Visuocortical changes during a freezing-like state in humans
Maria Lojowska, Sam Ling, Karin Roelofs, Erno Hermans
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, suggest 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 that is regulated by a common mechanism involving the amygdala.