The Why of the Cry

When you hear a baby relentlessly crying on an airplane, even through your noise-cancelling headphones, you can do nothing but sigh in defeat. With all hope of an in-flight nap destroyed, you might still find solace in the fact that the wailing baby is only performing the most basic function of being a newborn.

In fact, infants of many species cry when under distress, most often when they are uncomfortable, hungry, in pain, or isolated from their mother. Scientists are hesitant to consider non-human vocalizations “cries”, but neuroscience research suggests some commonalities between how and why infants of different species produce vocalizations when they are in distress. Some studies have shown that certain acoustic properties of vocalizations are associated with future diagnosis of developmental and psychiatric disorders (Sheinkopf et al., 2012; Smarius et al., 2017). Studying the neurobiological basis of infant vocalizations may help scientists understand how to identify individuals at risk for developing these disorders in order to better serve them with early and appropriate interventions.

The separation call: infant-mother interactions across species
Most non-human mammals “cry”, or emit distress vocalizations, when they are separated from their mothers, their main source of warmth, nutrition, and comfort. Separation calls are an innate response (Newman, 2004), and some researchers have even compared their reflexive nature to that of a sneeze (Blumberg & Alberts, 1990). Since infants have limited motor, cognitive, and communication skills, they rely on vocalizations to survive. When it comes to protecting their offspring, mothers are particularly vigilant to attending to their calls. Japanese macaques, for example, are better at responding to their own offspring’s calls than to the calls of other infants (Shizawa et al., 2005). Sheep, lambs, and ewes also develop specific vocalization structures that differentiate specific mother/infant pairs from each other (Walser et al., 1982).

Most non-human mammals “cry”, or emit distress vocalizations, when they are separated from their mothers, their main source of warmth, nutrition, and comfort.

Infants of some species modulate their vocalizations to make it easier for their mothers to find them without alerting predators of their location in the process. For example, rats and mice emit high-pitched vocalizations over 20kHz in frequency, which is above the normal hearing ability of their predators, including humans (Branchi et al., 2001). When rodent pups emit ultrasonic vocalizations, their mothers begin to lactate, search for their pups, improve the nest, and engage in high quality maternal care (Brouette-Lahlou et al., 1992; Brunelli et al., 2004; Hashimoto et al., 2001). Establishing these unique communication skills as infants sets the foundation for learning different social and mating calls they will use as adults (Brudzynski et al., 1999).

Different species produce vastly different vocalizations. Despite anatomical variation in the vocal system giving rise to these differences, parallels can be drawn in the underlying neurobiology. For instance, separating an infant from its mother causes the infant’s oxytocin and opioid neurotransmitter levels to decrease while they are vocalizing. When the infant and mother are reunited, vocalizations fade, and oxytocin and opioid levels are restored (Panksepp & Biven, 2012). Hormones and physiology of the caregiver are also affected when they hear infant distress calls (McNeilly et al., 1983). This dual-sided relationship helps support strong attachment between infants and caregivers.

What makes up a cry?
Every sound is defined by its acoustic qualities, which determine how the sound waves will travel from their origin and how it will be perceived by the listener. The most basic features of a sound are its duration, amplitude (loudness), and fundamental frequency (F0). F0 is the pitch of the cry, or how high or low it sounds. More complicated aspects of the sound are described by the phonation and formants. A sound’s phonation changes depending on different vibrations of the vocal folds, while formants can be changed by altering the size and shape of the vocal tract. These changes create subtle differences in sound, like the different vowel sounds of similar words like “hat” and “hot” (Titze et al., 2015).

Analyzing these features may have implications for early identification of infants at risk for developmental disorders, Autism Spectrum Disorder (ASD), and other concerns like mental health disorders and hearing impairment (Esposito et al., 2017). For example, one study found that infants who vocalized excessively were more likely to exhibit generalized anxiety and hyperactivity at age 5-6 (Smarius et al., 2017). On the other hand, infants later diagnosed with ASD made fewer but higher pitched calls than those who were not diagnosed. These children also demonstrated language delays at age 2 (Sheinkopf et al., 2012). Since infant vocalizations lay the groundwork for learning more complicated social communication, observing these differences in infancy may be the key to identifying vulnerable individuals.

Genetics and the environment: lessons from rodents
Genetic and environmental risk factors for developmental disorders can be studied in laboratory rodents by analyzing their distress calls and testing potential interventions that could support healthy development.

Researchers use genetic variants to model developmental disorders in mice (Premoli et al., 2020). They find that altering the expression of genes thought to underlie developmental disorders changes the acoustic properties and vocalization patterns in mouse pups (Penagarikano et al., 2011). Changing how these pups emit distress calls could directly influence the quality of maternal care they receive and have downstream effects on future social interactions. This altered mother-pup relationship and later peer relationships could, in turn, affect the development of emotional regulation and cognitive skills. Studying these variations in rodents helps researchers understand how early communication via distress calls reflects neural development, which programs behavior throughout life.

