The Basolateral Amygdala Is Essential for Rapid Escape: A Human and Rodent Study.

Rodent research delineates how the basolateral amygdala (BLA) and central amygdala (CeA) control defensive behaviors, but translation of these findings to humans is needed. Here, we compare humans with natural-selective bilateral BLA lesions to rats with a chemogenetically silenced BLA. We find, across species, an essential role for the BLA in the selection of active escape over passive freezing during exposure to imminent yet escapable threat (Timm). In response to Timm, BLA-damaged humans showed increased startle potentiation and BLA-silenced rats demonstrated increased startle potentiation, freezing, and reduced escape behavior as compared to controls. Neuroimaging in humans suggested that the BLA reduces passive defensive responses by inhibiting the brainstem via the CeA. Indeed, Timm conditioning potentiated BLA projections onto an inhibitory CeA pathway, and pharmacological activation of this pathway rescued deficient Timm responses in BLA-silenced rats. Our data reveal how the BLA, via the CeA, adaptively regulates escape behavior from imminent threat and that this mechanism is evolutionary conserved across rodents and humans.

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.

Facial emotion recognition in individuals with mild cognitive impairment: An exploratory study.

Understanding facial emotions is fundamental to interact in social environments and modify behavior accordingly. Neurodegenerative processes can progressively transform affective responses and affect social competence. This exploratory study examined the neurocognitive correlates of face recognition, in individuals with two mild cognitive impairment (MCI) etiologies (prodromal to dementia - MCI, or consequent to Parkinson's disease - PD-MCI). Performance on the identification and memorization of neutral and emotional facial expressions was assessed in 31 individuals with MCI, 26 with PD-MCI, and 30 healthy controls (HC). Individuals with MCI exhibited selective impairment in recognizing faces expressing fear, along with difficulties in remembering both neutral and emotional faces. Conversely, individuals with PD-MCI showed no differences compared with the HC in either emotion recognition or memory. In MCI, no significant association emerged between the memory for facial expressions and cognitive difficulties. In PD-MCI, regression analyses showed significant associations with higher-level cognitive functions in the emotional memory task, suggesting the presence of compensatory mechanisms. In a subset of participants, voxel-based morphometry revealed that the performance on emotional tasks correlated with regional changes in gray matter volume. The performance in the matching of negative expressions was predicted by volumetric changes in brain areas engaged in face and emotional processing, in particular increased volume in thalamic nuclei and atrophy in the right parietal cortex. Future studies should leverage on neuroimaging data to determine whether differences in emotional recognition are mediated by pathology-specific atrophic patterns.

Cortical mechanisms of spatial hearing.

Humans and other animals use spatial hearing to rapidly localize events in the environment. However, neural encoding of sound location is a complex process involving the computation and integration of multiple spatial cues that are not represented directly in the sensory organ (the cochlea). Our understanding of these mechanisms has increased enormously in the past few years. Current research is focused on the contribution of animal models for understanding human spatial audition, the effects of behavioural demands on neural sound location encoding, the emergence of a cue-independent location representation in the auditory cortex, and the relationship between single-source and concurrent location encoding in complex auditory scenes. Furthermore, computational modelling seeks to unravel how neural representations of sound source locations are derived from the complex binaural waveforms of real-life sounds. In this article, we review and integrate the latest insights from neurophysiological, neuroimaging and computational modelling studies of mammalian spatial hearing. We propose that the cortical representation of sound location emerges from recurrent processing taking place in a dynamic, adaptive network of early (primary) and higher-order (posterior-dorsal and dorsolateral prefrontal) auditory regions. This cortical network accommodates changing behavioural requirements and is especially relevant for processing the location of real-life, complex sounds and complex auditory scenes.

Early threat perception is independent of later cognitive and behavioral control. A virtual reality-EEG-ECG study.

Research on social threat has shown influences of various factors, such as agent characteristics, proximity, and social interaction on social threat perception. An important, yet understudied aspect of threat exposure concerns the ability to exert control over the threat and its implications for threat perception. In this study, we used a virtual reality (VR) environment showing an approaching avatar that was either angry (threatening body expression) or neutral (neutral body expression) and informed participants to stop avatars from coming closer under five levels of control success (0, 25, 50, 75, or 100%) when they felt uncomfortable. Behavioral results revealed that social threat triggered faster reactions at a greater virtual distance from the participant than the neutral avatar. Event-related potentials (ERPs) revealed that the angry avatar elicited a larger N170/vertex positive potential (VPP) and a smaller N3 than the neutral avatar. The 100% control condition elicited a larger late positive potential (LPP) than the 75% control condition. In addition, we observed enhanced theta power and accelerated heart rate for the angry avatar vs. neutral avatar, suggesting that these measures index threat perception. Our results indicate that perception of social threat takes place in early to middle cortical processing stages, and control ability is associated with cognitive evaluation in middle to late stages.

