Amygdala response to emotional stimuli without awareness:Facts and Interpretations

Over the past two decades, evidence has accumulated that the human amygdala exerts some of its functions also when the observer is not aware of the content, or even presence, of the triggering emotional stimulus. Nevertheless, there is as of yet no consensus on the limits and conditions that affect the extent of amygdalas response without focused attention or awareness. Here we review past and recent studies on this subject, examining neuroimaging literature on healthy participants as well as brain-damaged patients, and we comment on their strengths and limits. We propose a theoretical distinction between processes involved in attentional unawareness, wherein the stimulus is potentially accessible to enter visual awareness but fails to do so because attention is diverted, and in sensory unawareness, wherein the stimulus fails to enter awareness because its normal processing in the visual cortex is suppressed. We argue this distinction, along with data sampling amygdala responses with high temporal resolution, helps to appreciate the multiplicity of functional and anatomical mechanisms centered on the amygdala and supporting its role in non-conscious emotion processing. Separate, but interacting, networks relay visual information to the amygdala exploiting different computational properties of subcortical and cortical routes, thereby supporting amygdala functions at different stages of emotion processing. This view reconciles some apparent contradictions in the literature, as well as seemingly contrasting proposals, such as the dual stage and the dual route model. We conclude that evidence in favor of the amygdala response without awareness is solid, albeit this response originates from different functional mechanisms and is driven by more complex neural networks than commonly assumed. Acknowledging the complexity of such mechanisms can foster new insights on the varieties of amygdala functions without awareness and their impact on human behavior

Basic emotions in human neuroscience:Neuroimaging and beyond

The existence of so-called ‘basic emotions’ and their defining attributes represents a long lasting and yet unsettled issue in psychology. Recently, neuroimaging evidence, especially related to the advent of neuroimaging meta-analytic methods, has revitalized this debate in the endeavor of systems and human neuroscience. The core theme focuses on the existence of unique neural bases that are specific and characteristic for each instance of basic emotion. Here we review this evidence, outlining contradictory findings, strengths and limits of different approaches. Constructionism dismisses the existence of dedicated neural structures for basic emotions, considering that the assumption of a one-to-one relationship between neural structures and their functions is central to basic emotion theories. While these critiques are useful to pinpoint current limitations of basic emotions theories, we argue that they do not always appear equally generative in fostering new testable accounts on how the brain relates to affective functions. We then consider evidence beyond PET and fMRI, including results concerning the relation between basic emotions and awareness and data from neuropsychology on patients with focal brain damage. Evidence from lesion studies are indeed particularly informative, as they are able to bring correlational evidence typical of neuroimaging studies to causation, thereby characterizing which brain structures are necessary for, rather than simply related to, basic emotion processing. These other studies shed light on attributes often ascribed to basic emotions, such as automaticity of perception, quick onset, and brief duration. Overall, we consider that evidence in favor of the neurobiological underpinnings of basic emotions outweighs dismissive approaches. In fact, the concept of basic emotions can still be fruitful, if updated to current neurobiological knowledge that overcomes traditional one-to-one localization of functions in the brain. In particular, we propose that the structure-function relationship between brain and emotions is better described in terms of pluripotentiality, which refers to the fact that one neural structure can fulfill multiple functions, depending on the functional network and pattern of co-activations displayed at any given moment

Temporal and spatial neural dynamics in the perception of basic emotions from complex scenes

The different temporal dynamics of emotions are critical to understand their evolutionary role in the regulation of interactions with the surrounding environment. Here, we investigated the temporal dynamics underlying the perception of four basic emotions from complex scenes varying in valence and arousal (fear, disgust, happiness and sadness) with the millisecond time resolution of Electroencephalography (EEG). Event-related potentials were computed and each emotion showed a specific temporal profile, as revealed by distinct time segments of significant differences from the neutral scenes. Fear perception elicited significant activity at the earliest time segments, followed by disgust, happiness and sadness. Moreover, fear, disgust and happiness were characterized by two time segments of significant activity, whereas sadness showed only one long-latency time segment of activity. Multidimensional scaling was used to assess the correspondence between neural temporal dynamics and the subjective experience elicited by the four emotions in a subsequent behavioral task. We found a high coherence between these two classes of data, indicating that psychological categories defining emotions have a close correspondence at the brain level in terms of neural temporal dynamics. Finally, we localized the brain regions of time-dependent activity for each emotion and time segment with the low-resolution brain electromagnetic tomography. Fear and disgust showed widely distributed activations, predominantly in the right hemisphere. Happiness activated a number of areas mostly in the left hemisphere, whereas sadness showed a limited number of active areas at late latency. The present findings indicate that the neural signature of basic emotions can emerge as the byproduct of dynamic spatiotemporal brain networks as investigated with millisecond-range resolution, rather than in time-independent areas involved uniquely in the processing one specific emotion. Keywords: basic emotions, EEG, LORETA, ERP, IAPS, time, rapid perceptio

Emotional Voice and Emotional Body Postures Influence Each Other Independently of Visual Awareness

Multisensory integration may occur independently of visual attention as previously shown with compound face-voice stimuli. We investigated in two experiments whether the perception of whole body expressions and the perception of voices influence each other when observers are not aware of seeing the bodily expression. In the first experiment participants categorized masked happy and angry bodily expressions while ignoring congruent or incongruent emotional voices. The onset between target and mask varied from −50 to +133 ms. Results show that the congruency between the emotion in the voice and the bodily expressions influences audiovisual perception independently of the visibility of the stimuli. In the second experiment participants categorized the emotional voices combined with masked bodily expressions as fearful or happy. This experiment showed that bodily expressions presented outside visual awareness still influence prosody perception. Our experiments show that audiovisual integration between bodily expressions and affective prosody can take place outside and independent of visual awareness