Neural correlates of aversive anticipation: An activation likelihood estimate meta-analysis across multiple sensory modalities

Abstract

Anticipation is a universal preparatory response essential to the survival of an organism. Although meta-analytic synthesis of the literature exists for the anticipation of reward, a neuroimaging-based meta-analysis of the neural mechanisms of aversive anticipation is lacking. To address this gap in the literature, we ran an activation likelihood estimate (ALE) meta-analysis of 63 fMRI studies of aversive anticipation across multiple sensory modalities. Results of the ALE meta-analysis provide evidence for a core circuit involved in aversive anticipation, including the anterior insula, anterior cingulate cortex, mid-cingulate cortex, amygdala, thalamus, and caudate nucleus among other regions. Direct comparison of aversive anticipation studies using tactile versus visual stimuli identified additional regions involved in sensory specific aversive anticipation across these sensory modalities. Results from complementary multi-study voxel-wise and NeuroSynth analyses generally provide converging evidence for a core circuit involved in aversive anticipation. The multi-study voxel-wise analyses also implicate a more widespread preparatory response across sensory, motor, and cognitive control regions during more prolonged periods of aversive anticipation. The potential roles of these structures in anticipatory processing as well as avenues for future research are discussed.

Threat-anticipatory psychophysiological response is enhanced in youth with anxiety disorders and correlates with prefrontal cortex neuroanatomy

“…Some previous work suggests left laterality in dlPFC function during threat anticipation, 42,57 although such associations do not arise consistently. 20 Additional research is required to determine asymmetry in prefrontal cortex structural correlates of anticipatory response. We also reported novel associations between the thickness of the posterior insula and psychophysiological response to pain.…”

“…This work has implicated networks such as the insular and prefrontal cortices, as well as connected limbic structures. 4,8,10,[18][19][20][21] Such studies have primarily contrasted neural function during anticipation with safety conditions; relatively few studies have directly linked brain function to anticipatory psychophysiological response (e.g., Seifert and colleagues, 10 Wendt and colleagues 22 and Gu and colleagues 23 ), presenting a gap in the literature.…”

Anticipating control over aversive stimuli is mediated by the medial prefrontal cortex: An fMRI study with healthy adults

“…Not taking into account the dimension of control, there is a consistent body of research referring to the neural basis of the anticipation and the processing of aversive stimulation. A recent meta‐analysis of the neural correlates of aversive anticipation identified a core circuit including the anterior insula, the anterior cingulate cortex (ACC), the midcingulate cortex (MCC), the amygdala, thalamus, and caudate nucleus (Andrzejewski et al, 2019 ). Many of these regions overlap with areas identified as being crucial for the anticipation of rewards (Gu et al, 2019 ; X. Liu, Hairston, Schrier, & Fan, 2011 ; Wilson et al, 2018 ).…”

“…Concerning the actual processing of aversive stimulation, Hayes and Northoff ( 2011 ) showed that the most consistent findings across both human and animal studies demonstrate the implication of the amygdala, the anterior insula, the ventrolateral orbitofrontal cortex, and the rACC. Both of these meta‐analyses on the anticipation and the processing of aversive stimulation (Andrzejewski et al, 2019 ; Hayes & Northoff, 2011 ) considered studies using different sensory modalities. So far, only few studies have used auditory aversive stimuli (Bolstad et al, 2013 ; Carlson, Greenberg, Rubin, & Mujica‐Parodi, 2011 ) despite of the potential that auditory stimulation hold for experimental tasks, for example, in the context of fMRI with humans.…”

“…In consequence, we assumed that additional regions of the reward system would show modulated neural activation. We expected the implication of regions of the reward system that also mediate anticipatory responses, both in the context of aversion and reward (Andrzejewski et al, 2019 ; Gu et al, 2019 ; Wilson et al, 2018 ): the rACC, the anterior insula, the ventral striatum, and the amygdala. Finally, concerning (2) and in line with Hayes and Northoff ( 2011 ), we hypothesized that neural activation would increase in the anterior insula, the rACC, the ventrolateral orbitofrontal cortex, and the amygdala when participants processed aversive compared to neutral sounds.…”