Neural systems supporting interoceptive awareness

Influential theories of human emotion argue that subjective feeling states involve representation of bodily responses elicited by emotional events. Within this framework, individual differences in intensity of emotional experience reflect variation in sensitivity to internal bodily responses. We measured regional brain activity by functional magnetic resonance imaging (fMRI) during an interoceptive task wherein subjects judged the timing of their own heartbeats. We observed enhanced activity in insula, somatomotor and cingulate cortices. In right anterior insular/opercular cortex, neural activity predicted subjects' accuracy in the heartbeat detection task. Furthermore, local gray matter volume in the same region correlated with both interoceptive accuracy and subjective ratings of visceral awareness. Indices of negative emotional experience correlated with interoceptive accuracy across subjects. These findings indicate that right anterior insula supports a representation of visceral responses accessible to awareness, providing a substrate for subjective feeling states.     

Amygdala damage affects event‐related potentials for fearful faces at specific time windows

The amygdala is known to influence processing of threat‐related stimuli in distant brain regions, including visual cortex. The time‐course of these distant influences is unknown, although this information is important for resolving debates over likely pathways mediating an apparent rapidity in emotional processing. To address this, we recorded event‐related potentials (ERPs) to seen fearful face expressions, in preoperative patients with medial temporal lobe epilepsy who had varying degrees of amygdala pathology, plus healthy volunteers. We found that amygdala damage diminished ERPs for fearful versus neutral faces within the P1 time‐range, ∼100–150 ms, and for a later component at ∼500–600 ms. Individual severity of amygdala damage determined the magnitude of both these effects, consistent with a causal amygdala role. By contrast, amygdala damage did not affect explicit perception of fearful expressions nor a distinct emotional ERP effect at 150–250 ms. These results demonstrate two distinct time‐points at which the amygdala influences fear processing. The data also demonstrate that while not all aspects of expression processing are disrupted by amygdala damage, there is a crucial impact on an early P1 component. These findings are consistent with the existence of multiple processing stages or routes for fearful faces that vary in their dependence on amygdala function. Hum Brain Mapp, 2010. © 2009 Wiley‐Liss, Inc.     

Identification of the relative onset time of a two-tone complex: auditory sensitivity or language based?

Categorical perception occurs when equal physical differences on a continuum sometimes cause no changes in the identification of a stimulus, while at other points on the same continuum, that difference causes an abrupt change in perception. One of the unresolved issues regarding this phenomenon is what determines categorical perception: a special speech mode or "natural" psychophysical boundaries. One way to answer this question is by investigating categorical perception with non-speech stimuli. An example is the identification of the relative onset of a two-tone complex (TOT) analogous to voice-onset time (VOT), the acoustic cue to voicing in initial position. Studies in English found similar category boundaries for TOT and VOT (at +20 ms) supporting the non-speech specific theory. The purpose of this study was to investigate TOT in Hebrew-speaking listeners whose language uses very different VOT values from those reported in English. Twenty Hebrew-speaking young adults participated in this study. Stimuli consisted of a two-tone complex that varied in the relative onset time of the lower tone from a lead of -50 ms to a lag of +50 ms in 10 ms steps. Results show that: (1) All subjects were able to identify the lag conditions from the simultaneous ones but only half of them were also able to identify the lead from the simultaneous ones. This was explained in terms of prominent pitch cues available when shifting from simultaneous to lagging stimuli. (2) Hebrew category boundaries (CBs) for TOT are shorter than those of VOT, and both are shorter than the respective English ones. Nonetheless, all CBs fell into the range of 10 to 30 ms. The data support the hypothesis that "natural" psychophysical boundaries determine categorical perception but behavioral measures may be influenced by speech.     