Changing how these pups emit distress calls could directly influence the quality of maternal care they receive and have downstream effects on future social interactions.

Some investigators have also explored how vocalizations of rodent pups change after disrupting their neonatal environment. Since adverse experiences in childhood can have long-lasting effects, studying the basis of these changes in rodent models is of utmost importance. Pup distress calls can be used as a proxy for determining typical versus atypical development in various contexts. For example, when pups are raised in impoverished cage conditions, or repeatedly isolated for extended periods of time, they make fewer vocalizations at critical periods, and the types of vocalizations they emit are not appropriate for their age (Granata et al., 2021). Sensory interventions, such as exposing pups to a faux “mother” and heartbeat in their cage when subjected to stress, can prevent some of the vocal disruptions caused by adverse environments (Kentner et al., 2018).

Scientists once believed that infant vocalizations only relied on the brainstem, which regulates automatic functions like breathing and balance (Newman et al., 2007). However, regions involved in emotional regulation and fear, like the amygdala, can also affect how rat pups make distress calls (Muller et al., 2010). Understanding how infant vocalizations are related to these other brain areas underlying emotional behavior, many of which are implicated in psychiatric disorders, will help make connections between early and later life behaviors.

Conclusions
Changes in communication and social interaction are core indicators of several disorders, including developmental disorders like ASD and mental health disorders like anxiety, post-traumatic stress disorder, and schizophrenia. Identifying signs of these disorders as early as possible is essential to preventing long-term, debilitating mental health concerns. As such, psychological research has investigated vocalization patterns in infants as a behavioral readout that may be related to later diagnosis. The similarities between infant vocalizations across several species show that these mechanisms are highly evolutionarily conserved. Thus, researchers can use rodent models to understand how these disorders manifest and test interventions that could eventually be used to improve outcomes in humans. A baby’s cry is more than initially meets the ear; it could be one of the earliest clues into how the human brain is developing.

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Written by Lauren Granata
Edited by Abinaya Muthusamy and Caitlin Goodpaster
Illustrated by Sumana Shrestha

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References
Blumberg, Mark S., and Greta Sokoloff. “Do Infant Rats Cry?” Psychological Review 108, no. 1 (20010124): 83. https://doi.org/10.1037/0033-295X.108.1.83.

Branchi, Igor, Daniela Santucci, and Enrico Alleva. “Ultrasonic Vocalisation Emitted by Infant Rodents: A Tool for Assessment of Neurobehavioural Development.” Behavioural Brain Research 125, no. 1–2 (November 2001): 49–56. https://doi.org/10.1016/S0166-4328(01)00277-7.

Brouette-Lahlou, I., E. Vernet-Maury, and M. Vigouroux. “Role of Pups’ Ultrasonic Calls in a Particular Maternal Behavior in Wistar Rat: Pups’ Anogenital Licking.” Behavioural Brain Research 50, no. 1–2 (September 28, 1992): 147–54. https://doi.org/10.1016/s0166-4328(05)80296-7.

Brudzynski, Pricilla Kehoe, and Megan Callahan. “Sonographic Structure of Isolation-Induced Ultrasonic Calls of Rat Pups.” Developmental Psychobiology 34, no. 3 (April 13, 1999): 10.

Brunelli, Susan A., and Myron A. Hofer. “Selective Breeding for Infant Rat Separation-Induced Ultrasonic Vocalizations: Developmental Precursors of Passive and Active Coping Styles.” Behavioural Brain Research 182, no. 2 (September 4, 2007): 193–207. https://doi.org/10.1016/j.bbr.2007.04.014.

Granata, Lauren, Alissa Valentine, Jason L. Hirsch, Jennifer Honeycutt, and Heather Brenhouse. “Trajectories of Mother-Infant Communication: An Experiential Measure of the Impacts of Early Life Adversity.” Frontiers in Human Neuroscience 15 (2021). https://doi.org/10.3389/fnhum.2021.632702.

Hashimoto, Haruo, Naoki Moritani, Shinobu Aoki-Komori, Minoru Tanaka, and Toru R. Saito. “Comparison of Ultrasonic Vocalizations Emitted by Rodent Pups.” Experimental Animals 53, no. 5 (October 2004): 409–16. https://doi.org/10.1538/expanim.53.409.

