The Basolateral Amygdala Is Essential for Rapid Escape: A Human and Rodent Study

David Terburg, Diego Scheggia, Rodrigo Triana Del Rio, Floris Klumpers, Alexandru Cristian Ciobanu, Barak Morgan, Estrella R Montoya, Peter A Bos, Gion Giobellina, Erwin H van den Burg, Beatrice de Gelder, Dan J Stein, Ron Stoop, Jack van Honk

Research output: Contribution to journalArticleAcademicpeer-review

Abstract

Rodent research delineates how the basolateral amygdala (BLA) and central amygdala (CeA) control defensive behaviors, but translation of these findings to humans is needed. Here, we compare humans with natural-selective bilateral BLA lesions to rats with a chemogenetically silenced BLA. We find, across species, an essential role for the BLA in the selection of active escape over passive freezing during exposure to imminent yet escapable threat (Timm). In response to Timm, BLA-damaged humans showed increased startle potentiation and BLA-silenced rats demonstrated increased startle potentiation, freezing, and reduced escape behavior as compared to controls. Neuroimaging in humans suggested that the BLA reduces passive defensive responses by inhibiting the brainstem via the CeA. Indeed, Timm conditioning potentiated BLA projections onto an inhibitory CeA pathway, and pharmacological activation of this pathway rescued deficient Timm responses in BLA-silenced rats. Our data reveal how the BLA, via the CeA, adaptively regulates escape behavior from imminent threat and that this mechanism is evolutionary conserved across rodents and humans.

Original languageEnglish
Article numbere16
Pages (from-to)723-735
Number of pages29
JournalCell
Volume175
Issue number3
DOIs
Publication statusPublished - 18 Oct 2018

Keywords

  • CONDITIONED FEAR
  • THREAT
  • CIRCUIT
  • MAPS
  • ACTIVATIONS
  • AVOIDANCE
  • PATHWAYS
  • BEHAVIOR
  • ANXIETY
  • SYSTEM

Cite this

Terburg, D., Scheggia, D., Triana Del Rio, R., Klumpers, F., Ciobanu, A. C., Morgan, B., Montoya, E. R., Bos, P. A., Giobellina, G., van den Burg, E. H., de Gelder, B., Stein, D. J., Stoop, R., & van Honk, J. (2018). The Basolateral Amygdala Is Essential for Rapid Escape: A Human and Rodent Study. Cell, 175(3), 723-735. [e16]. https://doi.org/10.1016/j.cell.2018.09.028