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MECHANISMS REGULATING
AUDITORY COMMUNICATION IN PRIMATES
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John D. Newman, PhD, Head, Unit on Developmental Neuroethology Joseph Soltis, PhD, Postdoctoral Fellow |
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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 is devoted to investigating the changes in vocal behavior that are associated with maturation and social experience under normative conditions as well as the neural systems implicated in such behavior so that we can define their roles in mediating auditory communication. Vocal development is a dynamic process, and a pattern shared by several nonhuman primates has emerged regarding the nature of this process. Infants are highly vocal during periods of brief separation from their caregiver, and we take advantage of this behavior to document the range of vocalizations produced by infants of different ages. The role of individual experience during development is currently under investigation along with that of putative neural substrates to determine the mechanisms leading to the acquisition of adult vocal skills. Acoustic dimensions underlying species-specific vocal communication Newman, Soltis, Bernhards, Sander Adult squirrel monkeys make characteristic cry-like sounds when separated from their social group as well as upon hearing other individuals making the same sounds. Two species of squirrel monkey in our colony make cry sounds that are species-specific in their acoustic details, and some evidence from preliminary studies along with a published study using phonotaxic responses to infant cries suggests that each species preferentially responds to its own species' cries over those of the other species. The present study used responsive calling as an index of selectivity to digital samples of the cries of adults of both species. Animals were tested in their social groups, as were individual vocalizers' responses to each playback stimulus identified by human observers familiar to the subjects. Stimuli were cries of both species randomly ordered in groups of 16 trials per day. Subjects were tested in outdoor enclosures, where they would occasionally hear (and respond to) the cry sounds of other squirrel monkey groups at our facility. Stimuli were presented during silent periods of at least two minutes. Two groups of one of the two species have been tested to date. Individuals of these groups responded to cry stimuli from their own and the other species, invalidating the hypothesis that each species would only respond to its own species' cries. Two groups of the second species will be tested. Soltis J, Bernhards D, Donkin H, Newman JD. The squirrel monkey chuck call: vocal response to playback chucks based on acoustic structure and affiliative relationship with the caller. Am J Primatol 2002;57:119-130. Soltis J, Wegner FH, Newman JD. Adult cortisol response to immature offspring play in captive squirrel monkeys. Physiol Behav; in press. Neuroethology of crying Newman, Boyd, Bernhards, Sander The primate isolation call is functionally and acoustically homologous with the cry sounds of human infants. Like human infants, nonhuman primate infants emit continuous cry sounds when separated from their caregiver and social group. Given the difficulty of conducting invasive experimental neurological procedures in infants, little is known about the neural substrates underlying crying. However, the activation of the c-fos gene has been shown in a variety of behavioral contexts to identify brain areas involved in production of the behavior under study. The peptide product of c-fos activation, Fos, can be detected by immunocytological methods. Hence, the present study aims to identify Fos-labelled neurons following terminal experiments in which the animal is separated, allowed to make cry sounds for 20 to 60 minutes, and euthanized; we then process the brain for Fos immunocytochemistry. To date, we have studied infant common marmosets one to five months of age and have found label in areas expected to be involved in vocal production (hypothalamus, central gray of the midbrain) as well as in areas not thought to be involved in vocal production. In addition, a structure known to be involved in making the adult form of the species-typical cry sounds, the anterior cingulate gyrus, has shown little sign of Fos labeling. Most of the animals used so far have been suboptimal due to their weak crying (a result of poor health or other factors), and further work will use infant marmosets with more robust crying behavior and a broader age range. Newman JD. Auditory communication and central auditory mechanisms in the squirrel monkey: past and present. In: Ghazanfar A, ed. Primate Audition: Ethology and Neurobiology. Boca Raton: CRC Press LLC, 2003;227-246. Newman JD. The primate isolation call: a comparison with precocial birds and nonprimate mammals. In: Rogers L, Kaplan G, eds. Are Primates Special? Dordrecht, Netherlands: Kluwer Academic Publishers; in press. Newman JD. Vocal communication and the triune brain. Physiol Behav 2003;79:495-502. Maternal recognition of own infant's cries Newman; in collaboration with Kose, Lorberbaum In earlier work on this project using fMRI methods and human infant cries as acoustic stimuli, functional scans of mothers revealed several brain areas activated by the cries but less so or not at all by artificial noises. In the present study, we recruited a new sample of mothers and recorded the mothers' own infant cries for use in the fMRI scans. Infants six to eight weeks postpartum were exposed to a paradigm previously used to elicit cries only in neonates. The infant was undressed and placed on a cool surface two hours after feeding. Cries were induced in 33 to 34 infants within five minutes of the start of the procedure. Mothers (along with some fathers) were later asked to distinguish a digital recording of their own infant's cry sounds from the cry sounds of a healthy eight-week-old female infant used as a "standard" cry. All parents correctly identified their own infant's cry sounds. Parents also rated the cry from their own infant more like the cry sounds they heard at home than the cry of the unfamiliar infant. Parent subjects are now undergoing fMRI scans by using the same pair of acoustic stimuli (own infant's cry and standard cry) to examine whether new brain areas are activated beyond those activated in our earlier work using only standard cry stimuli.
Cohen-Manseld J, Werner P, Hammerschmidt K, Newman JD. Acoustic properties of vocally disruptive behaviors in the nursing home. Gerontology 2003;49:161-167. 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 Michelle Becker, PhD, Laboratory of Clinical Studies, NIAAA, Bethesda MD Samet Kose, MD, Medical University of South Carolina, Charleston SC Jeffrey Lorberbaum, MD, Medical University of South Carolina, Charleston SC
For further information, contact jdnewman@helix.nih.gov |
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