Kentner, Amanda C., Stephanie Scalia, Junyoung Shin, Mattia M. Migliore, and Alejandro N. Rondón-Ortiz. “Targeted Sensory Enrichment Interventions Protect against Behavioral and Neuroendocrine Consequences of Early Life Stress.” Psychoneuroendocrinology 98 (December 1, 2018): 74–85. https://doi.org/10.1016/j.psyneuen.2018.07.029.

McNeilly, A. S., I. C. Robinson, M. J. Houston, and P. W. Howie. “Release of Oxytocin and Prolactin in Response to Suckling.” Br Med J (Clin Res Ed) 286, no. 6361 (January 22, 1983): 257–59. https://doi.org/10.1136/bmj.286.6361.257.

Muller, Jeff, Susan Brunelli, and Harry Shair. “Rat Infant Isolation Vocalizations and Their Modulation by Social Cues as a Model of Expression of Infantile Emotionality.” In Handbook of Behavioral Neuroscience, 19:227–40. Elsevier, 2010. https://doi.org/10.1016/B978-0-12-374593-4.00023-1.

Newman, John D. “The Primate Isolation Call: A Comparison with Precocial Birds and Non-Primate Mammals.” In Comparative Vertebrate Cognition: Are Primates Superior to Non-Primates?, edited by Lesley J. Rogers and Gisela Kaplan, 171–87. Developments in Primatology: Progress and Prospects. Boston, MA: Springer US, 2004. https://doi.org/10.1007/978-1-4419-8913-0_5.

Newman, John D. “Neural Circuits Underlying Crying and Cry Responding in Mammals.” Behavioural Brain Research182, no. 2 (September 2007): 155–65. https://doi.org/10.1016/j.bbr.2007.02.011.

Panksepp, Jaak, Eric Nelson, and Marni Bekkedal. “Brain Systems for the Mediation of Social Separation-Distress and Social-Reward Evolutionary Antecedents and Neuropeptide Intermediaries.” Annals of the New York Academy of Sciences807, no. 1 Integrative N (January 1997): 78–100. https://doi.org/10.1111/j.1749-6632.1997.tb51914.x.

Peñagarikano, Olga, Brett S. Abrahams, Edward I. Herman, Kellen D. Winden, Amos Gdalyahu, Hongmei Dong, Lisa I. Sonnenblick, et al. “Absence of CNTNAP2 Leads to Epilepsy, Neuronal Migration Abnormalities, and Core Autism-Related Deficits.” Cell 147, no. 1 (September 30, 2011): 235–46. https://doi.org/10.1016/j.cell.2011.08.040.

Premoli, Marika, Maurizio Memo, and Sara Anna Bonini. “Ultrasonic Vocalizations in Mice: Relevance for Ethologic and Neurodevelopmental Disorders Studies.” Neural Regeneration Research 16, no. 6 (June 2021): 1158–67. https://doi.org/10.4103/1673-5374.300340.

Sheinkopf, Stephen J., Jana M. Iverson, Melissa L. Rinaldi, and Barry M. Lester. “Atypical Cry Acoustics in 6-Month-Old Infants at Risk for Autism Spectrum Disorder.” Autism Research: Official Journal of the International Society for Autism Research 5, no. 5 (October 2012): 331–39. https://doi.org/10.1002/aur.1244.

Shizawa, Y., M. Nakamichi, T. Hinobayashi, and T. Minami. “Playback Experiment to Test Maternal Responses of Japanese Macaques (Macaca Fuscata) to Their Own Infant’s Call When the Infants Were Four to Six Months Old.” Behavioural Processes 68, no. 1 (January 31, 2005): 41–46. https://doi.org/10.1016/j.beproc.2004.10.002.

Smarius, Laetitia Joanna Clara Antonia, Thea G. A. Strieder, Eva M. Loomans, Theo A. H. Doreleijers, Tanja G. M. Vrijkotte, Reinoud J. Gemke, and Manon van Eijsden. “Excessive Infant Crying Doubles the Risk of Mood and Behavioral Problems at Age 5: Evidence for Mediation by Maternal Characteristics.” European Child & Adolescent Psychiatry 26, no. 3 (March 2017): 293–302. https://doi.org/10.1007/s00787-016-0888-4.

Titze, Ingo R., Ronald J. Baken, Kenneth W. Bozeman, Svante Granqvist, Nathalie Henrich, Christian T. Herbst, David M. Howard, et al. “Toward a Consensus on Symbolic Notation of Harmonics, Resonances, and Formants in Vocalization.” The Journal of the Acoustical Society of America 137, no. 5 (May 2015): 3005–7. https://doi.org/10.1121/1.4919349.

Walser, Elizabeth, Eurof Walters, and Peter Hague. “Vocal Communication between Ewes and Their Own and Alien Lambs.” Behaviour 81, no. 2–4 (1982): 140–51. https://doi.org/10.1163/156853982X00120.

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