BOLD Coherence Reveals Segregated Functional Neural Interactions When Adapting to Distinct Torque Perturbations

Abstract

Tunik E, Schmitt PJ, Grafton ST. BOLD coherence reveals segregated functional neural interactions when adapting to distinct torque perturbations. J Neurophysiol 97: [2107][2108][2109][2110][2111][2112][2113][2114][2115][2116][2117][2118][2119][2120] 2007. First published January 3, 2007; doi:10.1152/jn.00405.2006. In the natural world, we experience and adapt to multiple extrinsic perturbations. This poses a challenge to neural circuits in discriminating between different context-appropriate responses. Using event-related fMRI, we characterized the neural dynamics involved in this process by randomly delivering a position-or velocity-dependent torque perturbation to subjects' arms during a target-capture task. Each perturbation was color-cued during movement preparation to provide contextual information. Although trajectories differed between perturbations, subjects significantly reduced error under both conditions. This was paralleled by reduced BOLD signal in the right dentate nucleus, the left sensorimotor cortex, and the left intraparietal sulcus. Trials included "NoGo" conditions to dissociate activity related to preparation from execution and adaptation. Subsequent analysis identified perturbationspecific neural processes underlying preparation ("NoGo") and adaptation ("Go") early and late into learning. Between-perturbation comparisons of BOLD magnitude revealed negligible differences for both preparation and adaptation trials. However, a network-level analysis of BOLD coherence revealed that by late learning, response preparation ("NoGo") was attributed to a relative focusing of coherence within cortical and basal ganglia networks in both perturbation conditions, demonstrating a common network interaction for establishing arbitrary visuomotor associations. Conversely, late-learning adaptation ("Go") was attributed to a focusing of BOLD coherence between a cortical-basal ganglia network in the viscous condition and between a cortical-cerebellar network in the positional condition. Our findings demonstrate that trial-to-trial acquisition of two distinct adaptive responses is attributed not to anatomically segregated regions, but to differential functional interactions within common sensorimotor circuits. I N T R O D U C T I O NEffective movement necessitates adaptation to perturbations to the sensorimotor system. Whether different neural circuits in the human brain underlie the nervous system's capability to flexibly adapt to various perturbations remains unknown. Although numerous imaging studies have investigated circuits involved in sensorimotor remapping, only a handful have addressed adaptation to torque perturbations. Early positron emission tomography (PET) studies of two-dimensional (2D) reaching under viscous resistance revealed a learning-dependent increase in regional cerebral blood flow (rCBF) to the left dorsolateral prefrontal (DLPFC) cortex and the bilateral putamen that, on retention testing, was reduced in the DLPFC but increased in the left posterior parietal, dorsal premotor, and right a...

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