Distributed task-specific processing of somatosensory feedback for voluntary motor control

Abstract

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.

Somatosensory Cortex Plays an Essential Role in Forelimb Motor Adaptation in Mice

“…Second, it is also possible that the CNS learned to ignore sensory feedback due to reduced fidelity in somatosensory feedback signals caused by S1 photoinhibition. Consistent with the former possibility, S1 neurons rapidly respond to unexpected perturbations to a forelimb movement (Fromm and Evarts, 1982; Omrani et al, 2016) and respond differently to externally versus self-generated touching (Blakemore et al, 1999). Although the question of whether these signals encode sensory prediction errors, and if they specifically drive motor adaptation remains to be examined.…”

“…It is, therefore, unclear whether one particular pathway plays a predominant role in motor adaptation. S1 receives feedback from the limb during reaching movements (Hikosaka et al, 1985; Omrani et al, 2016) and projects to important motor control centers such as motor cortex (Petrof et al, 2015) and via brainstem to cerebellum (Bower et al, 1981)—both areas that display rapid responses to S1 stimulation (Brown and Bower, 2002; Petrof et al, 2015). To test the role of S1 during adaptation, we transiently photoinhibited the forelimb area of S1 during movements.…”

“…While much attention has been paid to the cerebellum in motor adaptation (Diedrichsen et al, 2005; Gao et al, 1996; Proville et al, 2014; Smith and Shadmehr, 2005; Tseng et al, 2007; Wolpert et al, 1998), there has been less focus on cortical contributions, despite evidence that cortex responds rapidly after the onset of perturbations (Krebs et al, 1998; Omrani et al, 2016). Interestingly, several studies have suggested that primary somatosensory cortex (S1) may have a role in motor learning (Krebs et al, 1998; Pavlides et al, 1993; Vidoni et al, 2010), yet a causal role of S1 in motor adaptation has not been demonstrated.…”

Motor Cortex Embeds Muscle-like Commands in an Untangled Population Response

“…Indeed, conclusively discriminating between the two areas typically requires assessing microstimulation thresholds. We also note that both motor cortex and S1 exhibit strong proprioceptive responses, both project to spinal interneuron and motor-neuron populations 4 , and both are believed to contribute to feedback control 61 . It is thus a priori unclear whether to expect S1 trajectories to show high or low tangling.…”

Motor Cortical Visuomotor Feedback Activity Is Initially Isolated from Downstream Targets in Output-Null Neural State Space Dimensions

“…A variant of this it-is-solved-upstream possibility is that the necessary computations happen via dendritic processing at the motor cortical inputs (Mel, 1994). Arguing against this are studies showing that initial motor cortical spiking responses to mechanical arm perturbations are non-specific to the perturbation and behavioral context, and differ from subsequent correction-specific responses (Herter et al, 2008; Omrani et al, 2014, 2016, Pruszynski et al, 2011, 2014). Furthermore, the motor cortical data we will present show that initial responses to visual perturbations are inappropriate for generating corrections.…”