MECHANISMS REGULATING AUDITORY COMMUNICATION AND SOCIAL BEHAVIOR IN PRIMATES AND OTHER MAMMALS
     
John D. Newman, Ph.D., Head, Unit on Developmental Neuroethology
Joseph Soltis, Ph.D., Postdoctoral Fellow
R. Lucille Roberts, Ph.D., Research Fellow
Deborah Bernhards, B.S., Biological Technician
Kosunique Jenkins, M.S., Technical Training Fellow
John Newman
 

Our principal research goal is to understand the neural and hormonal mechanisms mediating expression of vocalizations and appropriate social responses to such sounds. In addition, we are attempting to understand the role of certain peptide hormones in the brain on the establishment and maintenance of social bonds between adults and between caregivers and their offspring.

Acoustic Dimensions Underlying Nonhuman Primate Conversational Communication
Soltis, Newman, Bernhards
Using standard playback methodology, we completed a new study of vocal communication in adult female squirrel monkeys (Saimiri sciureus). The purpose of the study was to determine which acoustic component of a frequent vocalization, the “chuck,” provided the most salient information regarding individual identity of the vocalizer. For our response mea-sure, we used a chuck “response” by a group member to the playback stimulus within four seconds. We digitized chucks recorded from the test group and then presented them intact, with a frequency-modulated component referred to as the “flag” removed, or with the flag of another individual (from another social group) electronically spliced onto a chuck instead of the naturally occurring flag for that vocalization. The rate of response to intact chucks was significantly higher than to the same chucks with the flag removed or to chucks with unfamiliar flags spliced onto them. The results suggest that the flag is an important acoustic feature used by females to determine whether they vocally respond in this form of conversational communication. To test whether the acoustic information in flags was sufficient to for a statistically separation of vocalizers, we measured and entered into a discriminant analysis several parameters of flags (such as flag duration, peak frequency, and so forth). The results indicated that flag parameters alone were sufficient to separate the chucks of vocalizers in a social group.

Hormonal Correlates of Affiliative Behavior in Nonhuman Primates

Soltis, Newman, Bernhards
In a second project, we are examining the hormonal correlates of affiliative behaviors in squirrel monkeys. Squirrel monkeys engage in three types of affiliation: mothering, allomother-ing by other adult females that extends to nursing and carrying, and same or opposite-sex affiliation among adults or adults and juveniles. Most of the affiliations involve adult females, as adult males are more solitary. We are investigating cortisol, which is implicated in the stress response, and prolactin, which has been implicated in affiliative behavior. We expected prolactin to be associated with allomothering because of its clear role in lactation and speculated that it may be associated with same-sex adult friendships because it has also been implicated in affiliative behaviors that do not involve lactation, such as male parenting behavior in the common marmoset, another neotropical primate. We compared prolactin and cortisol levels in blood and urine samples from the same monkey and noted a positive correlation. However, given that detection of prolactin requires a larger volume of urine than is typically produced in a single void, we collected urine samples from individual monkeys at the same time of day over several days and combined them for analysis. Despite the lack of precise temporal information, the advantage of using a noninvasive method for collecting samples for hormone analysis outweighs the disadvantage.

Based on analysis of data from three social groups, we concluded that urinary prolactin is positively associated with physical contact with infants and with the intensity of caregiving toward infants. Urinary cortisol is positively associated with the level of social disruption brought on by the presence of older infants and juveniles that spend a large portion of their day engaged in social play.

Neuroethology of Infant Crying
Newman, Bernhards
Two new studies initiated this year aim to understand the mechanisms underlying infant crying and the response of potential caregivers to cry sounds. The first study uses immuno-cytochemical techniques to reveal brain sites at which the protein product (Fos) of the immediate-early (IE) gene c-fos is found following a bout of crying in infant rats and infant marmosets. We have refined our technique to a point where we can routinely demonstrate Fos-like activity in the brains of experimental subjects and will further refine the methods to permit us to distinguish between specific and nonspecific activity at brain sites.

Figure 19

Positive correlation between urinary cortisol in adult females and the amount of disruptive playing by juveniles in social groups of captive squirrel monkeys. According to a principal components analysis, individual adults scoring high on this behavioral factor experienced a large number of play attempts by infants and juveniles and showed retaliatory aggression against them; they exhibited low levels of social affiliation with other adults. The relationship between individual factor scores and mean cortisol values is positive, suggesting that such disruption produces measurable physiological stress in the adult monkeys.

Eventually, we intend to use the same technique to identify brain sites where c-fos activity is associated with hearing infant cries. The second study uses playback techniques similar to those used in the “chuck” study (see above) to document response tendencies of adult squirrel monkeys upon hearing isolation calls. Initially, we are measuring the vocal responses of adults to adult isolation calls, but eventually we will measure the responses to infant cries. A major goal of our work is to identify the acoustic parameters in isolation calls (“cries”) that promote vocal and nonvocal responses to these sounds. Data collection is still in progress.

 

PUBLICATIONS

  1. Guard HJ, Newman JD, Roberts, RL. Morphine administration selectively facilitates social play in common marmosets. Dev Psychobiol. 2002;41:37-49.
  2. 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.
  3. 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, FL: CRC Press LLC, 2002;227-246.
  4. 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.

    COLLABORATORS

    Michelle Becker, Ph.D., Laboratory of Clinical Studies, NIAAA, Bethesda, MD
    Jiska Cohen-Mansfield, Ph.D., Research Institute, Hebrew Home of Greater Washington, Rockville, MD
    Jeffrey Lorberbaum, M.D., Medical University of South Carolina, Charleston, SC