A paleo-neurologic investigation of the social brain hypothesis in frontotemporal dementia.

The social brain hypothesis posits that a disproportionate encephalization in primates enabled to adapt behavior to a social context. Also, it has been proposed that phylogenetically recent brain areas are disproportionally affected by neurodegeneration. Using structural and functional magnetic resonance imaging, the present study investigates brain-behavior associations and neural integrity of hyperspecialized and domain-general cortical social brain areas in behavioral variant frontotemporal dementia (bvFTD). The results revealed that both structure and function of hyperspecialized social areas in the middle portion of the superior temporal sulcus (STS) are compromised in bvFTD, while no deterioration was observed in domain general social areas in the posterior STS. While the structural findings adhered to an anterior-posterior gradient, the functional group differences only occurred in the hyperspecialized locations. Activity in specialized regions was associated with structural integrity of the amygdala and with social deficits in bvFTD. In conclusion, the results are in line with the paleo-neurology hypothesis positing that neurodegeneration primarily hits cortical areas showing increased specialization, but also with the compatible alternative explanation that anterior STS regions degenerate earlier, based on stronger connections to and trans-neuronal spreading from regions affected early in bvFTD.

Voxelwise encoding models of body stimuli reveal a representational gradient from low-level visual features to postural features in occipitotemporal cortex.

Previous research on body representation in the brain has focused on category-specific representation, using fMRI to investigate the response pattern to body stimuli in occipitotemporal cortex. But the central question of the specific computations involved in body selective regions has not been addressed so far. This study used ultra-high field fMRI and banded ridge regression to investigate the computational mechanisms of coding body images, by comparing the performance of three encoding models in predicting brain activity in occipitotemporal cortex and specifically in the extrastriate body area (EBA). Our results indicate that bodies are encoded in occipitotemporal cortex and in the EBA according to a combination of low-level visual features and postural features.

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.

Decoding the difference between explicit and implicit body expression representation in high level visual, prefrontal and inferior parietal cortex.

Recent studies provide an increasing understanding of how visual objects categories like faces or bodies are represented in the brain and also raised the question whether a category based or more dynamic network inspired models are more powerful. Two important and so far sidestepped issues in this debate are, first, how major category attributes like the emotional expression directly influence category representation and second, whether category and attribute representation are sensitive to task demands. This study investigated the impact of a crucial category attribute like emotional expression on category area activity and whether this varies with the participants' task. Using (fMRI) we measured BOLD responses while participants viewed whole body expressions and performed either an explicit (emotion) or an implicit (shape) recognition task. Our results based on multivariate methods show that the type of task is the strongest determinant of brain activity and can be decoded in EBA, VLPFC and IPL. Brain activity was higher for the explicit task condition in VLPFC and was not emotion specific. This pattern suggests that during explicit recognition of the body expression, body category representation may be strengthened, and emotion and action related activity suppressed. Taken together these results stress the importance of the task and of the role of category attributes for understanding the functional organization of high level visual cortex.

Computation-Based Feature Representation of Body Expressions in the Human Brain.

Humans and other primate species are experts at recognizing body expressions. To understand the underlying perceptual mechanisms, we computed postural and kinematic features from affective whole-body movement videos and related them to brain processes. Using representational similarity and multivoxel pattern analyses, we showed systematic relations between computation-based body features and brain activity. Our results revealed that postural rather than kinematic features reflect the affective category of the body movements. The feature limb contraction showed a central contribution in fearful body expression perception, differentially represented in action observation, motor preparation, and affect coding regions, including the amygdala. The posterior superior temporal sulcus differentiated fearful from other affective categories using limb contraction rather than kinematics. The extrastriate body area and fusiform body area also showed greater tuning to postural features. The discovery of midlevel body feature encoding in the brain moves affective neuroscience beyond research on high-level emotion representations and provides insights in the perceptual features that possibly drive automatic emotion perception.

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.

Amygdala responds to direct gaze in real but not in computer-generated faces.

