Freezing of gaze during action preparation under threat imminence

Abstract

When confronted with threatening stimuli, animals typically respond with freezing behavior characterized by reduced movement and heart rate deceleration. Freezing-like responses during threat anticipation have also been observed in humans and are associated with anxiety. Recent evidence yet suggests that freezing does not necessarily reflect helpless immobility but can also aid the preparation of a threat escape. To investigate which further behavioral responses human freezing encompasses, we presented 50 young adults (10 male) with aversive stimuli that could sometimes be avoided while measuring gaze, cardiovascular and electrodermal activity. In trials in which the threat could be escaped, participants displayed reduced heart rate, increased electrodermal activity and reduced visual exploration. Furthermore, heart rate deceleration and restricted visual exploration predicted the speed of flight responses. These results provide evidence for freezing behavior in measures of visual exploration and suggest that such responding is adaptive in preparing the subsequent escape of approaching threats.

Approach-Avoidance Decisions Under Threat: The Role of Autonomic Psychophysiological States

“…Lesioning the CeA, a region critically implicated in the freezing response increased active avoidance in those animals (Choi and Kim, 2010;Lázaro-Muñoz et al, 2010). In contrast, human studies show that freezing facilitates rapid responding (Jennings and van der Molen, 2005;del Paso et al, 2015;Gladwin et al, 2016;Hashemi et al, 2019a,b;Ribeiro and Castelo-Branco, 2019;Rösler and Gamer, 2019) and one study showed that threatanticipatory freezing responses biased subsequent instrumental actions toward faster threat avoidance (Ly et al, 2014). Two recent studies (Hashemi et al, 2019a,b) manipulated threat of shock by using a task in which an avatar would shoot if an incorrect or delayed response was made.…”

“…Evidence for the involvement of freezing in information gathering comes from studies in humans showing that the magnitude of the freezing-related bradycardia is associated with changes in perception. For example, stronger freezing responses have been associated with preferential processing of low over high spatial frequency features of a visual stimulus (Lojowska et al, 2015(Lojowska et al, , 2018 and reduced visual exploration of non-threat-relevant stimulus features (Rösler and Gamer, 2019).…”

“…In the area of perceptual decision making, there is also evidence associating anticipatory bradycardia with faster decision making (Jennings and van der Molen, 2005;del Paso et al, 2015;Ribeiro and Castelo-Branco, 2019). Moreover, threat-anticipatory freezing responses are stronger when active responses are available to mitigate the threat, as compared to when it is not possible to escape the threat (Gladwin et al, 2016;Rösler and Gamer, 2019). To understand the apparent discrepancy between non-human animal and human findings, it is important to note that animal studies index freezing typically as the duration of immobility, while human studies typically index freezing as the magnitude of the freeze response (baseline-to-trough in terms of heart rate and/or immobility).…”

“…Freezing has been observed in both humans and non-human species, frequently in response to more distal threat (Blanchard et al, 2011;. Human studies have shown that the magnitude of the freezing response is associated with altered information processing (Lojowska et al, 2015) and action preparation (Mobbs and Kim, 2015;Gladwin et al, 2016;Hashemi et al, 2019a,b;Rösler and Gamer, 2019). Given the importance of information gathering and action preparation in making adaptive responses in threatening situations, freezing could therefore be more than a passive state to avoid predator detection.…”

Development of a Classical Conditioning Task for Humans Examining Phasic Heart Rate Responses to Signaled Appetitive Stimuli: A Pilot Study

“…Differential effects of US vs. neutral stimuli on heart rate were observed, and the data reflected awareness of the purported CS+ vs. CS-. As the task was simple and no behavioral responses were required, these cardiac responses were likely elicited by these stimuli, unconfounded by task difficulty (Richter, 2010;Fairclough and Ewing, 2017) or action/action preparation (Cooke et al, 2014;Rösler and Gamer, 2019). The data offer new information on adult human responses to appetitive stimuli and cues that predict them.…”