Publications (9)47.6 Total impact
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Article: Effect of Mother's Dominance Rank on Offspring Temperament in Infant Rhesus Monkeys (Macaca mulatta).
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ABSTRACT: In humans, temperament plays an important role in socialization and personality. Some temperaments, such as behavioral inhibition are associated with an increased risk for psychopathology. Nonhuman primates can serve as a model for neurobiological and developmental contributions to emotional development and several recent studies have begun to investigate temperament in nonhuman primates. In rhesus monkeys, dominance rank is inherited from the mother and is associated with social and emotional tendencies that resemble differences in temperament. The current study assessed differences in temperament in infant rhesus monkeys as a function of maternal dominance rank. Temperament was assessed in 26 infants (13 males) from birth until 6 months of age with a battery that included Brazelton test, human intruder test, human intruder-startle, cortisol stress reactivity, and home cage observations of interactions with peers and the mother. Throughout testing, infants lived with their mothers and a small group of other monkeys in indoor/outdoor runs. Dominance rank of the mothers within each run was rated as either low/middle (N = 18, 9 male) or high/alpha (N = 8, 4 female). Infants of high-ranking mothers displayed more intruder-directed aggression and reduced startle potentiation in the human intruder tests. Dominant offspring also had reduced levels cortisol and startle across development and spent more time away from mothers in the interaction tests. These results suggest that dominance of the mother may be reflected in behavioral reactivity of infants early in life. These findings set up future studies, which may focus on contributing factors to both dominance and temperament such as genetics, rearing, and socialization. Such factors are likely to interact across development in meaningful ways. These results also suggest future human-based studies of a similar relationship may be warranted, although social dominance is clearly more complex in human than macaque societies. Am. J. Primatol. 00:1-9, 2012. Published 2012 by Wiley Periodicals, Inc.†American Journal of Primatology 10/2012; · 2.22 Impact Factor -
Article: Amygdala volume predicts patterns of eye fixation in rhesus monkeys.
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ABSTRACT: In both human and nonhuman primates the eyes are a highly salient feature of the face, conveying identity, emotion and attentional direction of conspecifics. Studies have indicated that the amygdala plays an important role in eye contact, and amygdala dysfunction may underlie social deficits in disorders such as autism through effects on eye contact. In the present study we compared the volume of the amygdala in 32 juvenile rhesus monkeys to visual fixation patterns in a social memory paradigm. Amygdala volume was determined from manual traces of structural MRIs and fixation patterns were assessed using eyetracking methodology. A significant positive relationship was found between amygdala volume and fixation on both the face and the eye region. Amygdala volume was also found to relate to habituation across multiple presentations of different photographs of the same individual monkeys indicating a role in social memory. These data provide an important linkage between structural variation of amygdala and previous demonstrations of function in a nonhuman primate model.Behavioural brain research 04/2012; 229(2):433-7. · 3.22 Impact Factor -
Article: Developmental changes of rhesus monkeys in response to separation from the mother.
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ABSTRACT: The development of separation response behaviors in infant rhesus macaques across the first 6 months of life was assessed. Seventeen infants underwent a neonatal assessment at 7, 14, 21, and 30 days of age which included a brief period of social isolation. At 3 and 6 months of age these same monkeys and four additional subjects were again subjected to a period of brief social isolation and also exposed to a novel environment with their sedated mother. Results indicate a developmental increase followed by a steady decline in the frequency of separation vocalizations. A modest relationship between early-infancy locomotor profiles and separation responses was also observed at several time points suggesting a possible relationship between these measures. However, stable inter-individual measures of separation distress did not emerge until late in the infantile period. This could suggest that high levels of maternal contact-seeking behavior early in infancy are context specific and not a reliable index of enduring temperament. © 2011 Wiley Periodicals, Inc. Dev Psychobiol.Developmental Psychobiology 12/2011; · 2.98 Impact Factor -
Article: Developmental patterns of doublecortin expression and white matter neuron density in the postnatal primate prefrontal cortex and schizophrenia.
