Neuronal Correlates of Memory Formation in Motor Cortex after Adaptation to Force Field

Abstract

Activity of single neurons in the motor cortex has been shown to change during acquisition of motor skills. We previously reported that the combined activity of cell ensembles in the motor cortex of monkeys (Macaca fascicularis) evolves during adaptation to a novel force field perturbation to encode the direction of compensatory force when reaching to visual targets. We also showed that the population directional signal was altered by the available sensory feedback. Here, we examined whether traces of such activity would linger on to later constitute motor memories of the newly acquired skill and whether memory traces would differ depending on feedback. We found that motor-cortical cell ensembles retained features of their adaptive activity pattern in the absence of perturbation when reaching to both learned and unlearned targets. Moreover, the preferred directions of these cells rotated in the direction of force field while the entire population of cells produced no net rotation of preferred direction when returning to null-field reaches. Whereas the activity pattern and preferred direction rotations were comparable with and without visual feedback, changes in tuning amplitudes differed across feedback conditions. Last, savings in behavioral performance and neuronal activity during later reexposure to force field were apparent. Overall, the findings reflect a novel representation of motor memory by cell ensembles and indicate a putative role of the motor cortex in early acquisition of motor memory.

The Neuronal Basis of Long-Term Sensorimotor Learning

“…Comparisons of directional tuning and the resulting PDs in the three reference frames indicated that, during learning, neuronal activity was always consistent with the force-vector reference frame (Kalaska et al, 1989) but not with target or hand reference frames (Fig. 6 A, B) in which the PDs seemed to shift with forcefield direction as shown previously (Li et al, 2001;Arce et al, 2010b). When perturbation was removed, we observed apparent PD shifts on the population level in the opposite direction, as found in these previous studies.…”

Modulation Dynamics in the Orofacial Sensorimotor Cortex during Motor Skill Acquisition

“…Over a short time-scale, fluctuations in the daily behavioral performance correlated with the proportions of task- modulated MIo and SIo neurons; the more neurons were engaged in the task, the higher the success rates. These rapid fluctuations in the pool size of task-related neurons are consistent with the increased tongue representation occurring within an hour of tongue-task training in humans (Svensson et al, 2006;Arima et al, 2011). We would argue that the nonmonotonic fluctuations in success rate within a session do not signify periods of learning and unlearning but reflect the engagement of a learning process that results in monotonic improvements over days.…”

“…Specifically, the orofacial primary motor cortex (MIo) and somatosensory cortex (SIo) exhibit neuroplasticity related to acquisition of novel oromotor skills, intraoral manipulations, and pain (Murray et al, 1991;Lin et al, 1993;Svensson et al, 2003Svensson et al, , 2006Sessle et al, 2005Sessle et al, , 2007AviviArber et al, 2010AviviArber et al, , 2011Arima et al, 2011). Its dysfunction has been implicated in many orofacial sensorimotor disorders affecting feeding and speech found in stroke and Parkinsonism.…”

“…The current literature is conflicted as to the motor cortex's involvement in short-term and long-term learning (Kleim et al, 2004;Arima et al, 2011;Richardson et al, 2012), and the role of the somatosensory cortex at different stages of learning is poorly understood. Moreover, it remains unknown how learninginduced changes differ between the motor and sensory cortices in general and between MIo and SIo in particular.…”

Gain Field Encoding of the Kinematics of Both Arms in the Internal Model Enables Flexible Bimanual Action

“…Previous neurophysiological findings on the role of neurons in motor areas for motor learning also imply that the encoding of opposite-arm kinematics is very likely. Many neurons in the contralateral primary motor cortex (MI) are load sensitive (Evarts, 1968;Kalaska et al, 1989), and this load sensitivity emerges during motor learning (Gandolfo et al, 2000;Li et al, 2001;Arce et al, 2010). The neurons of the supplementary motor area (PadoaSchioppa et al, 2002(PadoaSchioppa et al, , 2004 and the premotor area (Xiao et al, 2006) of the contralateral hemisphere are also involved in the adaptation to novel loads.…”