Sleep sharpens sensory stimulus coding in human visual cortex after fear conditioning

Virginie Sterpenich; Camille Piguet; Martin Desseilles; Leonardo Ceravolo; Markus Gschwind; Dimitri Van De Ville; Patrik Vuilleumier; Sophie Schwartz

doi:10.1016/j.neuroimage.2014.06.003

Sleep sharpens sensory stimulus coding in human visual cortex after fear conditioning

Neuroimage. 2014 Oct 15:100:608-18. doi: 10.1016/j.neuroimage.2014.06.003. Epub 2014 Jun 14.

Authors

Virginie Sterpenich¹, Camille Piguet², Martin Desseilles³, Leonardo Ceravolo⁴, Markus Gschwind⁵, Dimitri Van De Ville⁶, Patrik Vuilleumier¹, Sophie Schwartz⁷

Affiliations

¹ Department of Neuroscience, Faculty of Medicine, University of Geneva, Switzerland; Swiss Center for Affective Sciences, University of Geneva, Switzerland; Geneva Neuroscience Center, University of Geneva, Switzerland.
² Department of Neuroscience, Faculty of Medicine, University of Geneva, Switzerland; Geneva Neuroscience Center, University of Geneva, Switzerland.
³ Department of Neuroscience, Faculty of Medicine, University of Geneva, Switzerland; Geneva Neuroscience Center, University of Geneva, Switzerland; Department of Psychology, University of Namur, Belgium.
⁴ Swiss Center for Affective Sciences, University of Geneva, Switzerland.
⁵ Department of Neuroscience, Faculty of Medicine, University of Geneva, Switzerland; Neurology Service, Department of Clinical Neurosciences, Centre Hospitalier Universitaire Vaudois (CHUV), Lausanne, Switzerland.
⁶ Geneva Neuroscience Center, University of Geneva, Switzerland; Department of Radiology and Medical Informatics, University of Geneva, Switzerland; Institute of Bioengineering, Ecole Polytechnique Fédérale de Lausanne, Switzerland.
⁷ Department of Neuroscience, Faculty of Medicine, University of Geneva, Switzerland; Swiss Center for Affective Sciences, University of Geneva, Switzerland; Geneva Neuroscience Center, University of Geneva, Switzerland. Electronic address: Sophie.Schwartz@unige.ch.

PMID: 24936680
DOI: 10.1016/j.neuroimage.2014.06.003

Abstract

Efficient perceptual identification of emotionally-relevant stimuli requires optimized neural coding. Because sleep contributes to neural plasticity mechanisms, we asked whether the perceptual representation of emotionally-relevant stimuli within sensory cortices is modified after a period of sleep. We show combined effects of sleep and aversive conditioning on subsequent discrimination of face identity information, with parallel plasticity in the amygdala and visual cortex. After one night of sleep (but neither immediately nor after an equal waking interval), a fear-conditioned face was better detected when morphed with another identity. This behavioral change was accompanied by increased selectivity of the amygdala and face-responsive fusiform regions. Overnight neural changes can thus sharpen the representation of threat-related stimuli in cortical sensory areas, in order to improve detection in impoverished or ambiguous situations. These findings reveal an important role of sleep in shaping cortical selectivity to emotionally-relevant cues and thus promoting adaptive responses to new dangers.

Keywords: Amygdala; Conditioning; Emotion; Functional MRI; Fusiform cortex; Memory consolidation; Perceptual learning; Sleep.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Adult
Amygdala / physiology*
Cerebral Cortex / physiology*
Conditioning, Classical / physiology*
Discrimination, Psychological / physiology
Face*
Fear / physiology*
Female
Functional Neuroimaging
Humans
Magnetic Resonance Imaging
Male
Neuronal Plasticity / physiology*
Random Allocation
Sleep / physiology*
Visual Cortex
Young Adult