Pia Rotshtein

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.

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.

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.

Dissociating the neural mechanisms of memory-based guidance of visual selection

Visual selection is influenced by items in working memory (WM) and priming from implicit memory when a stimulus is repeated across time. WM effects are typically held to be top-down in nature [Soto D, Heinke D, Humphreys GW, Blanco MJ (2005) J Exp Psychol Hum Percept Perform 31:248–261], whereas implicit priming may operate in a bottom-up manner [Theeuwes J, Reimann B, Mortier K (2006) Vis Cogn 14: 466–489]. How WM and implicit priming affects influence visual selection remains poorly understood, however. Here, we report functional MRI evidence that dissociates the neural mechanisms involved in these memory-based effects on selection. The reappearance of a stimulus held in WM enhanced activity in superior frontal gyrus, midtemporal, and occipital areas that are known to encode the prior occurrence of stimuli. In contrast, mere stimulus repetition elicited a suppressive response in the same regions. An additional finding was that a frontothalamic network was sensitive to the behavioral relevance of a match between the contents of WM and the visual search array, enhancing activity when the contents of WM matched the critical target of selection. Items held in WM influence selection by using neural coding distinct to effects of mere repetition.

Separating neural correlates of allocentric and egocentric neglect: Distinct cortical sites and common white matter disconnections

Insights into the functional nature and neuroanatomy of spatial attention have come from research in neglect patients but to date many conflicting results have been reported. The novelty of the current study is that we used voxel-wise analyses based on information from segmented grey and white matter tissue combined with diffusion tensor imaging to decompose neural substrates of different neglect symptoms. Allocentric neglect was associated with damage to posterior cortical regions (posterior superior temporal sulcus, angular, middle temporal and middle occipital gyri). In contrast, egocentric neglect was associated with more anterior cortical damage (middle frontal, postcentral, supramarginal, and superior temporal gyri) and damage within subcortical structures. Damage to intraparietal sulcus (IPS) and the temporo-parietal junction (TPJ) was associated with both forms of neglect. Importantly, we showed that both disorders were associated with white matter lesions suggesting damage within long association and projection pathways such as the superior longitudinal, superior fronto-occipital, inferior longitudinal, and inferior fronto-occipital fascicule, thalamic radiation, and corona radiata. We conclude that distinct cortical regions control attention (a) across space (using an egocentric frame of reference) and (b) within objects (using an allocentric frame of reference), while common cortical regions (TPJ, IPS) and common white matter pathways support interactions across the different cortical regions.

Role of Features and Second-order Spatial Relations in Face Discrimination, Face Recognition, and Individual Face Skills: Behavioral and Functional Magnetic Resonance Imaging Data

We compared the contribution of featural information and second-order spatial relations (spacing between features) in face processing. A fully factorial design has the same or different features (eyes, mouth, and nose) across two successive displays, whereas, orthogonally, the second-order spatial relations between those features were the same or different. The range of such changes matched the possibilities within the population of natural face images. Behaviorally, we found that judging whether two successive faces depicted the same person was dominated by features, although second-order spatial relations also contributed. This influence of spatial relations correlated, for individual subjects, with their skill at recognition of faces (as famous, or as previously exposed) in separate behavioral tests. Using the same repetition design in functional magnetic resonance imaging, we found feature-dependent effects in the lateral occipital and right fusiform regions. In addition, there were spatial relation effects in the bilateral inferior occipital gyrus and right fusiform that correlated with individual differences in (separately measured) behavioral sensitivity to those changes. The results suggest that featural and second-order spatial relation aspects of faces make distinct contributions to behavioral discrimination and recognition, with features contributing most to face discrimination and second-order spatial relational aspects correlating best with recognition skills. Distinct neural responses to these aspects were found with functional magnetic resonance imaging, particularly when individual skills were taken into account for the impact of second-order spatial relations.

Pleasant music overcomes the loss of awareness in patients with visual neglect

During the past 20 years there has been much research into the factors that modulate awareness of contralesional information in neurological patients with visual neglect or extinction. However, the potential role of the individuals emotional state in modulating awareness has been largely overlooked. In the current study, we induced a pleasant and positive affective response in patients with chronic visual neglect by allowing them to listen to their pleasant preferred music. We report that the patients showed enhanced visual awareness when tasks were performed under preferred music conditions relative to when tasks were performed either with unpreferred music or in silence. These results were also replicated when positive affect was induced before neglect was tested. Functional MRI data showed enhanced activity in the orbitofrontal cortex and the cingulate gyrus associated with emotional responses when tasks were performed with preferred music relative to unpreferred music. Improved awareness of contralesional (left) targets with preferred music was also associated with a strong functional coupling between emotional areas and attentional brain regions in spared areas of the parietal cortex and early visual areas of the right hemisphere. These findings suggest that positive affect, generated by preferred music, can decrease visual neglect by increasing attentional resources. We discuss the possible roles of arousal and mood in generating these effects.

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.

Coupling social attention to the self forms a network for personal significance

Prior social psychological studies show that newly assigned personal significance can modulate high-level cognitive processes, e.g., memory and social evaluation, with self- and other-related information processed in dissociated prefrontal structure: ventral vs. dorsal, respectively. Here, we demonstrate the impact of personal significance on perception and show the neural network that supports this effect. We used an associative learning procedure in which we “tag” a neutral shape with a self-relevant label. Participants were instructed to associate three neutral shapes with labels for themselves, their best friend, or an unfamiliar other. Functional magnetic resonance imaging data were acquired while participants judged whether the shape-label pairs were maintained or swapped. Behaviorally, participants rapidly tagged a neutral stimulus with self-relevance, showing a robust advantage for self-tagged stimuli. Self-tagging responses were associated with enhanced activity in brain regions linked to self-representation [the ventral medial prefrontal cortex (vmPFC)] and to sensory-driven regions associated with social attention [the left posterior superior temporal sulcus (LpSTS)]. In contrast, associations formed with other people recruited a dorsal frontoparietal control network, with the two networks being inversely correlated. Responses in the vmPFC and LpSTS predicted behavioral self-bias effects. Effective connectivity analyses showed that the vmPFC and the LpSTS were functionally coupled, with the strength of coupling associated with behavioral self-biases. The data show that assignment of personal social significance affects perceptual matching by coupling internal self-representations to brain regions modulating attentional responses to external stimuli.

Sensory-Specific Satiety Is Intact in Amnesics Who Eat Multiple Meals

What is the relationship between memory and appetite? We explored this question by examining preferences for recently consumed food in patients with amnesia. Although the patients were unable to remember having eaten, and were inclined to eat multiple meals, we found that sensory-specific satiety was intact in these patients. The data suggest that sensory-specific satiety can occur in the absence of explicit memory for having eaten and that impaired sensory-specific satiety does not underlie the phenomenon of multiple-meal eating in amnesia. Overeating in amnesia may be due to disruption of learned control by physiological aftereffects of a recent meal or to problems utilizing internal cues relating to nutritional state.