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MECHANISMS REGULATING
AUDITORY COMMUNICATION IN PRIMATES

 

John D. Newman, PhD, Head, Unit on Developmental Neuroethology

Michelle Becker, PhD, Postdoctoral Fellow

Deborah Bernhards, BS, Biological Technician

Maria Rakhovskaya, BA, BS, Technical Training Fellow

 

Understanding the mechanisms underlying the expression and perception of auditory communication in nonhuman primates provides important insights into the neural systems that mediate nonverbal auditory communication in humans. Our research focuses on the changes in vocal behavior that are associated with maturation and social experience as well as on the neural systems implicated in these developmental changes. Infants are highly vocal during brief periods of separation from their caregiver, and we take advantage of this behavior to collect and analyze temporal and acoustic patterns at different ages and under different social environments. We identify and study in detail the neural substrates that mediate vocal production in order to understand the genetic and experiential influences that guide the neural circuitry underlying such behavior. Crying is a compelling stimulus to caregivers, and we study the acoustic attributes that promote positive caregiver responses to crying infants. Of particular interest is the nature of the mechanisms underlying cry perception, which we study by using a variety of methodologies.

Functional imaging of brain areas responsive to infant cries in humans

Following two earlier studies with fewer subjects and an unfamiliar cry as the stimulus, the present study involved 40 mothers and a cry sequence from their own infant, recorded in the home when the infant was five to eight weeks of age. We computed differences between brain oxygen level changes in reaction to own infant or unfamiliar infant and mapped them onto MRI scans from each subject. Areas with increased activity in response to own infant included the medial preoptic area, midbrain, thalamus, ventral striatum, septum, amygdala, cingulate cortex, mesial prefrontal area, insula, and temporal pole. Subsequently, we recruited 10 fathers of the same set of infants for the fMRI study. In striking contrast to the mothers, fathers showed very limited differential brain activation to the cry stimuli, mainly in neocortex and cerebellum (also activated in the mothers). The results suggest that fathers and mothers use different brain circuitry in processing infant cry sounds.

Newman JD. Infant cry and colic: what lies beneath. Behav Brain Sci, in press.

Vocal responses to isolation calls in squirrel monkeys

Squirrel monkeys are highly social and exhibit a rich vocal repertoire; their brains have undergone extensive study in the context of brain-behavior relationships. The species is of additional interest in the context of our research in that the monkeys continue to make vocalizations acoustically and functionally similar to their infant cries (“isolation calls”) into adulthood. In this study, we examined vocal responses of listeners hearing the cries of distant animals. We tested groups of two species for possible differential responses to calls from their own species. We observed no significant differences in response to a stimulus call from the same or another species. The results confirm our anecdotal observations and suggest that squirrel monkeys may exhibit a type of altruistic or empathic vocal behavior.

Newman, JD. Motherese by any other name: mother-infant communication in non-hominin mammals. Behav Brain Sci, in press.

Newman, JD. The primate isolation call: a comparison with precocial birds and nonprimate mammals. In: Rogers L, Kaplan G, eds. Comparative Vertebrate Cognition: Are Primates Superior to Non-Primates? Dordrecht, Netherlands: Kluwer Academic Publishers, 2004;171-187.

Newman, JD. Vocal communication and the triune brain. Physiol Behav 2003;79:495-502.

Immunocytochemical studies of primate brains

Studies of the distribution of the protein products of gene expression have not been extensively reported in primates, particularly in the species that we study. We are therefore conducting two studies in this area. In the first, we are studying the distribution of Fos (c-fos gene product) in squirrel monkeys and marmosets after separating the individual for 20 minutes to encourage production of isolation calls. To date, we have processed and examined brain sections from six adult squirrel monkeys and eight adult marmosets. Results from the most robust vocalizers of both species show extensive label (marking the presence of Fos) in the anterior cingulate gyrus, preoptic area, hypothalamus, and periaqueductal gray of the midbrain, regions all implicated in vocal production in other studies. In addition, we found label in auditory cortex (activated as a result of auditory feedback from the vocalizing animal) and parts of the hippocampus. In the second study, we are examining the distribution of three calcium-binding proteins, calbindin, calretinin, and parvalbumin, with results pending.

Lorberbaum JP, Newman JD, Horwitz AR, Dubno JR, Lydiard RB, Hamner MB, Bohning DE, George MS. A potential role for thalamocingulate circuitry in human maternal behavior. Biol Psychiatry 2002;51:431-445.

COLLABORATORS

Samet Kose, MD, Medical University of South Carolina, Charleston, SC

Jeffrey Lorberbaum, MD, Medical University of South Carolina, Charleston, SC

Joseph Soltis, PhD, Disney’s Animal Kingdom, Lake Buena Vista, FL

For further information, contact newmanj@mail.nih.gov