Can I see it in the eyes? An investigation of freezing-like motion patterns in response to avoidable threat

Freezing is one of the most extensively studied defensive behaviors in rodents. Both reduced body and gaze movements during anticipation of threat also occur in humans and have been discussed as translational indicators of freezing but their relationship remains unclear. We thus set out to elucidate body and eye movements and concomitant autonomic dynamics in anticipation of avoidable threat. Specifically, 50 participants viewed naturalistic pictures that were preceded by a colored fixation cross, signaling them whether to expect an inevitable (shock), no (safety), or a potential shock (flight) that could be avoided by a quick button press. Body sway, eye movements, the heart rate and skin conductance were recorded. We replicated previously described reductions in body sway, gaze dispersion, and the heart rate, and a skin conductance increase in flight trials. Stronger reductions in gaze but not in body sway predicted faster motor reactions on a trial-wise basis, highlighting their functional role in action preparation. We failed to find a trait-like relationship between body and gaze movements across participants, but their temporal profiles were positively related within individuals, suggesting that both metrics partly reflect the same construct. However, future research is desirable to assess these response patterns in naturalistic environments. A more ethological examination of different movement dynamics upon threat would not only warrant better comparability between rodent and human research but also help determine whether and how eye-tracking could be implemented as a proxy for fear-related movements in restricted brain imaging environments. Our article unravels the relationship between body and eye movements in human threat anticipation, drawing parallels with freezing behavior in rodents. We reveal a physio-behavioral defensive state, emphasize eye-tracking's potential in neuroimaging, and spotlight the need for improved translational research practices across species.