. Firstly, although handgrip has been used to reflect potential aggression in response to infant cry in previous studies (Crouch et al., 2008), these studies did not include a control sound comparison. Similar null results were found in another population of expectant fathers (Alyousefi-Van Dijk et al., 2019) when comparing handgrip during infant cry and a frequency-matched white noise. These results together suggest that handgrip modulation may not be a specific response to infant cry per se but may reflect hyperarousal to aversive stimuli in general. Our null results may also be due to limitations of the handgrip task itself or an underpowered sample size. It was challenging for participants to master the half-strength grip procedure, and many subjects became frustrated during the training. It may be that this task is not reliable enough across participants to indicate a sensitive response to infant cry.

The relationship between psychological and neural response to infant cry was additionally only partially supported in the current investigation, unlike previous studies which found a relationship between neural activation in auditory cortices and greater irritation to infant cry in new fathers (Li et al., 2018). However, these results are in line with a previous investigation of mothers which failed to find a relationship between reported aversiveness of infant cry and neural activation to the same sound (Riem et al., 2012). These null results may be due to a small sample size and an underpowered whole-brain analysis. However, the current sample size is in line with the previous investigations (Riem et al., 2012; Li et al., 2018). Additionally, this relationship may be stronger in fathers who could be at risk for aggressive parenting or abuse. The current investigation sought to characterize the neural and psychological response to infant cry in a community sample of expectant fathers and thus may not capture the responses indicative of abusive parenting risk.

Higher prenatal testosterone predicted greater activation in right supramarginal gyrus, left occipital cortex and the precuneus cortex. As stated above, previous studies have found the supramarginal gyrus to be implicated in social cognition (Silani et al., 2013; Singer and Klimecki, 2014) and the precuneus cortex to be associated with arousal and reward learning (Swain, 2011). Previous studies of first-time fathers and baseline T found no neural activation differences in infant cry vs white noise in conjunction with T level (Li et al., 2018). However, T reactivity to infant stimuli has been found to be associated with greater neural activation in the left caudate to infant cry while listening to infant cry and watching infant video stimuli (Kuo et al., 2012). Given that this is the first investigation to look at neural activation to infant cry in expectant fathers and baseline prenatal T levels, this finding may be specific to the prenatal period. Additionally, greater activation to infant cry in association with higher T level may indicate a hyperreactivity to infant cry in line with previous investigations that have found a positive relationship between neural activation and greater reports of irritation to infant cry in new fathers (Li et al., 2018). However, the current investigation did not measure parenting behaviors post-partum in these fathers with higher T. Future studies can investigate whether fathers' prenatal responses to cry sounds predict their actual parenting behaviors following the birth of their child and how this relates to testosterone level across pregnancy.

The current study had a number of limitations. Our sample size was small (34 fathers), albeit larger than the samples used in most published studies of the parenting brain. Moreover, we used a multimodal approach, incorporating behavioral (handgrip), hormonal (testosterone) and self-report data as well as MRI data. Another limitation is that because our sample consisted of expectant fathers, we were not able to present own infant sounds and instead played unfamiliar cry sounds. However, this limitation is balanced by the advantage that the stimuli was standardized across participants and has been used in previous studies even with participants who were already parents. Additionally, testosterone levels and neuroimaging responses were collected on different days and therefore may not fully map onto each other. Finally, these data are cross-sectional, focusing only on expectant fathers. Future studies can extend this work by focusing on prenatal responses to cry as a predictor of later parenting behavior. Given the exploratory nature of this study and the novel population included, future research should endeavor for an increased sample size to replicate and clarify these results.

Despite its important limitations, this study is one of the first to investigate responses to infant cry in expectant fathers across multiple modalities. Our sample was ethnically diverse and contributed hormonal, behavioral, neural and self-report data. Our findings suggest that expectant fathers process infant cry as a salient and meaningful speech sound that may require empathic responding, even before the child is born. Additionally, it appears that testosterone may moderate this effect, with expectant fathers who were higher in testosterone also showing stronger neural responses to infant cry. Given the importance of fathers to healthy child development, this work contributes to our understanding of the fathering brain and can ultimately improve the detection of fathers at risk and inform the development of interventions that target expectant fathers.

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