Distributed affective space represents multiple emotion categories across the human brain

Abstract

The functional organization of human emotion systems as well as their neuroanatomical basis and segregation in the brain remains unresolved. Here, we used pattern classification and hierarchical clustering to characterize the organization of a wide array of emotion categories in the human brain. We induced 14 emotions (6 ‘basic’, e.g. fear and anger; and 8 ‘non-basic’, e.g. shame and gratitude) and a neutral state using guided mental imagery while participants' brain activity was measured with functional magnetic resonance imaging (fMRI). Twelve out of 14 emotions could be reliably classified from the haemodynamic signals. All emotions engaged a multitude of brain areas, primarily in midline cortices including anterior and posterior cingulate gyri and precuneus, in subcortical regions, and in motor regions including cerebellum and premotor cortex. Similarity of subjective emotional experiences was associated with similarity of the corresponding neural activation patterns. We conclude that different basic and non-basic emotions have distinguishable neural bases characterized by specific, distributed activation patterns in widespread cortical and subcortical circuits. Regionally differentiated engagement of these circuits defines the unique neural activity pattern and the corresponding subjective feeling associated with each emotion.

Distinct medial-temporal lobe mechanisms of encoding and amygdala-mediated memory reinstatement for disgust and fear

“…Although disgust and fear modulated memory of unitized associations through partly distinct neural mechanisms, we do not imply that there exist separate neural substrates for basic emotion categories, which has long been debated [68][69][70] . Rather, our study was designed to determine whether, and how, encoding and reinstatement of verbal associations may be differently modulated by disgust and fear regardless of overall negative valence and arousal.…”

Multivariate fMRI pattern analysis of fear perception across modalities

“…For instance, Saarmäki and colleagues demonstrated above‐chance classification accuracies for 12 emotions in response to guided mental imagery. Most notably, contributions from regions in the insula, supplementary motor area, and subcortical structures were identified in discriminating four negative emotions including fear from neutral (Saarimäki et al., ). Additionally, activity within‐ and across‐subjects in response to five emotions, as induced through movies was accurately classified above chance for all emotions, with contributions from parietal and frontal midline regions, and in particular, from the insula and amygdala for fear (Saarimäki et al., ).…”

Emotionotopy in the Human Right Temporo-Parietal Cortex

“…To obtain moment-by-moment emotion ratings during the Forrest Gump movie, we enrolled 12 healthy Italian native speakers (5F; mean age 26.6 years, range [24][25][26][27][28][29][30][31][32][33][34]. None of them reported to have watched the movie in one year period prior to the experiment.…”

“…However, despite this large body of evidence, it remains to be determined whether emotional experiences are better described through discrete basic emotions or emotion dimensions. Moreover, regardless of the adopted model, it is still debated how emotion features are spatially encoded in the brain 8,11,13,[30][31][32] . As a matter of fact, while findings support the role of distinct regions 7 , others indicate the recruitment of distributed networks in relation to specific affective states 33 .…”