Neonatal amygdala or hippocampus lesions influence responsiveness to objects

Bliss‐Moreau, Eliza; Toscano, J. E.; Bauman, Melissa D.; Mason, William A.; Amaral, David G.

doi:10.1002/dev.20451

Cited by 42 publications

(86 citation statements)

References 23 publications

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“…There was a similar maturational change of hostile behavior expression in Neo-Hibo animals, such that there were no group differences during infancy but decreased hostility in adulthood compared to controls. Reduced freezing and hostility during adulthood is consistent with reports of decreased defensive behaviors in monkeys with adult-onset hippocampal lesions (Machado & Bachevalier, 2008; Chudasama, et al, 2008, 2009) and decreased reactivity toward objects in other Neo-Hibo monkeys (Bliss-Moreau, et al, 2010, 2011a). Taken together, these results suggest that early hippocampal damage alters the typical developmental maturation of defensive behaviors, such that animals exhibit decreased defensive behaviors in adulthood.…”

Section: Discussionsupporting

confidence: 87%

“…Few studies have shown that neonatal hippocampal damage yields abnormal emotional reactivity to objects and social partners (Bauman et al, 2004; Bliss-Moreau et al, 2010, 2011a, 2013), but normal HPA-axis response to pharmacological challenges assessed at 2.5-4.5 months after the lesion (Goursaud et al, 2006). Yet, none of these studies have investigated the impact of early hippocampal damage on both behavioral and physiological (HPA axis) stress reactivity.…”

Section: Introductionmentioning

confidence: 99%

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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: Discussionsupporting

confidence: 87%

Section: Introductionmentioning

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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“…When interacting with novel objects and objects thought to engender threat responding at 18 months of age, amygdala-lesioned animals physically explored objects whereas control animals did not (Bliss-Moreau et al, 2010, Experiment 2), indicating that amygdala-lesioned animals’ affective processing was perturbed in nonsocial contexts. This supports the view that the amygdala is not necessary for social processing per se, but rather serves a broader function related to evaluating threat.…”

Section: Discussionmentioning

confidence: 99%

“…Subject selection and rearing history has been fully described in other publications (Bauman, 2004a, 2004b; Bliss-Moreau et al, 2010; Bliss-Moreau, Toscano, et al, 2011). Briefly, 24 infant rhesus macaque monkeys received bilateral ibotenic acid lesions of either the amygdala (five females, three males) or hippocampus (five females, three males), or sham control operations (four females, four males) at 12-16 days of age.…”

Section: Methodsmentioning

confidence: 99%

“…The extent to which early damage to the amygdala results in alterations in affective and social processing is less clear. The goal of the present paper is to evaluate variation in social processing in juvenile animals that received damage to the amygdala as neonates as part of our ongoing study of variation in affect (Bliss-Moreau, et al, 2010, 2011; Bliss-Moreau, Bauman, & Amaral, 2011) and social behavior (Bauman et al, 2004a, 2004b) following early amygdala damage.…”

Section: Introductionmentioning

confidence: 99%

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The Impact of Early Amygdala Damage on Juvenile Rhesus Macaque Social Behavior

Bliss‐Moreau¹,

Moadab²,

Bauman³

et al. 2013

Journal of Cognitive Neuroscience

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The present experiments continue a longitudinal study of rhesus macaque social behavior following bilateral neonatal ibotenic acid lesions of the amygdala or hippocampus, or sham operations. Juvenile animals (approximately 1.5- 2.5 years of age) were tested in four different social contexts—alone, while interacting with one familiar peer, while interacting with one unfamiliar peer, and in their permanent social groups. During infancy, the amygdala-lesioned animals displayed more interest in conspecifics (indexed by increased affiliative signaling) and paradoxically demonstrated more submission or fear (Bauman, Lavenex, Mason, Capitanio, & Amaral, 2004a, this journal). When these animals were assessed as juveniles, differences were less striking. Amygdala-lesioned animals generated fewer aggressive and affiliative signals (e.g., vocalizations, facial displays) and spent less time in social interactions with familiar peers. When animals were observed alone or with an unfamiliar peer, amygdala-lesioned, compared with other subjects, spent more time being inactive and physically explored the environment less. Despite the subtle, lesion-based differences in the frequency and duration of specific social behaviors, there were lesion-based differences in the organization of behavior such that lesion groups could be identified based on the patterning of social behaviors in a discriminant function analysis. The findings indicate that, although overall frequencies of many of the observed behaviors do not differ between groups, the general patterning of social behavior may distinguish the amygdala-lesioned animals.

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Autism: Animal Models

Bauman¹,

Crawley²,

Berman³

2019

Encyclopedia of Life Sciences

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Autism is a neurodevelopmental disorder characterised by deficits in social interaction, social communication, sensory abnormalities, stereotyped and repetitive behaviours, and restricted interests. Autism spectrum disorder (ASD) has proven difficult to study because of the diversity of its behavioural symptoms, complex genetics and lack of ubiquitous biomarkers. Progress in the development of heuristic animal models has allowed investigators to model some of the core symptoms of autism, including deficits in social interactions, aspects of social communication and stereotyped, repetitive behaviours. Specific hypotheses can now be formulated and tested in mouse, rat and non‐human primate models. Translational applications of animal models have advanced the discovery of therapeutic interventions for treating the core features of ASD. This article describes some of the major behavioural approaches and animal models designed to study neurodevelopmental disorders, with a focus on ASDs. Key Concepts Autism is a complex disorder whose underlying biology is being studied using rodent and non‐human primate animal models. Rodents and non‐human primates are social animals with rich and complex behavioural repertories that make them useful for modelling neurodevelopmental disorders. Many of the behaviours that reflect core deficits in autism, including social communication, social interaction, motor stereotypies and repetitive behaviours, can be modelled in rodents and non‐human primates. Inbred strains of mice can be used to discover genes important for the expression of complex behaviours and can provide insights into the neurobiology of social interactions and social communication. Mice and rats with targeted mutations in risk genes and deletions identified in people with autism provide research tools for investigating mechanistic substrates of the disorder and for discovering therapeutic interventions. Animal models of neurodevelopmental disorders, while important and useful, typically only model specific aspects of a disorder rather that recapitulating its full symptomatology.

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Neonatal amygdala or hippocampus lesions influence responsiveness to objects

Cited by 42 publications

References 23 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

The Impact of Early Amygdala Damage on Juvenile Rhesus Macaque Social Behavior

Autism: Animal Models

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