Ultrahigh Field fMRI Reveals Different Roles of the Temporal and Frontoparietal Cortices in Subjective Awareness.

A central question in consciousness theories is whether one is dealing with a dichotomous ("all-or-none") or a gradual phenomenon. In this 7T fMRI study, we investigated whether dichotomy or gradualness in fact depends on the brain region associated with perceptual awareness reports. Both male and female human subjects performed an emotion discrimination task (fear vs neutral bodies) presented under continuous flash suppression with trial-based perceptual awareness measures. Behaviorally, recognition sensitivity increased linearly with increased stimuli awareness and was at chance level during perceptual unawareness. Physiologically, threat stimuli triggered a slower heart rate than neutral ones during "almost clear" stimulus experience, indicating freezing behavior. Brain results showed that activity in the occipitotemporal, parietal, and frontal regions as well as in the amygdala increased with increased stimulus awareness while early visual areas showed the opposite pattern. The relationship between temporal area activity and perceptual awareness best fitted a gradual model while the activity in frontoparietal areas fitted a dichotomous model. Furthermore, our findings illustrate that specific experimental decisions, such as stimulus type or the approach used to evaluate awareness, play pivotal roles in consciousness studies and warrant careful consideration.

Early visual experience refines the retinotopic organization within and across visual cortical regions.

Early visual areas are retinotopically organized in human and non-human primates. Population receptive field (pRF) size increases with eccentricity and from lower- to higher-level visual areas. Furthermore, the cortical magnification factor (CMF), a measure of how much cortical space is devoted to each degree of visual angle, is typically larger for foveal as opposed to peripheral regions of the visual field. Whether this fine-scale organization within and across visual areas depends on early visual experience has yet been unknown. Here, we employed 7T functional magnetic resonance imaging pRF mapping to assess the retinotopic organization of early visual regions (i.e., V1, V2, and V3) in eight sight recovery individuals with a history of congenital blindness until a maximum of 4 years of age. Compared with sighted controls, foveal pRF sizes in these individuals were larger, and pRF sizes did not show the typical increase with eccentricity and down the visual cortical processing stream (V1-V2-V3). Cortical magnification was overall diminished and decreased less from foveal to parafoveal visual field locations. Furthermore, cortical magnification correlated with visual acuity in sight recovery individuals. The results of this study suggest that early visual experience is essential for refining a presumably innate prototypical retinotopic organization in humans within and across visual areas, which seems to be crucial for acquiring full visual capabilities.

Does the visual word form area split in bilingual readers? A millimeter-scale 7-T fMRI study.

In expert readers, a brain region known as the visual word form area (VWFA) is highly sensitive to written words, exhibiting a posterior-to-anterior gradient of increasing sensitivity to orthographic stimuli whose statistics match those of real words. Using high-resolution 7-tesla functional magnetic resonance imaging (fMRI), we ask whether, in bilingual readers, distinct cortical patches specialize for different languages. In 21 English-French bilinguals, unsmoothed 1.2-millimeters fMRI revealed that the VWFA is actually composed of several small cortical patches highly selective for reading, with a posterior-to-anterior word-similarity gradient, but with near-complete overlap between the two languages. In 10 English-Chinese bilinguals, however, while most word-specific patches exhibited similar reading specificity and word-similarity gradients for reading in Chinese and English, additional patches responded specifically to Chinese writing and, unexpectedly, to faces. Our results show that the acquisition of multiple writing systems can indeed tune the visual cortex differently in bilinguals, sometimes leading to the emergence of cortical patches specialized for a single language.

Inconsistencies in atlas-based volumetric measures of the human nucleus basalis of Meynert: A need for high-resolution alternatives.

