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

Silvia Mangia,Mauro Dinuzzo,Gisela E Hagberg,Daniele Mascali,Marta Moraschi,Federico Giove

doi:10.7554/elife.71016

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 magnetic resonance imaging (BOLD-fMRI) have markedly different neurometabolic responses as measured by proton functional magnetic resonance spectroscopy (1H-fMRS). 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 other 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.

Highlights

In the brain, sensory stimulation is associated with a substantial increase of regional functional hyperaemia as well as energy metabolism of glucose, the main cerebral energy substrate (Siesjo 1978)
Based on experimental evidence and metabolic modeling, we have previously proposed that the local input-output balance between neuronal synaptic/spiking activity is a primary determinant in the up-regulation of aerobic glycolysis (DiNuzzo and Giove 2012; DiNuzzo et al 2011; DiNuzzo and Nedergaard 2017)
The isoluminant chromatic flickering 408 stimulation at 30 Hz is above the critical flicker fusion (CFF) and we found that the blood-oxygenation level-dependent (BOLD) response in 409 secondary visual areas drops substantially compared with the concurrent BOLD response in V1

Summary

Introduction

Sensory stimulation is associated with a substantial increase of regional functional hyperaemia (i.e. cerebral blood flow, CBF) as well as energy metabolism of glucose, the main cerebral energy substrate (Siesjo 1978). The metabolic response to stimulation includes an oxidative component, as measured by the cerebral metabolic rate of oxygen (CMRO2), and a non-oxidative component, as reflected by lactate accumulation (Mangia et al 2009). Cortical lactate levels have been shown to increase during visual stimulation, simultaneously to the acceleration of the malate-aspartate shuttle, a process termed aerobic glycolysis (i.e. lactate production independent of oxygen availability) (Bednarik et al 2015; Bednarik et al 2018; Boillat et al 2020; Fernandes et al 2020; Lin et al 2010; Lin et al 2012; Mangia et al 2007a; Schaller et al 2013; Schaller et al 2014). The impact of information processing to the metabolic response of the cerebral cortex to sensory stimulation has not been fully investigated far. Nothing is known about the modulatory effect exerted by the perception of different stimuli on regional brain energy metabolism

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Discussion

Conclusion