Computer-generated (CG) faces are an important visual interface for human-computer interaction in social contexts. Here we investigated whether the human brain processes emotion and gaze similarly in real and carefully matched CG faces. Real faces evoked greater responses in the fusiform face area than CG faces, particularly for fearful expressions. Emotional (angry and fearful) facial expressions evoked similar activations in the amygdala in real and CG faces. Direct as compared with averted gaze elicited greater fMRI responses in the amygdala regardless of facial expression but only for real and not for CG faces. We observed an interaction effect between gaze and emotion (i.e., the shared signal effect) in the right posterior temporal sulcus and other regions, but not in the amygdala, and we found no evidence for different shared signal effects in real and CG faces. Taken together, the present findings highlight similarities (emotional processing in the amygdala) and differences (overall processing in the fusiform face area, gaze processing in the amygdala) in the neural processing of real and CG faces.

Computational Feature Analysis of Body Movements Reveals Hierarchical Brain Organization.

Social species spend considerable time observing the body movements of others to understand their actions, predict their emotions, watch their games, or enjoy their dance movements. Given the important information obtained from body movements, we still know surprisingly little about the details of brain mechanisms underlying movement perception. In this fMRI study, we investigated the relations between movement features obtained from automated computational analyses of video clips and the corresponding brain activity. Our results show that low-level computational features map to specific brain areas related to early visual- and motion-sensitive regions, while mid-level computational features are related to dynamic aspects of posture encoded in occipital-temporal cortex, posterior superior temporal sulcus and superior parietal lobe. Furthermore, behavioral features obtained from subjective ratings correlated with activity in higher action observation regions. Our computational feature-based analysis suggests that the neural mechanism of movement encoding is organized in the brain not so much by semantic categories than by feature statistics of the body movements.

The representation and plasticity of body emotion expression.

Emotions are expressed by the face, the voice and the whole body. Research on the face and the voice has not only demonstrated that emotions are perceived categorically, but that this perception can be manipulated. The purpose of this study was to investigate, via two separate experiments using adaptation and multisensory techniques, whether the perception of body emotion expressions also shows categorical effects and plasticity. We used an approach developed for studies investigating both face and voice emotion perception and created novel morphed affective body stimuli, which varied in small incremental steps between emotions. Participants were instructed to perform an emotion categorisation of these morphed bodies after adaptation to bodies conveying different expressions (Experiment 1), or while simultaneously hearing affective voices (Experiment 2). We show that not only is body expression perceived categorically, but that both adaptation to affective body expressions and concurrent presentation of vocal affective information can shift the categorical boundary between body expressions, specifically for the angry body expressions. Overall, our findings provide significant new insights into emotional body categorisation, which may prove important in gaining a deeper understanding of body expression perception in everyday social situations.

Intact hemisphere and corpus callosum compensate for visuomotor functions after early visual cortex damage.

Unilateral damage to the primary visual cortex (V1) leads to clinical blindness in the opposite visual hemifield, yet nonconscious ability to transform unseen visual input into motor output can be retained, a condition known as "blindsight." Here we combined psychophysics, functional magnetic resonance imaging, and tractography to investigate the functional and structural properties that enable the developing brain to partly overcome the effects of early V1 lesion in one blindsight patient. Visual stimuli appeared in either the intact or blind hemifield and simple responses were given with either the left or right hand, thereby creating conditions where visual input and motor output involve the same or opposite hemisphere. When the V1-damaged hemisphere was challenged by incoming visual stimuli, or controlled manual responses to these unseen stimuli, the corpus callosum (CC) dynamically recruited areas in the visual dorsal stream and premotor cortex of the intact hemisphere to compensate for altered visuomotor functions. These compensatory changes in functional brain activity were paralleled by increased connections in posterior regions of the CC, where fibers connecting homologous areas of the parietal cortex course.

Active Sound Localization Sharpens Spatial Tuning in Human Primary Auditory Cortex.

