Visuocortical changes during a freezing-like state in humans

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.