Abstract

The brain retains a lifelong ability to adapt through learning and in response to injury or disease-related damage, a process known as functional neuroplasticity. The neural energetics underlying functional brain plasticity have not been thoroughly investigated experimentally in the healthy human brain. A better understanding of the blood flow and metabolic changes that accompany motor skill acquisition, and which facilitate plasticity, is needed before subsequent translation to treatment interventions for recovery of function in disease. The aim of the current study was to characterize cerebral blood flow (CBF) and oxygen consumption (relative CMRO2) responses, using calibrated fMRI conducted in 20 healthy participants, during performance of a serial reaction time task which induces rapid motor adaptation. Regions of interest (ROIs) were defined from areas showing task-induced BOLD and CBF responses that decreased over time. BOLD, CBF and relative CMRO2 responses were calculated for each block of the task. Motor and somatosensory cortices and the cerebellum showed statistically significant positive responses to the task compared to baseline, but with decreasing amplitudes of BOLD, CBF, and CMRO2 response as the task progressed. In the cerebellum, there was a sustained positive BOLD response in the absence of a significant CMRO2 increase from baseline, for all but the first task blocks. This suggests that the brain may continue to elevate the supply energy even after CMRO2 has returned to near baseline levels. Relying on BOLD fMRI data alone in studies of plasticity may not reveal the nature of underlying metabolic responses and their changes over time. Calibrated fMRI approaches may offer a more complete picture of the energetic changes supporting plasticity and learning.

Highlights

  • The brain retains a lifelong ability to adapt through learning and in response to injury or disease-related damage, a process known as functional neuroplasticity

  • As CMRO2 and neuronal firing are closely coupled (Mathiesen et al, 1998; Martindale et al, 2003), a decreased neural response with age is a possible explanation for these results. Such changes in vascular reserve and neurovascular coupling (NVC) would not have been revealed by BOLD fMRI alone, and the results demonstrate the value of calibrated fMRI in studies where cerebral energetics may be altered by experimental conditions or over time

  • The results showed that there was a significant effect of time on performance; response accuracy improved over time; F(2.2, 38.3) = 12.47, p < 0.001

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Summary

Introduction

The brain retains a lifelong ability to adapt through learning and in response to injury or disease-related damage, a process known as functional neuroplasticity. Residual neuroplasticity in chronic diseases such as Multiple Sclerosis (MS), or following stroke, can be harnessed in rehabilitation strategies to promote recovery of function. The neuronal and vascular mechanisms underlying plasticity are not fully understood. Adequate energy delivery in the form of cerebral blood flow (CBF), which carries oxygen, glucose and other nutrients to tissue, is essential for healthy neuronal function, as is the capacity to metabolize these substrates. The neural energetics underlying functional brain plasticity have not been thoroughly investigated experimentally in the healthy human brain. A better understanding of the blood flow and metabolism changes which occur during motor skill acquisition, and which facilitate plasticity, is needed before characterization in disease, and subsequent translation to inform treatment interventions to maintain or recover function

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