Convergent BOLD and Beta-Band Activity in Superior Temporal Sulcus and Frontolimbic Circuitry Underpins Human Emotion Cognition.
The processing of social information in the human brain is widely distributed neuroanatomically and finely orchestrated over time. However, a detailed account of the spatiotemporal organization of these key neural underpinnings of human social cognition remains to be elucidated. Here, we applied functional magnetic resonance imaging (fMRI) and magnetoencephalography (MEG) in the same participants to investigate spatial and temporal neural patterns evoked by viewing videos of facial muscle configurations. We show that observing the emergence of expressions elicits sustained blood oxygenation level-dependent responses in the superior temporal sulcus (STS), a region implicated in processing meaningful biological motion. We also found corresponding event-related changes in sustained MEG beta-band (14-30 Hz) oscillatory activity in the STS, consistent with the possible role of beta-band activity in visual perception. Dynamically evolving fearful and happy expressions elicited early (0-400 ms) transient beta-band activity in sensorimotor cortex that persisted beyond 400 ms, at which time it became accompanied by a frontolimbic spread (400-1000 ms). In addition, individual differences in sustained STS beta-band activity correlated with speed of emotion recognition, substantiating the behavioral relevance of these signals. This STS beta-band activity showed valence-specific coupling with the time courses of facial movements as they emerged into full-blown fearful and happy expressions (negative and positive coupling, respectively). These data offer new insights into the perceptual relevance and orchestrated function of the STS and interconnected pathways in social-emotion cognition.
Section on Integrative Neuroimaging Clinical Brain Disorders Branch.
Mbemba
M
Jabbi
Section on Integrative Neuroimaging Clinical Brain Disorders Branch.
Philip D
PD
Kohn
Section on Integrative Neuroimaging Clinical Brain Disorders Branch.
Tiffany
T
Nash
Section on Integrative Neuroimaging Clinical Brain Disorders Branch.
Angela
A
Ianni
Section on Integrative Neuroimaging Clinical Brain Disorders Branch.
Christopher
C
Coutlee
MEG Core Facility, National Institute of Mental Health, Intramural Research Program, National Institutes of Health, Bethesda, MD 20892, USA.
Tom
T
Holroyd
MEG Core Facility, National Institute of Mental Health, Intramural Research Program, National Institutes of Health, Bethesda, MD 20892, USA.
Frederick W
FW
Carver
Clinical Brain Disorders Branch.
Qiang
Q
Chen
Section on Integrative Neuroimaging Clinical Brain Disorders Branch.
Brett
B
Cropp
Section on Integrative Neuroimaging Clinical Brain Disorders Branch.
J Shane
JS
Kippenhan
MEG Core Facility, National Institute of Mental Health, Intramural Research Program, National Institutes of Health, Bethesda, MD 20892, USA.
Stephen E
SE
Robinson
Clinical Brain Disorders Branch MEG Core Facility, National Institute of Mental Health, Intramural Research Program, National Institutes of Health, Bethesda, MD 20892, USA.
Richard
R
Coppola
Section on Integrative Neuroimaging Clinical Brain Disorders Branch.
Karen F
KF
Berman
D000328:Adult; D001611:Beta Rhythm / Q000502:physiology; D001931:Brain Mapping; D002560:Cerebrovascular Circulation / Q000502:physiology; D003071:Cognition / Q000502:physiology*; D004644:Emotions / Q000502:physiology*; D005071:Evoked Potentials; D000066499:Facial Recognition / Q000502:physiology*; D005260:Female; D005625:Frontal Lobe / Q000502:physiology*; D006801:Humans; D008032:Limbic System / Q000502:physiology*; D008279:Magnetic Resonance Imaging; D015225:Magnetoencephalography; D008297:Male; D009434:Neural Pathways / Q000502:physiology; D009483:Neuropsychological Tests; D010100:Oxygen / Q000097:blood; D010775:Photic Stimulation; D011930:Reaction Time / Q000502:physiology; D013702:Temporal Lobe / Q000502:physiology*
D010100:Oxygen
STS; coupling; emotion; neural; transient