The nucleus basalis of Meynert (nbM) is the major source of cortical acetylcholine (ACh) and has been related to cognitive processes and to neurological disorders. However, spatially delineating the human nbM in MRI studies remains challenging. Due to the absence of a functional localiser for the human nbM, studies to date have localised it using nearby neuroanatomical landmarks or using probabilistic atlases. To understand the feasibility of MRI of the nbM we set our four goals; our first goal was to review current human nbM region-of-interest (ROI) selection protocols used in MRI studies, which we found have reported highly variable nbM volume estimates. Our next goal was to quantify and discuss the limitations of existing atlas-based volumetry of nbM. We found that the identified ROI volume depends heavily on the atlas used and on the probabilistic threshold set. In addition, we found large disparities even for data/studies using the same atlas and threshold. To test whether spatial resolution contributes to volume variability, as our third goal, we developed a novel nbM mask based on the normalized BigBrain dataset. We found that as long as the spatial resolution of the target data was 1.3 mm isotropic or above, our novel nbM mask offered realistic and stable volume estimates. Finally, as our last goal we tried to discern nbM using publicly available and novel high resolution structural MRI ex vivo MRI datasets. We find that, using an optimised 9.4T quantitative T2⁎ ex vivo dataset, the nbM can be visualised using MRI. We conclude caution is needed when applying the current methods of mapping nbM, especially for high resolution MRI data. Direct imaging of the nbM appears feasible and would eliminate the problems we identify, although further development is required to allow such imaging using standard (f)MRI scanning.

Acquired prosopagnosia with structurally intact and functional fusiform face area and with face identity-specific configuration processing deficits.

Prosopagnosia or loss of face perception and recognition is still poorly understood and rare single cases of acquired prosopagnosia can provide a unique window on the behavioural and brain basis of normal face perception. The present study of a new case of acquired prosopagnosia with bilateral occipito-temporal lesions but a structurally intact FFA and OFA investigated whether the lesion overlapped with the face network and whether the structurally intact FFA showed a face selective response. We also investigated the behavioral correlates of the neural findings and assessed configural processing in the context of facial and non-facial identity recognition, expression recognition and memory, also focusing on the face-selectivity of each specific deficit. The findings reveal a face-selective response in the FFA, despite lesions in the face perception network. At the behavioural level, the results showed impaired configural processing for facial identity, but not for other stimulus categories and not for facial expression recognition. These findings challenge a critical role of the FFA for face identity processing and support a domain-specific account of configural processing.

Being the victim of virtual abuse changes default mode network responses to emotional expressions.

Recent behavioural studies have provided evidence that virtual reality (VR) experiences have an impact on socio-affective processes, and a number of findings now underscore the potential of VR for therapeutic interventions. An interesting recent result is that when male offenders experience a violent situation as a female victim of domestic violence in VR, their sensitivity for recognition of fearful facial expressions improves. A timely question now concerns the underlying brain mechanisms of these behavioural effects as these are still largely unknown. The current study used fMRI to measure the impact of a VR intervention in which participants experienced a violent aggression from the specific vantage point of the victim. We compared brain processes related to facial and bodily emotion perception before and after the VR experience. Our results show that the virtual abuse experience led to an enhancement of Default Mode Network (DMN) activity, specifically associated with changes in the processing of ambiguous emotional stimuli. In contrast, DMN activity was decreased when observing fully fearful expressions. Finally, we observed increased variability in brain activity for male versus female facial expressions. Taken together, these results suggest that the first-person perspective of a virtual violent situation impacts emotion recognition through modifications in DMN activity. Our study contributes to a better understanding of the brain mechanisms associated with the behavioural effects of VR interventions in the context of a violent confrontation with the male participant embodied as a female victim. Furthermore, this research also consolidates the use of VR embodied perspective-taking interventions for addressing socio-affective impairments.

Reorganization of Sound Location Processing in the Auditory Cortex of Blind Humans.

Auditory spatial tasks induce functional activation in the occipital-visual-cortex of early blind humans. Less is known about the effects of blindness on auditory spatial processing in the temporal-auditory-cortex. Here, we investigated spatial (azimuth) processing in congenitally and early blind humans with a phase-encoding functional magnetic resonance imaging (fMRI) paradigm. Our results show that functional activation in response to sounds in general-independent of sound location-was stronger in the occipital cortex but reduced in the medial temporal cortex of blind participants in comparison with sighted participants. Additionally, activation patterns for binaural spatial processing were different for sighted and blind participants in planum temporale. Finally, fMRI responses in the auditory cortex of blind individuals carried less information on sound azimuth position than those in sighted individuals, as assessed with a 2-channel, opponent coding model for the cortical representation of sound azimuth. These results indicate that early visual deprivation results in reorganization of binaural spatial processing in the auditory cortex and that blind individuals may rely on alternative mechanisms for processing azimuth position.