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ABSTRACT: Postnatal neurogenesis occurs in the subventricular zone and dentate gyrus, and evidence suggests that new neurons may be present in additional regions of the mature primate brain, including the prefrontal cortex (PFC). Addition of new neurons to the PFC implies local generation of neurons or migration from areas such as the subventricular zone. We examined the putative contribution of new, migrating neurons to postnatal cortical development by determining the density of neurons in white matter subjacent to the cortex and measuring expression of doublecortin (DCX), a microtubule-associated protein involved in neuronal migration, in humans and rhesus macaques. We found a striking decline in DCX expression (human and macaque) and density of white matter neurons (humans) during infancy, consistent with the arrival of new neurons in the early postnatal cortex. Considering the expansion of the brain during this time, the decline in white matter neuron density does not necessarily indicate reduced total numbers of white matter neurons in early postnatal life. Furthermore, numerous cells in the white matter and deep grey matter were positive for the migration-associated glycoprotein polysialiated-neuronal cell adhesion molecule and GAD65/67, suggesting that immature migrating neurons in the adult may be GABAergic. We also examined DCX mRNA in the PFC of adult schizophrenia patients (n = 37) and matched controls (n = 37) and did not find any difference in DCX mRNA expression. However, we report a negative correlation between DCX mRNA expression and white matter neuron density in adult schizophrenia patients, in contrast to a positive correlation in human development where DCX mRNA and white matter neuron density are higher earlier in life. Accumulation of neurons in the white matter in schizophrenia would be congruent with a negative correlation between DCX mRNA and white matter neuron density and support the hypothesis of a migration deficit in schizophrenia.PLoS ONE 01/2011; 6(9):e25194. · 4.09 Impact Factor -
Article: The effect of gonadectomy on prepulse inhibition and fear-potentiated startle in adolescent rhesus macaques.
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ABSTRACT: Sex steroids, such as testosterone, can regulate brain development, cognition and modify psychiatric conditions. However, the role of adolescent testosterone in the emergence of cognitive deficits relevant to psychiatric illness has not been directly studied in primates. We examined whether removing testosterone during adolescence in rhesus macaques would affect prepulse inhibition (PPI) and fear-potentiated startle (FPS), which are translational tests of cognition affected in psychiatric disorders. Prepubertal macaques (30 months old) were castrated (n=6) or sham operated (n=6), and PPI and (FPS) were tested before the onset of puberty (34 months old) and after the pubertal surge in sex hormones 16 months later (50 months old). As expected there were no differences between the gonadectomized and intact groups' level of startle amplitude, PPI or (FPS) before puberty. After puberty, the intact group displayed substantially less PPI than the gonadectomized group, consistent with evidence that PPI is attenuated by endogenous increases in sex hormones. At the end of the study, testosterone among the intact monkeys was also correlated with tyrosine hydroxylase levels in the putamen, suggesting the attenuation of PPI by gonadal sex hormones may be influenced by subcortical dopamine. Thus, puberty involves significant increases in sex hormones, which in turn may modulate subcortical dopamine synthesis and affect cognitive functions impaired in psychiatric illnesses such as schizophrenia.Psychoneuroendocrinology 07/2010; 35(6):896-905. · 5.81 Impact Factor -
Article: Adverse rearing experiences enhance responding to both aversive and rewarding stimuli in juvenile rhesus monkeys.
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ABSTRACT: While adverse rearing is thought to alter threat responding, the effects on appetitive behavior remains minimally explored. This study examines the effects that early life emotional adversity has on response to both threatening and appetitive stimuli in juvenile rhesus monkeys. Twenty-four, 2-year-old monkeys with differential rearing histories were tested for fear-potentiated startle responding and consumption of an artificially sweetened solution. Relative to monkeys reared under typical conditions, monkeys removed from their mothers at birth and reared with peers demonstrated both increases in reward responding, as evidenced by greater consumption of a palatable solution in a free choice test, and increased threat responding, as evidenced by enhanced fear-potentiated startle responding. Findings suggest that early rearing impacts juvenile manifestations of both appetitive and aversive emotional systems. Results are discussed in the context of development, anxiety, depression, and substance abuse.Biological psychiatry 06/2009; 66(7):702-4. · 8.93 Impact Factor -
Article: AX+/BX- discrimination learning in the fear-potentiated startle paradigm in monkeys.
