Mapping the neural circuitry of predator fear in the nonhuman primate
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ORIGINAL ARTICLE
Mapping the neural circuitry of predator fear in the nonhuman primate Quentin Montardy1 · William C. Kwan2 · Inaki C. Mundinano2 · Dylan M. Fox2 · Liping Wang1 · Cornelius T. Gross3 · James A. Bourne2 Received: 15 May 2020 / Accepted: 9 November 2020 © The Author(s) 2020
Abstract In rodents, innate and learned fear of predators depends on the medial hypothalamic defensive system, a conserved brain network that lies downstream of the amygdala and promotes avoidance via projections to the periaqueductal gray. Whether this network is involved in primate fear remains unknown. To address this, we provoked flight responses to a predator (moving snake) in the marmoset monkey under laboratory conditions. We combined c-Fos immunolabeling and anterograde/retrograde tracing to map the functional connectivity of the ventromedial hypothalamus, a core node in the medial hypothalamic defensive system. Our findings demonstrate that the ventromedial hypothalamus is recruited by predator exposure in primates and that anatomical connectivity of the rodent and primate medial hypothalamic defensive system are highly conserved. Keywords Ventromedial hypothalamus · Instinctive predator fear · Connectivity · Mapping · Marmoset · Nonhuman primate
Introduction Lesions of the amygdala block the processing of learned and innate fear stimuli in multiple species, including humans (LeDoux 2014; Anderson and Adolphs 2014; Feinstein et al. 2011; Feinstein 2013; Martinez et al. 2011). However, fear Electronic supplementary material The online version of this article (https://doi.org/10.1007/s00429-020-02176-6) contains supplementary material, which is available to authorized users. * Cornelius T. Gross [email protected] 1
Shenzhen Key Lab of Neuropsychiatric Modulation and Collaborative Innovation Center for Brain Science, Guangdong Provincial Key Laboratory of Brain Connectome and Behavior, CAS Center for Excellence in Brain Science and Intelligence Technology, Brain Cognition and Brain Disease Institute (BCBDI), Shenzhen Institutes of Advanced Technology, Chinese Academy of Sciences, Shenzhen-Hong Kong Institute of Brain Science-Shenzhen Fundamental Research Institutions, Shenzhen 518055, China
2
Australian Regenerative Medicine Institute, Monash University, Clayton, VIC 3800, Australia
3
Epigenetics and Neurobiology Unit, EMBL Rome, European Molecular Biology Laboratory, Via Ramarini 32, 00015 Monterotondo, RM, Italy
induced by internally generated stimuli, such as the inhalation of carbon dioxide, do not require the amygdala (Feinstein et al. 2011). These observations suggest that circuits downstream of the amygdala are sufficient to sustain the behavioral and emotional correlates of fear. This view is supported by extensive work in rodents demonstrating that a circuit from the amygdala to the medial hypothalamus and brainstem, called the medial hypothalamic defensive system, is both necessary and sufficient for innate and learned defensive responses to predators (Canteras 2002; Gross and Canteras
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