Emergence of stereotypies in juvenile monkeys (Macaca mulatta) with neonatal amygdala or hippocampus lesions.

Bauman, Melissa D.; Toscano, J. E.; Babineau, Brooke A.; Mason, William A.; Amaral, David G.

doi:10.1037/a0012600

Cited by 47 publications

(47 citation statements)

References 57 publications

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“…The HI paradigm has been proven to be a robust task for identifying anxious temperament (Kalin, et al, 2001; Fox, et al, 2008; Oler, et al, 2010; Shackman, et al, 2013), and may be more sensitive for detecting anxiety-like behaviors than social interaction observations or reactions to novel objects used in earlier studies. Contrary to previous studies indicating Neo-Hibo lesions increased motor stereotypies, with no difference in self-directed behaviors (Bauman, et al, 2008), the current study showed the reverse, i.e. no differences in stereotypies, and increased self-directed behaviors (self-grooming and self-clasping) during both infancy and adulthood.…”

Section: Discussioncontrasting

confidence: 99%

Increased anxiety-like behaviors, but blunted cortisol stress response after neonatal hippocampal lesions in monkeys

Raper

Wilson

Sánchez

et al. 2017

Psychoneuroendocrinology

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The hippocampus is most notably known for its role in cognition and spatial memory; however it also plays an essential role in emotional behaviors and neuroendocrine responses. The current study investigated the long-term effects of neonatal hippocampal lesions (Neo-Hibo) on emotional and hypothalamic-pituitary-adrenal (HPA) axis functioning. During infancy, unlike controls, Neo-Hibo monkeys exhibited enhanced expression of emotional behaviors (e.g. freezing, anxiety-like, and self-directed behaviors) when exposed to a human intruder (HI task). Upon reaching adulthood, they exhibited reduced freezing and hostility, but increased anxiety-like and self-directed behaviors during the HI task. Neo-Hibo monkeys behaved as if they systematically over-rated the risk inherent in the HI task, which supports Gray and McNaughton's septo-hippocampal theory of anxiety. Also, in adulthood, the increased levels of anxiety-like behaviors in Neo-Hibo monkeys were associated with a blunted cortisol response to the HI task. Examination of basal HPA axis function revealed that Neo-Hibo monkeys exhibited the typical diurnal cortisol decline throughout the day, but had lower cortisol concentrations in the morning as compared to controls. Taken together these data suggest that an intact hippocampus during development plays a larger role beyond that of inhibitory/negative feedback regulation of the HPA axis stress-activation, and may be critical for HPA axis basal functioning as well as for the stress response. The behavioral and neuroendocrine changes demonstrated in the current study are reminiscent of those seen in human or nonhuman primates with adult-onset hippocampal damage, demonstrating little functional compensation following early hippocampal damage.

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Section: Discussioncontrasting

confidence: 99%

Increased anxiety-like behaviors, but blunted cortisol stress response after neonatal hippocampal lesions in monkeys

Raper

Wilson

Sánchez

et al. 2017

Psychoneuroendocrinology

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“…By 18 months of age, hippocampus-lesioned animals were more active than control subjects. This is consistent with the hypermotoric behavior that we have documented with these animals in social settings (Bauman et al, 2008; Lavenex, et al, 2008) and with evidence from other research groups who have demonstrated hyperactivity in hippocampus-lesioned adult macaques (e.g., Machado & Bachevalier, 2006). …”

Section: Discussionsupporting

confidence: 91%

Neonatal amygdala or hippocampus lesions influence responsiveness to objects

Bliss‐Moreau

Toscano

Bauman

et al. 2010

Developmental Psychobiology

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Medial temporal lobe brain structures, such as the amygdala, play an important role in the normal perception and generation of emotional behavior. Little research, however, has assessed the role of such structures across the neurodevelopmental trajectory. We assessed emotional behavioral responses of rhesus macaques that received bilateral ibotenic acid lesions of the amygdala or hippocampus at two weeks of age and sham-operated controls. At 9 and 18 months of age, animals interacted with novel objects that varied in visual complexity as a means of varying emotional salience. All animals behaved differently in the presence of visually simple, as compared to complex, objects, suggesting that they were sensitive to variation in emotional salience. Across both experiments, amygdala-lesioned animals appeared to be less behaviorally inhibited insofar as they explored all objects most readily. Interestingly, hippocampus-lesioned animals’ propensity for exploration mirrored that of control animals in some contexts but amygdala-lesioned animals in other contexts. At 18 months of age, both amygdala-lesioned and hippocampus-lesioned animals were judged to be less fearful than controls during the testing procedure. Implications for understanding the neurobiology of emotional behavior are discussed.

