Abstract
Subjective assessment of emotional valence is typically associated with both brain activity and autonomic arousal. Accurately assessing emotional salience is particularly important when perceiving threat. We sought to characterize the neural correlates of the interaction between behavioral and autonomic responses to potentially threatening visual and auditory stimuli. Twenty-five healthy male subjects underwent fMRI scanning whilst skin conductance responses (SCR) were recorded. One hundred and eighty pictures, sentences, and sounds were assessed as “harmless” or “threatening.” Individuals' stimulus-locked, phasic SCRs and trial-by-trial behavioral assessments were entered as regressors into a flexible factorial design to establish their separate autonomic and behavioral neural correlates, and convolved to examine psycho-autonomic interaction (PAI) effects. Across all stimuli, “threatening,” compared with “harmless” behavioral assessments were associated with mainly frontal and precuneus activation with specific within-modality activations including bilateral parahippocampal gyri (pictures), bilateral anterior cingulate cortex (ACC) and frontal pole (sentences), and right Heschl's gyrus and bilateral temporal gyri (sounds). Across stimulus modalities SCRs were associated with activation of parieto-occipito-thalamic regions, an activation pattern which was largely replicated within-modality. In contrast, PAI analyses revealed modality-specific activations including right fusiform/parahippocampal gyrus (pictures), right insula (sentences), and mid-cingulate gyrus (sounds). Phasic SCR activity was positively correlated with an individual's propensity to assess stimuli as “threatening.” SCRs may modulate cognitive assessments on a “harmless–threatening” dimension, thereby modulating affective tone and hence behavior.
Highlights
Changing environmental stimuli are rapidly processed by the brain to allow reorienting of cognitive resources such as attention toward possible threats (Öhman et al, 2001a,b)
BEHAVIORAL, PHYSIOLOGICAL, AND NEUROPSYCHOLOGICAL For behavioral response times (RTs), in a 3 × 2 × 2 within-subject, repeatedmeasures ANOVA, there was a main effect of subjective assessment [“threatening” longer RTs than “harmless”; F(1, 24) = 14.51, p = 0.001; Figure 2], a main effect of modality [sounds longer RTs than sentences; sentences longer RTs than pictures; F(2, 48) = 98.05, p < 0.001; Figure 2], but no main effect of the presence or absence of an skin conductance responses (SCR) [F(1, 24) = 0.26, p = 0.614]
There were no significant differences in the number of SCRs to stimuli assessed as “threatening” compared with those assessed as “harmless”
Summary
Changing environmental stimuli are rapidly processed by the brain to allow reorienting of cognitive resources such as attention toward possible threats (Öhman et al, 2001a,b) Such potential threats are identified by their emotional salience—a stimulus’s state or quality of standing out relative to neighboring stimuli. An “emotional coloring” of the mental state accompanying every act or thought, arises from a dynamic interaction between cognitive assessment and ANS activity (Ross, 1997) Disturbance of this dynamic interaction, for example, in schizophrenia, may manifest as “sinister attribution bias” in which patients attribute negative connotations to apparently benign situations (Peer et al, 2004; Premkumar et al, 2008; Cohen and Minor, 2010). Individuals within the “healthy” continuum may demonstrate varying levels of ANS and BOLD activity in response to potentially threatening stimuli which could influence the way in which they perceive stimuli and thereby interpret the world (Martin and Penn, 2001; Allen et al, 2007)
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