Abstract

Metabolic pathways underlying brain function remain largely unexplored during neurodevelopment, predominantly due to the lack of feasible techniques for use with awake infants. Broadband near-infrared spectroscopy (bNIRS) provides the opportunity to explore the relationship between cerebral energy metabolism and blood oxygenation/haemodynamics through the measurement of changes in the oxidation state of mitochondrial respiratory chain enzyme cytochrome-c-oxidase (ΔoxCCO) alongside haemodynamic changes. We used a bNIRS system to measure ΔoxCCO and haemodynamics during functional activation in a group of 42 typically developing infants aged between 4 and 7 months. bNIRS measurements were made over the right hemisphere over temporal, parietal and central cortical regions, in response to social and non-social visual and auditory stimuli. Both ΔoxCCO and Δ[HbO2] displayed larger activation for the social condition in comparison to the non-social condition. Integration of haemodynamic and metabolic signals revealed networks of stimulus-selective cortical regions that were not apparent from analysis of the individual bNIRS signals. These results provide the first spatially resolved measures of cerebral metabolic activity alongside haemodynamics during functional activation in infants. Measuring synchronised changes in metabolism and haemodynamics have the potential for uncovering the development of cortical specialisation in early infancy.

Highlights

  • Specialisation of function by region is one of the key organising principles of the human brain

  • We report the use of a novel technique, referred to as broadband near-infrared spectroscopy, that allows non-invasive measurement of cellular energy metabolism alongside haemodynamics/oxygenation in awake infants

  • A significant mismatch was observed over the parietal-central area for the non-social condition, where haemodynamic activity appeared to exceed metabolic activity as reflected by negative relative cost (rCST). This is in contrast to the results presented in a previous paper that utilised the same technique with broadband NIRS measurements over the visual cortex in adults (Pinti et al, 2021), where all cortical regions showed coordinated/matched cerebral metabolism and haemodynamic activity

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Summary

Introduction

Specialisation of function by region is one of the key organising principles of the human brain. Indirect evidence suggests that in some cases specialisation emerges gradually over the course of development (Johnson, 2011) Such observations are critical for testing theoretical predictions about the degree to which core principles of brain organisation are present at birth or emerge through experience, and how that process takes place. Regional Neurometabolic Coupling in Infancy of brain activity This technique infers localisation of specific cognitive measures by detecting regional changes in the ratio of oxygenated/deoxygenated haemoglobin ( referred to as blood oxygenation levels). Neural and glial cells detect this demand and as a result produce metabolites that act on blood vessels to produce regionally-specific increases in blood flow and the changes in blood oxygenation levels that are measured by fMRI, in a process referred to as neurovascular coupling (NVC) (Abbott et al, 2006). Techniques are required that allow measurement of different components of the NVC pathway such as metabolism and blood oxygenation in awake infants

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