Cross-species convergence in pupillary response: understanding human anxiety via non-human primate amygdala lesion

David Pagliaccio, Daniel S. Pine, Ellen Leibenluft, Olga Dal Monte, Bruno B. Averbeck, Vincent Costa

Research output: Contribution to journalArticle

Abstract

Few studies have used matched affective paradigms to compare humans and non-human primates. In monkeys with amygdala lesions and youth with anxiety disorders, we examined cross-species pupillary responses during a saccade-based, affective attentional capture task. Given evidence of enhanced amygdala function in anxiety, we hypothesized that opposite patterns would emerge in lesioned monkeys and anxious participants. A total of 53 unmedicated youths (27 anxious, 26 healthy) and 8 adult male rhesus monkeys (Macaca mulatta) completed matched behavioral paradigms. Four monkeys received bilateral excitotoxic amygdala lesions and four served as unoperated controls. Compared to healthy youth, anxious youth exhibited increased pupillary constriction in response to emotional and non-emotional distractors (F(1,48) = 6.28, P = 0.02, η2p = 0.12). Pupillary response was associated significantly with anxiety symptoms severity (F(1,48) = 5.59, P = 0.02, η2p = 0.10). As hypothesized, lesioned monkeys exhibited the opposite pattern i.e. decreased pupillary constriction in response to distractors, compared to unoperated control monkeys (F(1,32) = 24.22, P < 0.001, η2 = 0.33). Amygdala lesioned monkeys and youth with anxiety disorders show opposite patterns of pupil constriction in the context of an affective distractor task. Such findings suggest the presence of altered amygdala circuitry functioning in anxiety. Future lesion and human neuroimaging work might examine the way in which specific amygdala sub-nuclei and downstream circuits mediate these effects.

Original languageEnglish (US)
Pages (from-to)591-599
Number of pages9
JournalSocial cognitive and affective neuroscience
Volume14
Issue number6
DOIs
StatePublished - Aug 7 2019

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Amygdala
Primates
Haplorhini
Anxiety
Constriction
Anxiety Disorders
Macaca mulatta
Saccades
Pupil
Neuroimaging

Keywords

  • amygdala
  • anxiety
  • attention
  • emotion
  • pupillometry
  • rhesus

ASJC Scopus subject areas

  • Experimental and Cognitive Psychology
  • Cognitive Neuroscience

Cite this

Cross-species convergence in pupillary response : understanding human anxiety via non-human primate amygdala lesion. / Pagliaccio, David; Pine, Daniel S.; Leibenluft, Ellen; Monte, Olga Dal; Averbeck, Bruno B.; Costa, Vincent.

In: Social cognitive and affective neuroscience, Vol. 14, No. 6, 07.08.2019, p. 591-599.

Research output: Contribution to journalArticle

Pagliaccio, David ; Pine, Daniel S. ; Leibenluft, Ellen ; Monte, Olga Dal ; Averbeck, Bruno B. ; Costa, Vincent. / Cross-species convergence in pupillary response : understanding human anxiety via non-human primate amygdala lesion. In: Social cognitive and affective neuroscience. 2019 ; Vol. 14, No. 6. pp. 591-599.
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