Corrective responses to limb disturbances are surprisingly complex, but the neural basis of these goal-directed responses is poorly understood. Here we show that somatosensory feedback is transmitted to many sensory and motor cortical regions within 25 ms of a mechanical disturbance applied to the monkey's arm. When limb feedback was salient to an ongoing motor action (task engagement), neurons in parietal area 5 immediately (~25 ms) increased their response to limb disturbances, whereas neurons in other regions did not alter their response until 15 to 40 ms later. In contrast, initiation of a motor action elicited by a limb disturbance (target selection) altered neural responses in primary motor cortex~65 ms after the limb disturbance, and then in dorsal premotor cortex, with no effect in parietal regions until 150 ms post-perturbation. Our findings highlight broad parietofrontal circuits that provide the neural substrate for goal-directed corrections, an essential aspect of highly skilled motor behaviors.

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Standing balance is often threatened in everyday life. These threats typically involve scenarios in which either the likelihood or the consequence of falling is higher than normal. When cats are placed in these scenarios they respond by increasing the sensitivity of muscle spindles imbedded in the leg muscles, presumably to increase balance-relevant afferent information available to the nervous system. At present, it is unknown whether humans also respond to such postural threats by altering muscle spindle sensitivity. Here we present two studies that probed the effects of postural threat on spinal stretch reflexes. In study 1 we manipulated the threat associated with an increased consequence of a fall by having subjects stand at the edge of an elevated surface (3.2 m). In study 2 we manipulated the threat by increasing the likelihood of a fall by occasionally tilting the support surface on which subjects stood. In both scenarios we used Hoffmann (H) and tendon stretch (T) reflexes to probe the spinal stretch reflex circuit of the soleus muscle. We observed increased T-reflex amplitudes and unchanged H-reflex amplitudes in both threat scenarios. These results suggest that the synaptic state of the spinal stretch reflex is unaffected by postural threat and that therefore the muscle spindles activated in the T-reflexes must be more sensitive in the threatening conditions. We propose that this increase in sensitivity may function to satisfy the conflicting needs to restrict movement with threat, while maintaining a certain amount of sensory information related to postural control.

Corrective responses to external perturbations are sensitive to the behavioral task being performed. It is believed that primary motor cortex (M1) forms part of a transcortical pathway that contributes to this sensitivity. Previous work has identified two distinct phases in the perturbation response of M1 neurons, an initial response starting ∼20 ms after perturbation onset that does not depend on the intended motor action and a task-dependent response that begins ∼40 ms after perturbation onset. However, this invariant initial response may reflect ongoing postural control or a task-independent response to the perturbation. The present study tested these two possibilities by examining if being engaged in an ongoing postural task before perturbation onset modulated the initial perturbation response in M1. Specifically, mechanical perturbations were applied to the shoulder and/or elbow while the monkey maintained its hand at a central target or when it was watching a movie and not required to respond to the perturbation. As expected, corrective movements, muscle stretch responses, and M1 population activity in the late perturbation epoch were all significantly diminished in the movie task. Strikingly, initial perturbation responses (<40 ms postperturbation) remained the same across tasks, suggesting that the initial phase of M1 activity constitutes a task-independent response that is sensitive to the properties of the mechanical perturbation but not the goal of the ongoing motor task.

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