Kim Kwang S, Hinkley Leighton B, Brent Kurtis, Gaines Jessica L, Pongos Alvincé L, Gupta Saloni, Dale Corby L, Nagarajan Srikantan S, Houde John F
Department of Speech, Language, and Hearing Sciences, Purdue University, West Lafayette, IN, USA.
Department of Radiology and Biomedical Imaging, University of California San Francisco, San Francisco, CA, USA.
J Neurosci. 2025 May 27. doi: 10.1523/JNEUROSCI.2084-24.2025.
The human sensorimotor system has a remarkable ability to learn movements from sensory experience. A prominent example is sensorimotor adaptation, learning that characterizes the sensorimotor system's response to persistent sensory errors by adjusting future movements to compensate for those errors. A component of sensorimotor adaptation is implicit (i.e., the learner is unaware of the learning) which has been suggested to result from sensory prediction errors-discrepancies between predicted sensory consequences of motor commands and actual sensory feedback. However, neurophysiological evidence that sensory prediction errors drive adaptation has never been directly demonstrated. Here, we examined prediction errors via magnetoencephalography imaging of the auditory cortex during sensorimotor adaptation of speech to altered auditory feedback, an entirely implicit adaptation task. Specifically, we measured how speaking-induced suppression (SIS)-a neural representation of auditory prediction errors-changed over the trials of the adaptation experiment. In both male and female speakers, reduction in SIS (reflecting larger prediction errors) during the early learning phase compared to the initial unaltered feedback phase positively correlated with behavioral adaptation extents, suggesting that larger prediction errors were associated with more learning. In contrast, such a reduction in SIS was not found in a control experiment in which participants heard unaltered feedback and thus did not adapt. In addition, in some participants who reached a plateau in the late learning phase, SIS increased, demonstrating that prediction errors were minimal when there was no further adaptation. Together, these findings provide the first direct neurophysiological evidence for the hypothesis that prediction errors drive sensorimotor adaptation. This work investigates mechanisms of sensorimotor adaptation, the phenomenon of motor learning due to exposure to altered sensory feedback. Models of motor control have hypothesized that sensorimotor adaptation is driven by sensory prediction errors - the discrepancy between predicted and actual sensory feedback. Here, we provide for the first time direct neurophysiological evidence that speech sensorimotor adaptation is indeed driven by sensory prediction errors using magnetoencephalography (MEG) imaging of auditory cortex during speaking.
人类感觉运动系统具有从感官体验中学习运动的非凡能力。一个突出的例子是感觉运动适应，这种学习通过调整未来的运动以补偿这些误差来表征感觉运动系统对持续感觉误差的反应。感觉运动适应的一个组成部分是内隐的（即学习者没有意识到学习），有人认为这是由感觉预测误差导致的——运动指令的预测感觉结果与实际感觉反馈之间的差异。然而，感觉预测误差驱动适应的神经生理学证据从未得到直接证明。在这里，我们在将语音感觉运动适应于改变的听觉反馈（一项完全内隐的适应任务）的过程中，通过对听觉皮层进行脑磁图成像来检查预测误差。具体来说，我们测量了在适应实验的各个试验中，说话诱发抑制（SIS）——听觉预测误差的一种神经表征——是如何变化的。在男性和女性说话者中，与最初未改变的反馈阶段相比，早期学习阶段SIS的降低（反映出更大的预测误差）与行为适应程度呈正相关，这表明更大的预测误差与更多的学习相关。相比之下，在一个对照实验中未发现SIS有这样的降低，在该对照实验中参与者听到的是未改变的反馈，因此没有适应。此外，在一些在学习后期达到平稳期的参与者中，SIS增加了，这表明当没有进一步适应时，预测误差最小。总之，这些发现为预测误差驱动感觉运动适应这一假设提供了首个直接的神经生理学证据。这项工作研究了感觉运动适应的机制，即由于暴露于改变的感觉反馈而导致的运动学习现象。运动控制模型假设感觉运动适应是由感觉预测误差驱动的——预测和实际感觉反馈之间的差异。在这里，我们首次提供了直接的神经生理学证据，证明在说话过程中使用听觉皮层的脑磁图（MEG）成像，语音感觉运动适应确实是由感觉预测误差驱动的。