Spatial hearing sensitivity in humans is dynamic and task-dependent, but the mechanisms in human auditory cortex that enable dynamic sound location encoding remain unclear. Using functional magnetic resonance imaging (fMRI), we assessed how active behavior affects encoding of sound location (azimuth) in primary auditory cortical areas and planum temporale (PT). According to the hierarchical model of auditory processing and cortical functional specialization, PT is implicated in sound location ("where") processing. Yet, our results show that spatial tuning profiles in primary auditory cortical areas (left primary core and right caudo-medial belt) sharpened during a sound localization ("where") task compared with a sound identification ("what") task. In contrast, spatial tuning in PT was sharp but did not vary with task performance. We further applied a population pattern decoder to the measured fMRI activity patterns, which confirmed the task-dependent effects in the left core: sound location estimates from fMRI patterns measured during active sound localization were most accurate. In PT, decoding accuracy was not modulated by task performance. These results indicate that changes of population activity in human primary auditory areas reflect dynamic and task-dependent processing of sound location. As such, our findings suggest that the hierarchical model of auditory processing may need to be revised to include an interaction between primary and functionally specialized areas depending on behavioral requirements.SIGNIFICANCE STATEMENT According to a purely hierarchical view, cortical auditory processing consists of a series of analysis stages from sensory (acoustic) processing in primary auditory cortex to specialized processing in higher-order areas. Posterior-dorsal cortical auditory areas, planum temporale (PT) in humans, are considered to be functionally specialized for spatial processing. However, this model is based mostly on passive listening studies. Our results provide compelling evidence that active behavior (sound localization) sharpens spatial selectivity in primary auditory cortex, whereas spatial tuning in functionally specialized areas (PT) is narrow but task-invariant. These findings suggest that the hierarchical view of cortical functional specialization needs to be extended: our data indicate that active behavior involves feedback projections from higher-order regions to primary auditory cortex.

fMRI-based Multivariate Pattern Analyses Reveal Imagery Modality and Imagery Content Specific Representations in Primary Somatosensory, Motor and Auditory Cortices.

Previous studies have shown that the early visual cortex contains content-specific representations of stimuli during visual imagery, and that these representational patterns of imagery content have a perceptual basis. To date, there is little evidence for the presence of a similar organization in the auditory and tactile domains. Using fMRI-based multivariate pattern analyses we showed that primary somatosensory, auditory, motor, and visual cortices are discriminative for imagery of touch versus sound. In the somatosensory, motor and visual cortices the imagery modality discriminative patterns were similar to perception modality discriminative patterns, suggesting that top-down modulations in these regions rely on similar neural representations as bottom-up perceptual processes. Moreover, we found evidence for content-specific representations of the stimuli during auditory imagery in the primary somatosensory and primary motor cortices. Both the imagined emotions and the imagined identities of the auditory stimuli could be successfully classified in these regions.

Opponent Coding of Sound Location (Azimuth) in Planum Temporale is Robust to Sound-Level Variations.

Coding of sound location in auditory cortex (AC) is only partially understood. Recent electrophysiological research suggests that neurons in mammalian auditory cortex are characterized by broad spatial tuning and a preference for the contralateral hemifield, that is, a nonuniform sampling of sound azimuth. Additionally, spatial selectivity decreases with increasing sound intensity. To accommodate these findings, it has been proposed that sound location is encoded by the integrated activity of neuronal populations with opposite hemifield tuning ("opponent channel model"). In this study, we investigated the validity of such a model in human AC with functional magnetic resonance imaging (fMRI) and a phase-encoding paradigm employing binaural stimuli recorded individually for each participant. In all subjects, we observed preferential fMRI responses to contralateral azimuth positions. Additionally, in most AC locations, spatial tuning was broad and not level invariant. We derived an opponent channel model of the fMRI responses by subtracting the activity of contralaterally tuned regions in bilateral planum temporale. This resulted in accurate decoding of sound azimuth location, which was unaffected by changes in sound level. Our data thus support opponent channel coding as a neural mechanism for representing acoustic azimuth in human AC.

Localization of complex sounds is modulated by behavioral relevance and sound category.

Meaningful sounds represent the majority of sounds that humans hear and process in everyday life. Yet studies of human sound localization mainly use artificial stimuli such as clicks, pure tones, and noise bursts. The present study investigated the influence of behavioral relevance, sound category, and acoustic properties on the localization of complex, meaningful sounds in the horizontal plane. Participants localized vocalizations and traffic sounds with two levels of behavioral relevance (low and high) within each category, as well as amplitude-modulated tones. Results showed a small but significant effect of behavioral relevance: localization acuity was higher for complex sounds with a high level of behavioral relevance at several target locations. The data also showed category-specific effects: localization biases were lower, and localization precision higher, for vocalizations than for traffic sounds in central space. Several acoustic parameters influenced sound localization performance as well. Correcting localization responses for front-back reversals reduced the overall variability across sounds, but behavioral relevance and sound category still had a modulatory effect on sound localization performance in central auditory space. The results thus demonstrate that spatial hearing performance for complex sounds is influenced not only by acoustic characteristics, but also by sound category and behavioral relevance.