Pavlovian threat learning shapes the kinematics of action

Abstract

Prompt response to environmental threats is critical to survival. Previous research has revealed mechanisms underlying threat-conditioned physiological responses, but little is known about how threats shape action. Here we tested if threat learning shapes the kinematics of reaching in human adults. In two different experiments conducted on independent samples of participants, after Pavlovian threat learning, in which a stimulus anticipated the delivery of an aversive shock, whereas another did not, the peak velocity and acceleration of reaching increased for the shocked-paired stimulus, relative to the unpaired one. These kinematic changes appeared as a direct consequence of learning, emerging even in absence of an actual threat to body integrity, as no shock occurred during reaching. Additionally, they correlated with the strength of sympathetic response during threat learning, establishing a direct relationship between previous learning and subsequent changes in action. The increase in velocity and acceleration of action following threat learning may be adaptive to facilitate the implementation of defensive responses. Enhanced action invigoration may be maladaptive, however, when defensive responses are inappropriately enacted in safe contexts, as exemplified in a number of anxiety-related disorders.

Theta and alpha power track the acquisition and reversal of threat predictions and correlate with skin conductance response

“…Such results may suggest a direct relationship between response of the central and peripheral nervous systems during threat learning, with both the alpha and theta rhythms being correlated with the peripheral expression of threat learning, possibly to ensure the timely preparation of responses to the upcoming danger. Indeed, an increase in skin conductance has been reported immediately before the initiation of responses in an active avoidance task (Löw et al, 2015), and more broadly, activation of the sympathetic nervous system facilitates action and is characteristic of active defense behaviors (Cannon, 1939; Critchley, 2002; Hamm, 2020; Starita et al, 2022).…”

“…The US consisted of a 2 ms aversive electrical shock (Effting & Kindt, 2007; Krypotos et al, 2014, 2015; Starita et al, 2022; Stemerding et al, 2022) generated by a Digitimer Stimulator (Model DS7A, Digitimer Ltd., UK) and delivered to the participants' right wrist through pre‐gelled Ag/AgCl snapped electrodes (Friendship Medical, SEAg‐S‐15000/15 × 20). The US intensity ( M = 43.47 mA, SD = 22.41 mA) was calibrated for each participant to a level deemed “highly unpleasant, but not painful” using an ascending staircase procedure (Lonsdorf et al, 2017; Starita et al, 2016, 2022; Starita, Kroes, et al, 2019). Participants rated the unpleasantness of the shock on a scale ranging from 0 (no sensation) to 10 (painful).…”

“…The US consisted of a 2 ms aversive electrical shock (Effting & Kindt, 2007;Krypotos et al, 2014Krypotos et al, , 2015Starita et al, 2022;Stemerding et al, 2022) for each participant to a level deemed "highly unpleasant, but not painful" using an ascending staircase procedure (Lonsdorf et al, 2017;Starita et al, 2016Starita et al, , 2022Starita, Kroes, et al, 2019). Participants rated the unpleasantness of the shock on a scale ranging from 0 (no sensation) to 10 (painful).…”

“…During reversal, the contingencies were reversed, such that hiragana A was now the new CS− (old CS+) and hiragana B the new CS+ (old CS−). Hiragana assignment to each CS role was counterbalanced between participants.The US consisted of a 2 ms aversive electrical shock(Effting & Kindt, 2007;Krypotos et al, 2014Krypotos et al, , 2015Starita et al, 2022;Stemerding et al, 2022) generated by a Digitimer Stimulator (Model DS7A, Digitimer Ltd., UK) and delivered to the participants' right wrist through pre-gelled Ag/AgCl snapped electrodes (Friendship Medical, SEAg-S-15000/15 × 20). The US intensity (M = 43.47 mA, SD = 22.41 mA) was calibrated…”

Editorial: The neurobiological and cognitive underpinnings of appetitive and aversive motivation

“…These processes are central to survival and wellbeing: They help organisms anticipate, adapt, and react to changes in their internal states and in their environment by eliciting multifarious affective responses and appetitive or defensive behaviors (Berridge, 2018 ; Levy and Schiller, 2021 ; Stussi and Pool, 2022 ). For instance, organisms are typically motivated by the opportunity of obtaining rewards and avoiding punishments or threats, which in turn facilitates the execution of approach and avoidance behaviors, respectively (Guitart-Masip et al, 2014 ; Starita et al, 2022 ). Whereas, these forms of appetitive and aversive motivation are generally highly adaptive and contribute to healthy functioning, they can sometimes go awry and become maladaptive.…”