Early excitatory and inhibitory modifications in the motor cortex following skill learning support motor memory consolidation and cortical plasticity overnight

Abstract

The learning of new motor skills constitutes an inseparable part of our lives. Motor consolidation refers to the offline processing of motor memories following the acquisition of new motor skills. The animal literature suggests that the primary motor cortex (M1) plays a key role in motor memory consolidation, and structural and functional plasticity in M1 following motor consolidation have been demonstrated. However, the mechanisms supporting motor memory consolidation and plasticity in the human M1 are not well understood. Initial human neuroimaging studies show that the initial stages of motor learning in humans are accompanied by short-term temporal dynamics of the brains main excitatory and inhibitory neurotransmitters - Glutamate (Glu) and GABA - in M1, but it remains unclear how these relate to the question of motor memory consolidation. Here, we show that early Glu and GABA modifications in M1 following motor skill learning may play vital roles in supporting motor memory consolidation and neural plasticity that take place over longer time scales. Using a multimodal magnetic resonance approach implemented on ultra-high field 7T scanner in healthy young adults (n=36), we found increased Glu and decreased GABA in M1 during the initial offline period following learning to support consolidation-related local and inter-regional functions of M1, such as motor memory reactivation and increased functional connectivity with the striatum. These neurochemical changes also correlated with overnight structural and functional plasticity expressed as increased M1 grey matter volume and functional connectivity, while Glu modifications also correlated with adaptive behavior, as reflected by improvements in skill performance. Our results provide intriguing microscale mechanistic evidence to the potential distinctive roles of Glu and GABA in promoting motor memory consolidation and plasticity in the human M1. They also highlight a role for early neurochemical modifications to memory consolidation and plasticity in the human brain and may hold important clinical implications in rehabilitative settings such as in stroke and brain injury.