Threat Anticipation in Pulvinar and in Superficial Layers of Primary Visual Cortex (V1). Evidence from Layer-Specific Ultra-High Field 7T fMRI.

The perceptual system gives priority to threat-relevant signals with survival value. In addition to the processing initiated by sensory inputs of threat signals, prioritization of threat signals may also include processes related to threat anticipation. These neural mechanisms remain largely unknown. Using ultra-high-field 7 tesla (7T) fMRI, we show that anticipatory processing takes place in the early stages of visual processing, specifically in the pulvinar and V1. When anticipation of a threat-relevant fearful face target triggered false perception of not-presented target, there was enhanced activity in the pulvinar as well as in the V1 superficial-cortical-depth (layers 1-3). The anticipatory activity was absent in the LGN or higher visual cortical areas (V2-V4). The effect in V1 was specific to the perception of fearful face targets and did not generalize to happy face targets. A preliminary analysis showed that the connectivity between the pulvinar and V1 superficial-cortical-depth was enhanced during false perception of threat, indicating that the pulvinar and V1 may interact in preparation of anticipated threat. The anticipatory processing supported by the pulvinar and V1 may play an important role in non-sensory-input-driven anxiety states.

Unconscious fearful body perception enhances discrimination of conscious anger expressions under continuous flash suppression.

The continuous flash suppression (CFS) paradigm is increasingly used to study unconscious visual perception. Our goal was to use CFS and to to compare the results with previous findings from patients with brain lesions, and studies of healthy participants. We used an emotion discrimination task and bilaterally presented whole-body postures expressing fear or anger, rendering the stimuli invisible in either one of the visual fields. We found that the CFS presentation did not yield the classical redundant target effect of response facilitation when the unconsciously seen stimuli had congruent emotions; instead we found a facilitation effect in reaction times by body stimuli of incongruent emotions, especially by the unconscious fearful body facilitating discrimination of conscious angry body. Our results with healthy participants showed similarities to hemianopia patients without blindsight, but not to blindsight or neglect patients, indicating that unconscious visual processing is not a single phenomenon, but is likely to involve multiple mechanisms, processes and brain regions. Further studies are necessary to validate the facilitation effect of fearful bodies on other tasks, and to study the neural substrates of this effect.

Influence of continuous flash suppression mask frequency on stimulus visibility.

The continuous flash suppression (CFS) paradigm is increasingly used in consciousness research, but its mechanisms are still not fully understood. To better understand its temporal properties, we presented the CFS masks at 9 frequencies, and examined their influence on stimuli visibility, while taking into account the inter-individual variability and the change of CFS suppression as the experiment progressed. The frequencies consisted of fundamental frequencies of 3, 4 and 5 Hz, and their 2nd and 3rd harmonics, which included the 10 Hz frequency typically used in most of the CFS studies. We found that the suppression of stimulus awareness was stronger under 4, 6 and 8 Hz than 10 Hz. After controlling for inter-individual variability with mixed-effects analysis, we found that the number of seen trials was lower for the 4 Hz-basis frequencies than the 5 Hz ones, and was lower for the 2nd than 3rd harmonic. We propose that this may be caused by an interaction between the CFS masks and the ongoing sampling of the attentional mechanism. Examining individual data, we also found a habituation effect that the participants saw significantly more stimuli as the experiment progressed. Our results suggest that these factors need to be taken care of in future CFS studies in order to achieve optimal visual awareness suppression and ensure the generalizability of results.

Classical paintings may trigger pain and pleasure in the gendered brain.

