Perception affects the brain’s metabolic response to sensory stimulation

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 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) in primary visual cortex (V1) 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 is perceived, without any relation with behavioral or physiological variables. Wheras 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 indicate 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.

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“…The cerebral metabolic rate of oxygen can be used to measure oxidative phosphorylation of ATP, and a nonoxidative component, aerobic glycolysis, is reflected by lactate accumulation (Fox et al, 1988). DiNuzzo et al reported that stimulus perception affects the lactate and glutamate response in the primary visual cortex in a 3T-fMRS study (DiNuzzo et al, 2022). Further, an fMRS study suggesting habituation of neuronal firing showed that the BOLD response was preserved while the lactate accumulation was reduced over time during repeated photic stimulation (Mangia, Tkac, Logothetis, et al, 2007).…”

“…Further, an fMRS study suggesting habituation of neuronal firing showed that the BOLD response was preserved while the lactate accumulation was reduced over time during repeated photic stimulation (Mangia, Tkac, Logothetis, et al, 2007). For lactate analysis, we screened participants with CRLB of lactate < 35% (DiNuzzo et al, 2022).…”

“…Seven of the metabolites met the CRLB criterion: NAA, NAAG, mI, glutamate, Glx, tCho, and tCr. The threshold CRLB was set at 35% for lactate (DiNuzzo et al, 2022). Among the participants included in the Glx analysis, 24 in the AIC group and 27 in the mPFC group met the criterion for lactate analysis.…”

“…Interestingly, recent studies with 1 H-functional magnetic resonance spectroscopy (fMRS) showed the change of glutamate and/or lactate concentration during cognitive tasks such as the emotional Stroop task (Yoo et al, 2022) and visual perception (DiNuzzo et al, 2022). Lactate is a biological indicator of energy metabolism and is produced through aerobic glycolysis, responsible for 30-40% of the brain's energy metabolism (Mangia et al, 2009).…”