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ABSTRACT: Individuals with anxiety disorders often do not respond to safety signals and hence continue to be afraid and anxious. Consequently, it is important to develop paradigms in animals that can directly study brain systems involved in learning about, and responding to, safety signals. We previously developed a discrimination procedure in rats of the form AX+/BX-, where cues A and X presented together are paired with an aversive stimulus and cues B and X presented together predict the absence of an aversive stimulus. The present experiment adapted this procedure to the fear-potentiated startle paradigm in rhesus monkeys.Learning & memory (Cold Spring Harbor, N.Y.) 03/2008; 15(2):63-6. · 4.08 Impact Factor -
Article: Modulation of fear-potentiated startle and vocalizations in juvenile rhesus monkeys by morphine, diazepam, and buspirone.
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ABSTRACT: Modulation of the acoustic startle response by aversive sensory stimulation is a simple and objective indicator of emotionality in rodents and human beings that has been extremely valuable for the analysis of neural systems associated with fear and anxiety. We have described a paradigm for measuring fear-potentiated, whole-body acoustic startle in nonhuman primates and have developed a protocol for maintaining fear-potentiated startle over repeated sessions with minimal extinction to allow measurement of pharmacological effects on fear-potentiated startle by using within-subjects designs in relatively small groups of monkeys. A novel, within-subjects testing protocol was used to examine the effects of three compounds in rhesus monkeys that have anxiolytic effects in rodents on fear-potentiated startle but that differ in their mechanism of action. Spontaneous vocalizations during testing also were recorded. Juvenile monkeys that were trained to associate a visual stimulus with a fear-inducing air blast to the face were tested after acute administration of different doses of buspirone diazepam, morphine, or vehicle. Monkeys rapidly developed a robust and persistent elevation of startle response in the presence of the CS during repeated testing sessions. Diazepam and morphine produced dose-related reductions of fear-potentiated startle. Buspirone did not significantly reduce fear-potentiated startle at the doses tested, although a trend was evident at the highest dose. All drugs reduced rates of coo vocalizations during startle testing. These fear-potentiated startle results suggest that rhesus monkeys have a pharmacological profile with respect to these compounds that is closer to humans than to rats. This demonstrates the value of examining the effects of drugs on fear-potentiated startle in nonhuman primates.Biological Psychiatry 03/2007; 61(3):389-95. · 8.28 Impact Factor -
Article: Rearing effects on cerebrospinal fluid oxytocin concentration and social buffering in rhesus monkeys.
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ABSTRACT: Mother-reared (MR) and nursery-reared (NR) male rhesus monkeys exhibit profound and persistent differences in social and emotional behavior. Compared to MR animals, NR monkeys show reduced reciprocal social behaviors and increased agonistic behavior and high levels of stereotypy. Cerebrospinal fluid oxytocin (CSF OT) in NR monkeys was significantly reduced compared to MR monkeys measured at 18, 24, and 36 months of age. Correlations between OT and individual social behavioral profiles measured across rearing conditions also revealed a significant association between OT and the expression of affiliative social behaviors including allogrooming and reciprocal intermale mounting at each age examined. In contrast, CSF vasopressin levels did not differ according to rearing history, but did correlate with fearful behaviors independent of rearing history. Differential rearing was not associated with differences in basal or stress-related plasma cortisol, although these levels did progressively decline as monkeys matured. MR but not NR monkeys were able to use a social companion to buffer their response to a stressor, but OT levels did not appear to be sensitive to the presence of a social companion in either group. These results are consistent with earlier reports from studies of rodents suggesting an important role for central OT pathways in the development of social affiliation.Neuropsychopharmacology 06/2003; 28(5):910-8. · 7.99 Impact Factor
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Institutions
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2011–2012
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National Institute of Mental Health (NIMH)
Bethesda, MD, USA
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