Emergence of a stable cortical map for neuroprosthetic control.

Cortical control of neuroprosthetic devices is known to require neuronal adaptations. It remains unclear whether a stable cortical representation for prosthetic function can be stored and recalled in a manner that mimics our natural recall of motor skills. Especially in light of the mixed evidence for a stationary neuron-behavior relationship in cortical motor areas, understanding this relationship during long-term neuroprosthetic control can elucidate principles of neural plasticity as well as improve prosthetic function. Here, we paired stable recordings from ensembles of primary motor cortex neurons in macaque monkeys with a constant decoder that transforms neural activity to prosthetic movements. Proficient control was closely linked to the emergence of a surprisingly stable pattern of ensemble activity, indicating that the motor cortex can consolidate a neural representation for prosthetic control in the presence of a constant decoder. The importance of such a cortical map was evident in that small perturbations to either the size of the neural ensemble or to the decoder could reversibly disrupt function. Moreover, once a cortical map became consolidated, a second map could be learned and stored. Thus, long-term use of a neuroprosthetic device is associated with the formation of a cortical map for prosthetic function that is stable across time, readily recalled, resistant to interference, and resembles a putative memory engram

Local and system mechanisms for action execution and observation in parietal and premotor cortices

The action observation network (AON) includes a system of brain areas largely shared with action execution in both human and nonhuman primates. Yet temporal and tuning specificities of distinct areas and of physiologically identified neuronal classes in the encoding of self and others’ action remain unknown. We recorded the activity of 355 single units from three crucial nodes of the AON, the anterior intraparietal area (AIP), and premotor areas F5 and F6, while monkeys performed a Go/No-Go grasping task and observed an experimenter performing it. At the system level, during task execution, F6 displays a prevalence of suppressed neurons and signals whether an action has to be performed, whereas AIP and F5 share a prevalence of facilitated neurons and remarkable target selectivity; during task observation, F5 stands out for its unique prevalence of facilitated neurons and its stronger and earlier modulation than AIP and F6. By applying unsupervised clustering of spike waveforms, we found distinct cell classes unevenly distributed across areas, with different firing properties and carrying specific visuomotor signals. Broadly spiking neurons exhibited a balanced amount of facilitated and suppressed activity during action execution and observation, whereas narrower spiking neurons showed more mutually facilitated responses during the execution of one's own and others’ action, particularly in areas AIP and F5. Our findings elucidate the time course of activity and firing properties of neurons in the AON during one's own and others’ action, from the system level of anatomically distinct areas to the local level of physiologically distinct cell classes

Local and system mechanisms for action execution and observation in parietal and premotor cortices

The action observation network (AON) includes a system of brain areas largely shared with action execution in both human and nonhuman primates. Yet temporal and tuning specificities of distinct areas and of physiologically identified neuronal classes in the encoding of self and others’ action remain unknown. We recorded the activity of 355 single units from three crucial nodes of the AON, the anterior intraparietal area (AIP), and premotor areas F5 and F6, while monkeys performed a Go/No-Go grasping task and observed an experimenter performing it. At the system level, during task execution, F6 displays a prevalence of suppressed neurons and signals whether an action has to be performed, whereas AIP and F5 share a prevalence of facilitated neurons and remarkable target selectivity; during task observation, F5 stands out for its unique prevalence of facilitated neurons and its stronger and earlier modulation than AIP and F6. By applying unsupervised clustering of spike waveforms, we found distinct cell classes unevenly distributed across areas, with different firing properties and carrying specific visuomotor signals. Broadly spiking neurons exhibited a balanced amount of facilitated and suppressed activity during action execution and observation, whereas narrower spiking neurons showed more mutually facilitated responses during the execution of one’s own and others’ action, particularly in areas AIP and F5. Our findings elucidate the time course of activity and firing properties of neurons in the AON during one’s own and others’ action, from the system level of anatomically distinct areas to the local level of physiologically distinct cell classes

Mirror Activity in the Macaque Motor System

Mirror neurons (MirNs) within ventral premotor cortex (PMv) and primary motor cortex (M1), including pyramidal tract neurons (PTNs) projecting to the spinal cord, modulate their activity during both the execution and observation of motor acts. However, movement is not produced in the latter condition, and mirror responses cannot be explained by lowlevel muscle activity. Relatively reduced activity in M1 during observation may help to suppress movement. Here, we examined the extent to which activity at different stages of action observation reflects grasp representation and suppression of movement across multiple levels of the mirror system in monkeys and humans. We recorded MirNs in M1 and F5 (rostral PMv), including identified PTNs, in two macaque monkeys as they performed, observed, and withheld reach-to-grasp actions. Time-varying population activity was more distinct between execution and observation in M1 than in F5, and M1 activity in the lead-up to the observation of movement onset shared parallels with movement withholding activity. In separate experiments, modulation of short-latency responses evoked in hand muscles by pyramidal tract stimulation revealed modest grasp-specific facilitation at the spinal level during grasp observation. This contrasted with a relative suppression of excitability prior to observed movement onset or when monkeys simply withheld movement. Additional cortical recording experiments examined how contextual factors, such as observing to imitate, observing while engaged in action, or observation with reduced visual information, modulated mirror activity in M1 and F5. Finally, single-pulse transcranial magnetic stimulation (TMS) in healthy human volunteers was used to examine changes in corticospinal excitability (CSE) during action observation and withholding. Overall, the results reveal distinctions in the profile of mirror activity across premotor and motor areas. While F5 maintains a more abstract representation of grasp independent of the acting agent, a balance of excitation and inhibition in motor cortex and spinal circuitry during action observation may support a flexible dissociation between initiation of grasping actions and representation of observed grasp

Forward estimation of movement state in posterior parietal cortex

During goal-directed movements, primates are able to rapidly and accurately control an online trajectory despite substantial delay times incurred in the sensorimotor control loop. To address the problem of large delays, it has been proposed that the brain uses an internal forward model of the arm to estimate current and upcoming states of a movement, which are more useful for rapid online control. To study online control mechanisms in the posterior parietal cortex (PPC), we recorded from single neurons while monkeys performed a joystick task. Neurons encoded the static target direction and the dynamic movement angle of the cursor. The dynamic encoding properties of many movement angle neurons reflected a forward estimate of the state of the cursor that is neither directly available from passive sensory feedback nor compatible with outgoing motor commands and is consistent with PPC serving as a forward model for online sensorimotor control. In addition, we found that the space–time tuning functions of these neurons were largely separable in the angle–time plane, suggesting that they mostly encode straight and approximately instantaneous trajectories