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“…Raw data are presented here for the purposes of interpretation; log transformed data are available upon request. For the sake of analytic continuity with previous reports on these subjects (Bauman et al, 2004a; Bauman et al, 2008) and in order to establish an understanding of the developmental trajectory of specific behaviors, ANOVAs were conducted on individual behaviors. In some cases, the omnibus test did not reach conventional levels of significances, but visual inspection of each group’s marginal means suggested that there were significant differences between two of the three groups.…”

Section: Methodsmentioning

confidence: 99%

“…The role of the amygdala in normal social and affective development, however, has received less attention as only a few laboratories have undertaken developmental studies following early amygdala damage (e.g., Thompson, Schwartzbaum, & Harlow, 1969; Thompson & Towfighi, 1976; Thompson, Bergland, & Towfighi, 1977, Beauregard, Malkova, & Bachevalier, 1995; Bachevalier, Alvarado, & Malkova, 1999; Bachevalier & Beauregard, 1999; Goursaud & Bachevalier, 2007; Goursaud, Wallen, & Bachevalier, 2014; Raper, Stephens, Sanchez, Bachevalier, & Wallen, 2014; Stephens, Raper, Bachevalier, Wallen, 2014; Bauman, Lavenex, Mason, Capitanio, & Amaral, 2004a; Bauman, Lavenex, Mason, Capitanio, & Amaral, 2004b; Bauman, Toscano, Mason, Lavenex, & Amaral, 2006; Bauman, Toscano, Babineau, Mason, & Amaral, 2008; Bliss-Moreau, Toscano, Bauman, Mason, & Amaral, 2010; Bliss-Moreau, Toscano, Bauman, Mason, & Amaral, 2011; Bliss-Moreau, Bauman, & Amaral, 2011; Bliss-Moreau, Moadab, Bauman, & Amaral, 2013). As part of an ongoing study, we evaluated social behavior at a critical developmental time point—the transition to adulthood—in a cohort of female rhesus macaques who received neonatal damage to the amygdala.…”

mentioning

confidence: 99%

“…Subjects in the current study received bilateral, neurotoxic lesions of the amygdala or hippocampus or control operations at two weeks of age and subsequently participated in several years of affective processing and social behavior testing while being socially housed in various configurations (Bauman et al, 2004a; Bauman et al, 2004b; Bauman et al, 2006; Bauman et al, 2008; Bliss-Moreau et al, 2010; Bliss-Moreau, Toscano et al, 2011; Bliss-Moreau, Bauman et al, 2011; Bliss-Moreau et al, 2013; Moadab et al, 2015). Animals with early amygdala damage from this cohort, in contrast to their hippocampus-lesioned and neurologically intact peers, demonstrated consistent blunting of affective responsivity to novel and threatening objects (Bliss-Moreau et al, 2010; Bliss-Moreau, Toscano et al, 2011).…”

mentioning

confidence: 99%

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Early amygdala or hippocampus damage influences adolescent female social behavior during group formation.

Moadab¹,

Bliss‐Moreau²,

Bauman³

et al. 2017

Behavioral Neuroscience

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This study continues a longitudinal analysis of rhesus macaque social behavior following bilateral neonatal ibotenic acid lesions of the amygdala or hippocampus, or sham operations. The social behavior of female subjects was evaluated at a critical developmental time point—the transition to adulthood. At approximately 4 years of age, female subjects were housed in small groups with other female subjects and reproductively viable adult males. As compared to neurologically intact control animals and animals with early amygdala damage, animals with early hippocampal damage were more social with their female peers. In contrast, as compared to control animals, animals with early amygdala damage spent less time with the males, engaged less frequently in behaviors typical of reproductive consortships, had higher frequencies of self-directed stereotypies, and became pregnant later. Males also generated fewer communicative signals towards animals with early amygdala damage than to control animals and animals with early hippocampus damage. Rates of sexual behavior were generally low for all animals and there were no lesion-based differences in their frequencies. Discriminant function analyses demonstrated that patterns of affiliative social behaviors differed across the three experimental groups, both in terms of the social behaviors directed to the males, and the social behaviors generated by the males towards the females. In four of the five social groups, amygdala-lesioned animals were lowest ranked, potentially contributing to reduced sociability interactions with males. Other potential mechanisms and the experiments needed to elucidate them are discussed.

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Emergence of stereotypies in juvenile monkeys (Macaca mulatta) with neonatal amygdala or hippocampus lesions.

Cited by 47 publications

References 57 publications

Increased anxiety-like behaviors, but blunted cortisol stress response after neonatal hippocampal lesions in monkeys

Increased anxiety-like behaviors, but blunted cortisol stress response after neonatal hippocampal lesions in monkeys

Neonatal amygdala or hippocampus lesions influence responsiveness to objects

Early amygdala or hippocampus damage influences adolescent female social behavior during group formation.

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