Temporal specificity of the initial adaptive response in motor adaptation

Repeated exposure to a novel physical environment eventually leads to a mature adaptive response whereby feedforward changes in motor output mirror both the amplitude and temporal structure of the environmental perturbations. However, adaptive responses at the earliest stages of learning have been found to be not only smaller, but systematically less specific in their temporal structure compared to later stages of learning. This observation has spawned a lively debate as to whether the temporal structure of the initial adaptive response is, in fact, stereotyped and non-specific. To settle this debate, we directly measured the adaptive responses to velocity-dependent and position-dependent force-field perturbations (vFFs and pFFs) at the earliest possible stage of motor learning in humans–after just a single-movement exposure. In line with previous work, we found these earliest stage adaptive responses to be more similar than the perturbations that induced them. However, the single-trial adaptive responses for vFF and pFF perturbations were clearly distinct, and the disparity between them reflected the difference between the temporal structure of the perturbations that drove them. Critically, we observed these differences between single-trial adaptive responses when vFF and pFF perturbations were randomly intermingled from one trial to the next within the same block, indicating perturbation response specificity at the single trial level. These findings demonstrate that the initial adaptive responses to physical perturbations are not stereotyped. Instead, the neural plasticity in sensorimotor areas is sensitive to the temporal structure of a movement perturbation even at the earliest stage in learning. This insight has direct implications for the development of computational models of early-stage motor adaptation and the evolution of this adaptive response with continued training.Author summary: With repeated exposure to a perturbation, the sensorimotor system learns to develop an adaptive response that is highly specific to both the amplitude and temporal structure of that perturbation in order to effectively counteract it. It is widely known that the amplitude of the adaptive response starts small and gradually grows to the right size with repeated exposure. However, it is also the case that the temporal structure of the adaptive response starts somewhat generically and gradually grows into the right shape with repeated exposure. A key question is whether the adaptive response to a perturbation begins with a stereotyped temporal structure that only becomes specified with further practice, or if it begins with a degree of specificity for the experienced perturbation that need only to be refined by practice. Here, by precisely measuring the temporal pattern of motor output in the single-trial adaptive response to two different perturbations, we show that the initial adaptive response is indeed specific to the temporal characteristics of the perturbation, even when the disturbance randomly changed from one trial to the next. These results demonstrate that the sensorimotor system is sensitive to the temporal features of a disturbance, even when experienced just once.