Closed-loop decoder adaptation shapes neural plasticity for skillful neuroprosthetic control.

Neuroplasticity may play a critical role in developing robust, naturally controlled neuroprostheses. This learning, however, is sensitive to system changes such as the neural activity used for control. The ultimate utility of neuroplasticity in real-world neuroprostheses is thus unclear. Adaptive decoding methods hold promise for improving neuroprosthetic performance in nonstationary systems. Here, we explore the use of decoder adaptation to shape neuroplasticity in two scenarios relevant for real-world neuroprostheses: nonstationary recordings of neural activity and changes in control context. Nonhuman primates learned to control a cursor to perform a reaching task using semistationary neural activity in two contexts: with and without simultaneous arm movements. Decoder adaptation was used to improve initial performance and compensate for changes in neural recordings. We show that beneficial neuroplasticity can occur alongside decoder adaptation, yielding performance improvements, skill retention, and resistance to interference from native motor networks. These results highlight the utility of neuroplasticity for real-world neuroprostheses.

Chronic, wireless recordings of large-scale brain activity in freely moving rhesus monkeys.

Advances in techniques for recording large-scale brain activity contribute to both the elucidation of neurophysiological principles and the development of brain-machine interfaces (BMIs). Here we describe a neurophysiological paradigm for performing tethered and wireless large-scale recordings based on movable volumetric three-dimensional (3D) multielectrode implants. This approach allowed us to isolate up to 1,800 neurons (units) per animal and simultaneously record the extracellular activity of close to 500 cortical neurons, distributed across multiple cortical areas, in freely behaving rhesus monkeys. The method is expandable, in principle, to thousands of simultaneously recorded channels. It also allows increased recording longevity (5 consecutive years) and recording of a broad range of behaviors, such as social interactions, and BMI paradigms in freely moving primates. We propose that wireless large-scale recordings could have a profound impact on basic primate neurophysiology research while providing a framework for the development and testing of clinically relevant neuroprostheses.

Reversible large-scale modification of cortical networks during neuroprosthetic control.

Brain-machine interfaces (BMIs) provide a framework for studying cortical dynamics and the neural correlates of learning. Neuroprosthetic control has been associated with tuning changes in specific neurons directly projecting to the BMI (hereafter referred to as direct neurons). However, little is known about the larger network dynamics. By monitoring ensembles of neurons that were either causally linked to BMI control or indirectly involved, we found that proficient neuroprosthetic control is associated with large-scale modifications to the cortical network in macaque monkeys. Specifically, there were changes in the preferred direction of both direct and indirect neurons. Notably, with learning, there was a relative decrease in the net modulation of indirect neural activity in comparison with direct activity. These widespread differential changes in the direct and indirect population activity were markedly stable from one day to the next and readily coexisted with the long-standing cortical network for upper limb control. Thus, the process of learning BMI control is associated with differential modification of neural populations based on their specific relation to movement control.

Cortical representation of ipsilateral arm movements in monkey and man.

A fundamental organizational principle of the primate motor system is cortical control of contralateral limb movements. Motor areas also appear to play a role in the control of ipsilateral limb movements. Several studies in monkeys have shown that individual neurons in primary motor cortex (M1) may represent, on average, the direction of movements of the ipsilateral arm. Given the increasing body of evidence demonstrating that neural ensembles can reliably represent information with a high temporal resolution, here we characterize the distributed neural representation of ipsilateral upper limb kinematics in both monkey and man. In two macaque monkeys trained to perform center-out reaching movements, we found that the ensemble spiking activity in M1 could continuously represent ipsilateral limb position. Interestingly, this representation was more correlated with joint angles than hand position. Using bilateral electromyography recordings, we excluded the possibility that postural or mirror movements could exclusively account for these findings. In addition, linear methods could decode limb position from cortical field potentials in both monkeys. We also found that M1 spiking activity could control a biomimetic brain-machine interface reflecting ipsilateral kinematics. Finally, we recorded cortical field potentials from three human subjects and also consistently found evidence of a neural representation for ipsilateral movement parameters. Together, our results demonstrate the presence of a high-fidelity neural representation for ipsilateral movement and illustrates that it can be successfully incorporated into a brain-machine interface.

Upward transtentorial herniation, hydrocephalus, and cerebellar edema in hypertensive encephalopathy.

BACKGROUND: Edema of the cerebellum with secondary obstructive hydrocephalus is a rare presentation of hypertensive encephalopathy. The authors report an unusual case of isolated posterior fossa swelling with upward transtentorial herniation and hydrocephalus causing neurologic deterioration. These patients are often initially evaluated by a neurologist because of the acute neurologic symptoms. Prompt diagnosis with aggressive blood pressure control may obviate the need for emergent cerebrospinal fluid (CSF) diversion. REVIEW SUMMARY: This is a case report of a 26-year-old man who presented to the emergency room with confusion and somnolence over a 2-day period. His initial blood pressure was 175/110 mmHg. On examination he was disoriented, with a Glasgow Coma Scale score of 12 points, opening his eyes only to loud verbal stimuli, verbalizing inappropriately, and he was only able to follow simple commands. Neuroimaging revealed edema of the cerebellar folia with noncommunicating hydrocephalus and upward transtentorial herniation. Differential diagnoses of posterior fossa tumor, rhombencephalitis, and hypertensive encephalopathy were entertained. A thorough literature review is included with the discussion of this case. The patient underwent emergent ventriculostomy for CSF drainage and prompt blood pressure control with nitroprusside. After 48 hours of CSF drainage and correction of his hypertension, his neurologic examination normalized. Repeat imaging revealed near resolution of the obstructive hydrocephalus and cerebellar edema. CONCLUSION: Isolated edema of the cerebellum with upward transtentorial herniation and obstructive hydrocephalus is a rare presentation of hypertensive encephalopathy and should be considered in patients with an acute hypertensive crisis and mental status changes. This entity responds to prompt blood pressure control; however, emergent ventriculostomy by a neurosurgical team should be entertained for neurologic deterioration secondary to significant obstructive hydrocephalus, as illustrated in this case.

Learning to control a brain-machine interface for reaching and grasping by primates.

Reaching and grasping in primates depend on the coordination of neural activity in large frontoparietal ensembles. Here we demonstrate that primates can learn to reach and grasp virtual objects by controlling a robot arm through a closed-loop brain-machine interface (BMIc) that uses multiple mathematical models to extract several motor parameters (i.e., hand position, velocity, gripping force, and the EMGs of multiple arm muscles) from the electrical activity of frontoparietal neuronal ensembles. As single neurons typically contribute to the encoding of several motor parameters, we observed that high BMIc accuracy required recording from large neuronal ensembles. Continuous BMIc operation by monkeys led to significant improvements in both model predictions and behavioral performance. Using visual feedback, monkeys succeeded in producing robot reach-and-grasp movements even when their arms did not move. Learning to operate the BMIc was paralleled by functional reorganization in multiple cortical areas, suggesting that the dynamic properties of the BMIc were incorporated into motor and sensory cortical representations.