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Neuropsychologia. 2019 May 31;131:9-24. doi: 10.1016/j.neuropsychologia.2019.05.027. [Epub ahead of print]

Human amygdala response to unisensory and multisensory emotion input: No evidence for superadditivity from intracranial recordings.

Author information

1
Department of Clinical Neuroscience, University Hospital of Geneva, Switzerland; Center for Affective Sciences, University of Geneva, Switzerland; Campus Biotech, Geneva, Switzerland. Electronic address: judith.dominguezBorras@unige.ch.
2
Department of Clinical Neuroscience, University Hospital of Geneva, Switzerland; Center for Affective Sciences, University of Geneva, Switzerland; Campus Biotech, Geneva, Switzerland. Electronic address: raphael.guex@unige.ch.
3
Facultad de Psicología, Universidad Autónoma de Madrid, Spain. Electronic address: cmendezbertolo@gmail.com.
4
Campus Biotech, Geneva, Switzerland; Department of Basic Neuroscience, Faculty of Medicine, University of Geneva, Switzerland. Electronic address: guillaume.legendre@unige.ch.
5
Department of Clinical Neuroscience, University Hospital of Geneva, Switzerland. Electronic address: laurent.spinelli@hcuge.ch.
6
Department of Experimental Psychology, Complutense University of Madrid, Spain; Laboratory for Clinical Neuroscience, Centre for Biomedical Technology, Universidad Politécnica de Madrid, Spain. Electronic address: smoratti@psi.ucm.es.
7
Department of Psychology, University of Zurich, Switzerland. Electronic address: sascha.fruehholz@psychologie.uzh.ch.
8
Department of Clinical Neuroscience, University Hospital of Geneva, Switzerland; Department of Basic Neuroscience, Faculty of Medicine, University of Geneva, Switzerland. Electronic address: pierre.megevand@hcuge.ch.
9
Campus Biotech, Geneva, Switzerland; Department of Basic Neuroscience, Faculty of Medicine, University of Geneva, Switzerland. Electronic address: luc.arnal@unige.ch.
10
Laboratory for Clinical Neuroscience, Centre for Biomedical Technology, Universidad Politécnica de Madrid, Spain; Department of Neuroimaging, Alzheimer's Disease Research Centre, Reina Sofia-CIEN Foundation, Madrid, Spain. Electronic address: bryan.strange@upm.es.
11
Department of Clinical Neuroscience, University Hospital of Geneva, Switzerland. Electronic address: margitta.seeck@hcuge.ch.
12
Center for Affective Sciences, University of Geneva, Switzerland; Campus Biotech, Geneva, Switzerland; Department of Basic Neuroscience, Faculty of Medicine, University of Geneva, Switzerland. Electronic address: patrik.vuilleumier@unige.ch.

Abstract

The amygdala is crucially implicated in processing emotional information from various sensory modalities. However, there is dearth of knowledge concerning the integration and relative time-course of its responses across different channels, i.e., for auditory, visual, and audiovisual input. Functional neuroimaging data in humans point to a possible role of this region in the multimodal integration of emotional signals, but direct evidence for anatomical and temporal overlap of unisensory and multisensory-evoked responses in amygdala is still lacking. We recorded event-related potentials (ERPs) and oscillatory activity from 9 amygdalae using intracranial electroencephalography (iEEG) in patients prior to epilepsy surgery, and compared electrophysiological responses to fearful, happy, or neutral stimuli presented either in voices alone, faces alone, or voices and faces simultaneously delivered. Results showed differential amygdala responses to fearful stimuli, in comparison to neutral, reaching significance 100-200 ms post-onset for auditory, visual and audiovisual stimuli. At later latencies, ∼400 ms post-onset, amygdala response to audiovisual information was also amplified in comparison to auditory or visual stimuli alone. Importantly, however, we found no evidence for either super- or subadditivity effects in any of the bimodal responses. These results suggest, first, that emotion processing in amygdala occurs at globally similar early stages of perceptual processing for auditory, visual, and audiovisual inputs; second, that overall larger responses to multisensory information occur at later stages only; and third, that the underlying mechanisms of this multisensory gain may reflect a purely additive response to concomitant visual and auditory inputs. Our findings provide novel insights on emotion processing across the sensory pathways, and their convergence within the limbic system.

KEYWORDS:

Amygdala; Auditory emotion; Intracranial EEG; Local-field potentials; Multisensory processing; Visual emotion

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