Sensing the invisible: differential sensitivity of visual cortex and amygdala to traumatic context

To what extent does emotional traumatic context affect sensory processing in the brain? A striking example of emotional impact on sensation is manifested in posttraumatic stress disorder (PTSD), in which a severe emotional trauma produces recurrent and vivid unpleasant sensory recollections. Here we report on an fMRI study exploring the sensory processing of trauma-related pictures in the visual cortex and amygdala in respect to PTSD. The impact of traumatic experience on brain responses was tested in relation to stimuli content and its level of recognition in a parametric factorial design. Twenty combat veterans, 10 with and 10 without PTSD, viewed backward-masked images of combat and noncombat content, presented at below, near, and above recognition thresholds. The response to combat content evoked more activation in the visual cortex in PTSD subjects than in non-PTSD subjects, only when images were presented at below recognition threshold. By contrast, the amygdala demonstrated increased activation in PTSD subjects irrespective of content and recognition threshold of the images. These intriguing findings are compatible with the notion that in PTSD, emotional traumatic experience could modify visual processing already at the preattentive level. On the other hand, lack of content specificity in the amygdala point to a possible predisposed mechanism for pathological processing of traumatic experience. The differential sensitivity of the amygdala and visual cortex to traumatic context implies distinct roles of limbic and sensory regions in the registration and recollection of emotional experience in the brain.     

Activity in the human brain predicting differential heart rate responses to emotional facial expressions

The James-Lange theory of emotion proposes that automatically generated bodily reactions not only color subjective emotional experience of stimuli, but also necessitate a mechanism by which these bodily reactions are differentially generated to reflect stimulus quality. To examine this putative mechanism, we simultaneously measured brain activity and heart rate to identify regions where neural activity predicted the magnitude of heart rate responses to emotional facial expressions. Using a forewarned reaction time task, we showed that orienting heart rate acceleration to emotional face stimuli was modulated as a function of the emotion depicted. The magnitude of evoked heart rate increase, both across the stimulus set and within each emotion category, was predicted by level of activity within a matrix of interconnected brain regions, including amygdala, insula, anterior cingulate, and brainstem. We suggest that these regions provide a substrate for translating visual perception of emotional facial expression into differential cardiac responses and thereby represent an interface for selective generation of visceral reactions that contribute to the embodied component of emotional reaction.     

On-line attentional selection from competing stimuli in opposite visual fields: effects on human visual cortex and control processes

We used fMRI to investigate competition and on-line attentional selection between targets and distractors in opposite visual hemifields. Displays comprised a high-contrast square-wave grating, defined as target by its orientation, presented alone (unilateral) or with a similar distractor of orthogonal orientation in the opposite hemifield (bilateral displays). The target appeared unpredictably on the left or right, precluding anticipatory attention to one side. We found greater activation in target-contralateral superior occipital gyrus for unilateral than for bilateral displays, indicating suppression of the target's visual representation by distractor presence despite the competing distractor projecting to a different occipital hemisphere. Several frontal and parietal regions showed greater activation for bilateral than unilateral trials, suggesting involvement in on-line attentional selection. This was particularly pronounced for regions in bilateral intraparietal sulcus (IPS), which also showed greater functional coupling with occipital cortex specifically on bilateral trials that required selection plus some repetition-suppression effects when target side was repeated, but again only on bilateral trials requiring selection. Our results indicate that competition between visual stimuli in opposite hemifields can influence occipital cortex, and implicate IPS in resolution of this competition by selection.     

Differential stimuli and task effects in the amygdala and sensory areas

Whether the amygdala responds in a stimulus- or a task-specific way, and how it corresponds to such effects in sensory cortices is dubious. Eighteen volunteers participated in a functional magnetic resonance imaging study in which they were asked to identify either emotion or gender in visually presented scenes, faces, and sentences. Amygdala and the lateral occipital complex showed similar stimulus effect with greater activation to scenes than to faces and sentences, whereas the superior temporal complex responded preferentially to sentences. No task effect was observed in the amygdala, whereas lateral occipital complex and superior temporal complex showed left lateralized selectivity to the emotional task. These results suggest that the amygdala is more sensitive to stimulus than explicit task parameters when processing emotion.     

A critique of functional localisers

In this critique, we review the usefulness of functional localising scans in functional MRI studies. We consider their conceptual motivations and the implications for experimental design and inference. Functional localisers can often be viewed as acquiring data from cells that have been removed from an implicit factorial design. This perspective reveals their potentially restrictive nature. We deconstruct two examples from the recent literature to highlight the key issues. We conclude that localiser scans can be unnecessary and, in some instances, lead to a biased and inappropriately constrained characterisation of functional anatomy.