Overgeneralization of autonomic defensive reactions in obesity

Abstract

Generalizing defensive responses to new stimuli resembling learned threats is an adaptive process within an ever-changing environment. However, evaluation mechanisms excessively biased toward generalization (i.e., overgeneralization) may underlie anxiety-related symptoms. In the context of obesity, fear memory and fear generalization processes have never been investigated. In this study, participants with obesity and healthy participants as controls underwent a single-cue auditory fear conditioning paradigm and recognition memory tasks. We analyzed the autonomic reactions evoked by threat-predictive and new stimuli, as well as the recognition performance towards the same cues. We found that participants with obesity displayed similar autonomic defensive responses to a learned fearful stimulus, but enhanced reactions to new stimuli, when compared with the controls. We detected no significant differences between groups in recognition abilities. Our results provided the first evidence that obesity may widen fear generalization patterns. This alteration may encourage future research in investigating the link between emotional dysregulation and clinical anxiety-related symptoms in obesity.

Keywords: Fear generalization; Fear memory; Fear overgeneralization; Obesity; Skin conductance responses.

Fig. 1

Schematic diagram depicting the experimental outline. In the first session (day 1), participants with obesity (n = 16) and healthy participants (n = 16) underwent a preconditioning phase in which they were exposed to neutral pictures and a neutral tone (800 Hz). Then, they underwent a single-cue fear conditioning in which the neutral tone (conditioned stimulus, CS, 800 Hz) was paired with multisensory cues composed of fearful pictures and auditory scream samples (unconditioned stimuli, USs). During the whole session, SCRs were recorded. In the second session (day 2), subjects were re-exposed to the neutral pictures, and then they underwent an autonomic reactions test during which they were presented with the CS and two new stimuli (NS₁, 400 Hz and NS₂, 1200 Hz) while being recorded in their SCRs. Then, participants underwent a 2AFC recognition task during which they were presented with tone pairs each composed of the CS and one of the two NSs, and they were asked to recognize the CS providing a confidence level for each choice. Participants then underwent a 2AFC perceptual discrimination test, in which they had to judge whether the two tones in each pair (CS and/or NSs) were “the same tone” or “different tones”. Last, participants rated the fear feelings evoked by the USs.

Fig. 2

Autonomic reactions during pre-conditioning, conditioning, and pre-test phases. (A) Dot plot representing the mean SCRs elicited by the neutral pictures during the first session in the two conditions. Electrodermal reactions were similar between the two groups. (B) Mean SCRs evoked by the 800 Hz tone in the pre-conditioning were comparable between the two groups. (C) Participants’ reactions to the USs in the conditioning phase were similar in the two groups. (D) The two groups similarly responded to the neutral pictures during the pre-test phase in the second session. All data are mean and SEM. Student’s unpaired t test (A, B, C, D).

Fig. 3

Autonomic reactions during the test session. Healthy participants showed a specific pattern of defensive responses: the CS evoked significantly higher SCRs than the NS₁ and almost significantly higher than the NS₂. Instead, participants with obesity showed a generalized pattern of defensive reactions since SCRs were similarly strong to the CS and the NSs. CS-evoked responses were similar between groups but participants with obesity reacted stronger to both the NSs relative to the healthy participants. *P < 0.05, **P < 0.01. All data are mean and SEM. The level “0” corresponds to the pre-conditioning mean SCR response to the CS. 2 × 3 mixed ANOVA followed by Bonferroni-adjusted post hoc comparisons.

Fig. 4

Recognition performance and appraisal of fear feelings during the test session. (A) Recognition patterns were similar between the two groups. (B) Confidence levels were comparable between the two groups, both for correct responses and for recognition errors. (C) Fear ratings of the USs were similar in the two groups. All data are mean and SEM. Student’s unpaired t test (A, B, C).