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

• Published in: Journal of neurophysiology 2007-03, Vol.97 (3), p.2107-2120
• Main Authors: Tunik, Eugene, Schmitt, Paul J, Grafton, Scott T
• Format: Article
• Language: English
• Subjects: Adaptation, Physiological - physiology; Adult; Analysis of Variance; Brain Mapping; Cerebral Cortex - blood supply; Cerebral Cortex - physiology; Female; Humans; Image Processing, Computer-Assisted - methods; Magnetic Resonance Imaging - methods; Male; Oxygen - blood; Posture - physiology; Psychomotor Performance - physiology; Torque
• ISSN: 0022-3077; 1522-1598
• DOI: 10.1152/jn.00405.2006

1 Department of Psychological and Brain Sciences, Center for Cognitive Neuroscience, Dartmouth College, Hanover, New Hampshire; 2 Department of Physical Therapy, Steinhardt School of Education, New York University, New York, New York; and 3 Department of Psychology, Sage Center for the Study of the Mind, University of California–Santa Barbara, Santa Barbara, California Submitted 17 April 2006; accepted in final form 15 December 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 perturbation-specific 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. Address for reprint requests and other correspondence: S. T. Grafton, Department of Psychology, Sage Center for the Study of th