Visuocortical changes during a freezing-like state in humans

Neuroimage. 2018 Oct 1;179:313-325. doi: 10.1016/j.neuroimage.2018.06.013. Epub 2018 Jun 6.

Abstract

An adaptive response to threat requires optimized detection of critical sensory cues. This optimization is thought to be aided by freezing - an evolutionarily preserved defensive state of immobility characterized by parasympathetically mediated fear bradycardia and regulated by the amygdala-periaqueductal grey (PAG) circuit. Behavioral observations in humans and animals have suggested that freezing is also a state of enhanced visual sensitivity, particularly for coarse visual information, but the underlying neural mechanisms remain unclear. We induced a freezing-like state in healthy volunteers using threat of electrical shock and measured threat-related changes in both stimulus-independent (baseline) and stimulus-evoked visuocortical activity to low-vs. high-spatial frequency gratings, using functional MRI. As measuring immobility is not feasible in MRI environments, we used fear bradycardia and amygdala-PAG coupling in inferring a freezing-like state. An independent functional localizer and retinotopic mapping were used to assess the retinotopic specificity of visuocortical modulations. We found a threat-induced increase in baseline (stimulus-independent) visuocortical activity that was retinotopically nonspecific, which was accompanied by increased connectivity with the amygdala. A positive correlation between visuocortical activity and fear bradycardia (while controlling for sympathetic activation), and a concomitant increase in amygdala-PAG connectivity, confirmed the specificity of these findings for the parasympathetically dominated freezing-like state. Visuocortical responses to gratings were retinotopically specific, but did not differ between threat and safe conditions across participants. However, individuals who exhibited better discrimination of low-spatial frequency stimuli showed reduced stimulus-evoked V1 responses under threat. Our findings suggest that a defensive state of freezing involves an integration of preparatory defensive and perceptual changes which may be regulated by a common mechanism involving the amygdala.

Keywords: Fear bradycardia; Freezing; Functional MRI; Spatial frequency; Visual perception.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adult
  • Amygdala / physiology*
  • Brain Mapping / methods
  • Fear / physiology*
  • Female
  • Freezing Reaction, Cataleptic / physiology*
  • Humans
  • Magnetic Resonance Imaging
  • Male
  • Periaqueductal Gray / physiology
  • Visual Cortex / physiology*
  • Young Adult