The human body is the most common object of pictorial representation in western art and its representations trigger a vast range of experiences from pain to pleasure. The goal of this study was to investigate brain activity triggered by paintings of male and female body images exemplifying conditions associated with pleasure or pain. Our findings show participant-general as well as gender specific brain activity for either the pain or the pleasure conditions. Although our participants were fully aware that they were viewing artworks, the inferior parietal lobule - known for its role in the perception of emotional body images - and the somatosensory cortex related to touch were selectively active for female body paintings in all participants in the pleasure conditions. As regards gender we observed that the sight of female bodies activated the subgenual anterior cingulate cortex in males, an area known to subserve autonomic arousal. In contrast, in females the sight of the male body activated reward and control related parts of the dorsal anterior cingulate cortex. This study supports the notion that some basic evolutionary processes operate when we view body images, also when they are cultural heritage paintings far removed from daily experience.

The Influence of Conscious and Unconscious Body Threat Expressions on Motor Evoked Potentials Studied With Continuous Flash Suppression.

The observation of threatening expression in others is a strong cue for triggering an action response. One method of capturing such action responses is by measuring the amplitude of motor evoked potentials (MEPs) elicited with single pulse TMS over the primary motor cortex. Indeed, it has been shown that viewing whole body expressions of threat modulate the size of MEP amplitude. Furthermore, emotional cues have been shown to act on certain brain areas even outside of conscious awareness. In the current study, we explored if the influence of viewing whole body expressions of threat extends to stimuli that are presented outside of conscious awareness in healthy participants. To accomplish this, we combined the measurement of MEPs with a continuous flash suppression task. In experiment 1, participants were presented with images of neutral bodies, fearful bodies, or objects that were either perceived consciously or unconsciously, while single pulses of TMS were applied at different times after stimulus onset (200, 500, or 700 ms). In experiment 2 stimuli consisted of neutral bodies, angry bodies or objects, and pulses were applied at either 200 or 400 ms post stimulus onset. In experiment 1, there was a general effect of the time of stimulation, but no condition specific effects were evident. In experiment 2 there were no significant main effects, nor any significant interactions. Future studies need to look into earlier effects of MEP modulation by emotion body stimuli, specifically when presented outside of conscious awareness, as well as an exploration of other outcome measures such as intracortical facilitation.

Dynamic Interactions between Emotion Perception and Action Preparation for Reacting to Social Threat: A Combined cTBS-fMRI Study.

Expressions of emotion are powerful triggers for situation-appropriate responses by the observer. Of particular interest regarding the preparation of such adaptive actions are parietal and premotor cortices, given their potential for interaction with the amygdala (AMG), which is known to play a crucial role in the processing of affective information and in motor response. We set out to disentangle the respective roles of the inferior parietal lobule (IPL) and ventral premotor cortex (PMv) in humans in the processing of emotional body expressions by assessing remote effects of continuous theta burst stimulation (cTBS) in the action network and in AMG. Participants were presented with blocks of short videos showing either angry or neutral whole-body actions. The experiment consisted of three fMRI sessions: two sessions were preceded by stimulation of either right IPL (rIPL) or right PMv (rPMv); and a third session assessed baseline activity. Interestingly, whereas at baseline the left AMG did not differentiate between neutral and angry body postures, a significant difference between these conditions emerged after stimulation of either rIPL or rPMv, with much larger responses to angry than to neutral stimuli. In addition, the effects of cTBS stimulation and emotion were also observed in two other action-relevant areas, the supplementary motor area and the superior parietal cortex. Together, these results show how areas involved in action and emotion perception and in action preparation interact dynamically.

Ventral and Dorsal Pathways Relate Differently to Visual Awareness of Body Postures under Continuous Flash Suppression.

Visual perception includes ventral and dorsal stream processes. However, it is still unclear whether the former is predominantly related to conscious and the latter to nonconscious visual perception as argued in the literature. In this study upright and inverted body postures were rendered either visible or invisible under continuous flash suppression (CFS), while brain activity of human participants was measured with functional MRI (fMRI). Activity in the ventral body-sensitive areas was higher during visible conditions. In comparison, activity in the posterior part of the bilateral intraparietal sulcus (IPS) showed a significant interaction of stimulus orientation and visibility. Our results provide evidence that dorsal stream areas are less associated with visual awareness.

