Perception is associated with the brain's metabolic response to sensory stimulation

Abstract
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Abstract

Processing of incoming sensory stimulation triggers an increase of cerebral perfusion and blood oxygenation (neurovascular response) as well as an alteration of the metabolic neurochemical profile (neurometabolic response). Here we show in human primary visual cortex (V1) that perceived and unperceived isoluminant chromatic flickering stimuli designed to have similar neurovascular responses as measured by blood oxygenation level dependent functional MRI (BOLD-fMRI) have markedly different neurometabolic responses as measured by functional MRS. In particular, a significant regional buildup of lactate, an index of aerobic glycolysis, and glutamate, an index of malate-aspartate shuttle, occurred in V1 only when the flickering was perceived, without any relation with behavioral or physiological variables. Whereas the BOLD-fMRI signal in V1, a proxy for input to V1, was insensitive to flickering perception by design, the BOLD-fMRI signal in secondary visual areas was larger during perceived than unperceived flickering, indicating increased output from V1. These results demonstrate that the upregulation of energy metabolism induced by visual stimulation depends on the type of information processing taking place in V1, and that 1H-fMRS provides unique information about local input/output balance that is not measured by BOLD fMRI.

Data availability

The study was developed using SPM12 (https://www.fil.ion.ucl.ac.uk/spm/software/spm12/), LCmodel (http://s-provencher.com/lcmodel.shtml), jMRUI (http://www.jmrui.eu/) and AFNI (https://afni.nimh.nih.gov/). Data used for all the figures and for Tables 2-3 is available as source data to each element. Source data include also custom Matlab code for processing related to each figure. The raw data include sensitive data. The raw dataset cannot be made available in a public repository because of constraints originally set by the Ethics Committee and included in the informed consent signed by participants. Raw data that support the findings of this study are available from the corresponding author upon signing a MTA that would include: a list of authorized researchers; a commitment to not disclose the raw data to persons not included in the list; and a commitment to destroy the raw data when legitimate use is finished. Commercial use of the raw data is not permitted.

Article and author information

Author details

Mauro DiNuzzo

Museo Storico della Fisica e Centro Studi e Ricerche Enrico Fermi, Rome, Italy

Competing interests
The authors declare that no competing interests exist.
Silvia Mangia

Center for Magnetic Resonance Research, University of Minnesota, Minneapolis, United States

Competing interests
The authors declare that no competing interests exist.
Marta Moraschi

Department of Radiation Oncology, Campus Bio-Medico University of Rome, Rome, Italy

Competing interests
The authors declare that no competing interests exist.
Daniele Mascali

Dipartimento di Neuroscienze, Università Gabriele D'Annunzio, Chieti, Italy

Competing interests
The authors declare that no competing interests exist.
Gisela E Hagberg

High-Field Magnetic Resonance, Max Planck Institute for Biological Cybernetics and Biomedical Magnetic Resonance, Tübingen, Germany

Competing interests
The authors declare that no competing interests exist.
Federico Giove

Museo Storico della Fisica e Centro Studi e Ricerche Enrico Fermi, Rome, Italy

For correspondence
federico.giove@uniroma1.it

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0002-6934-3146

Funding

Ministero della Salute (Ricerca Corrente)

Federico Giove

Max Planck Institute for Biological Cybernetics (Open Access funding)

Gisela E Hagberg

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Ethics

Human subjects: This study included human subjects and was performed by the authors in compliance with all applicable ethical standards, including the Helsinki declaration and its amendments, institutional/national standards, and international/national/institutional guidelines. The study was approved by the Ethics Committee of Fondazione Santa Lucia (Rome). All subjects gave informed consent before being enrolled in the study.

Copyright

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.