Looking at the face and seeing the whole body. Neural basis of combined face and body expressions.

In the natural world, faces are not isolated objects but are rather encountered in the context of the whole body. Previous work has studied the perception of combined faces and bodies using behavioural and electrophysiological measurements, but the neural correlates of emotional face-body perception still remain unexplored. Here, we combined happy and fearful faces and bodies to investigate the influence of body expressions on the neural processing of the face, the effect of emotional ambiguity between the two and the role of the amygdala in this process. Our functional magnetic resonance imaging analyses showed that the activity in motor, prefrontal and visual areas increases when facial expressions are presented together with bodies rather than in isolation, consistent with the notion that seeing body expressions triggers both emotional and action-related processes. In contrast, psychophysiological interaction analyses revealed that amygdala modulatory activity increases after the presentation of isolated faces when compared to combined faces and bodies. Furthermore, a facial expression combined with a congruent body enhanced both cortical activity and amygdala functional connectivity when compared to an incongruent face-body compound. Finally, the results showed that emotional body postures influence the processing of facial expressions, especially when the emotion conveyed by the body implies danger.

Looming sensitive cortical regions without V1 input: evidence from a patient with bilateral cortical blindness.

Fast and automatic behavioral responses are required to avoid collision with an approaching stimulus. Accordingly, looming stimuli have been found to be highly salient and efficient attractors of attention due to the implication of potential collision and potential threat. Here, we address the question of whether looming motion is processed in the absence of any functional primary visual cortex and consequently without awareness. For this, we investigated a patient (TN) suffering from complete, bilateral damage to his primary visual cortex. Using an fMRI paradigm, we measured TN's brain activation during the presentation of looming, receding, rotating, and static point lights, of which he was unaware. When contrasted with other conditions, looming was found to produce bilateral activation of the middle temporal areas, as well as the superior temporal sulcus and inferior parietal lobe (IPL). The latter are generally thought to be involved in multisensory processing of motion in extrapersonal space, as well as attentional capture and saliency. No activity was found close to the lesioned V1 area. This demonstrates that looming motion is processed in the absence of awareness through direct subcortical projections to areas involved in multisensory processing of motion and saliency that bypass V1.

The Body as a Tool for Anger Awareness--Differential Effects of Angry Facial and Bodily Expressions on Suppression from Awareness.

Emotional signals are perceived whether or not we are aware of it. The evidence so far mostly came from studies with facial expressions. Here, we investigated whether the pattern of non-conscious face expression perception is found for whole body expressions. Continuous flash suppression (CFS) was used to measure the time for neutral, fearful, and angry facial or bodily expressions to break from suppression. We observed different suppression time patterns for emotions depending on whether the stimuli were faces or bodies. The suppression time for anger was shortest for bodily expressions, but longest for the facial expressions. This pattern indicates different processing and detection mechanisms for faces and bodies outside awareness, and suggests that awareness mechanisms associated with dorsal structures might play a role in becoming conscious of angry bodily expressions.

Neural correlates of body and face perception following bilateral destruction of the primary visual cortices.

Non-conscious visual processing of different object categories was investigated in a rare patient with bilateral destruction of the visual cortex (V1) and clinical blindness over the entire visual field. Images of biological and non-biological object categories were presented consisting of human bodies, faces, butterflies, cars, and scrambles. Behaviorally, only the body shape induced higher perceptual sensitivity, as revealed by signal detection analysis. Passive exposure to bodies and faces activated amygdala and superior temporal sulcus. In addition, bodies also activated the extrastriate body area, insula, orbitofrontal cortex (OFC) and cerebellum. The results show that following bilateral damage to the primary visual cortex and ensuing complete cortical blindness, the human visual system is able to process categorical properties of human body shapes. This residual vision may be based on V1-independent input to body-selective areas along the ventral stream, in concert with areas involved in the representation of bodily states, like insula, OFC, and cerebellum.