Towards hippocampal navigation for brain-computer interfaces.

Automatic wheelchairs directly controlled by brain activity could provide autonomy to severely paralyzed individuals. Current approaches mostly rely on non-invasive measures of brain activity and translate individual commands into wheelchair movements. For example, an imagined movement of the right hand would steer the wheelchair to the right. No research has investigated decoding higher-order cognitive processes to accomplish wheelchair control. We envision an invasive neural prosthetic that could provide input for wheelchair control by decoding navigational intent from hippocampal signals. Navigation has been extensively investigated in hippocampal recordings, but not for the development of neural prostheses. Here we show that it is possible to train a decoder to classify virtual-movement speeds from hippocampal signals recorded during a virtual-navigation task. These results represent the first step toward exploring the feasibility of an invasive hippocampal BCI for wheelchair control.

Real-time synthesis of imagined speech processes from minimally invasive recordings of neural activity.

Speech neuroprosthetics aim to provide a natural communication channel to individuals who are unable to speak due to physical or neurological impairments. Real-time synthesis of acoustic speech directly from measured neural activity could enable natural conversations and notably improve quality of life, particularly for individuals who have severely limited means of communication. Recent advances in decoding approaches have led to high quality reconstructions of acoustic speech from invasively measured neural activity. However, most prior research utilizes data collected during open-loop experiments of articulated speech, which might not directly translate to imagined speech processes. Here, we present an approach that synthesizes audible speech in real-time for both imagined and whispered speech conditions. Using a participant implanted with stereotactic depth electrodes, we were able to reliably generate audible speech in real-time. The decoding models rely predominately on frontal activity suggesting that speech processes have similar representations when vocalized, whispered, or imagined. While reconstructed audio is not yet intelligible, our real-time synthesis approach represents an essential step towards investigating how patients will learn to operate a closed-loop speech neuroprosthesis based on imagined speech.

Embedded adaptive deep brain stimulation for cervical dystonia controlled by motor cortex theta oscillations.

Dystonia is a disabling movement disorder characterized by excessive muscle contraction for which the underlying pathophysiology is incompletely understood and treatment interventions limited in efficacy. Here we utilize a novel, sensing-enabled, deep brain stimulator device, implanted in a patient with cervical dystonia, to record local field potentials from chronically implanted electrodes in the sensorimotor cortex and subthalamic nuclei bilaterally. This rechargeable device was able to record large volumes of neural data at home, in the naturalistic environment, during unconstrained activity. We confirmed the presence of theta (3-7 Hz) oscillatory activity, which was coherent throughout the cortico-subthalamic circuit and specifically suppressed by high-frequency stimulation. Stimulation also reduced the duration, rate and height of theta bursts. These findings motivated a proof-of-principle trial of a new form of adaptive deep brain stimulation - triggered by theta-burst activity recorded from the motor cortex. This facilitated increased peak stimulation amplitudes without induction of dyskinesias and demonstrated improved blinded clinical ratings compared to continuous DBS, despite reduced total electrical energy delivered. These results further strengthen the pathophysiological role of low frequency (theta) oscillations in dystonia and demonstrate the potential for novel adaptive stimulation strategies linked to cortico-basal theta bursts.

Musical Hallucinations in Chronic Pain: The Anterior Cingulate Cortex Regulates Internally Generated Percepts.

The anterior cingulate cortex (ACC) has been extensively implicated in the functional brain network underlying chronic pain. Electrical stimulation of the ACC has been proposed as a therapy for refractory chronic pain, although, mechanisms of therapeutic action are still unclear. As stimulation of the ACC has been reported to produce many different behavioral and perceptual responses, this region likely plays a varied role in sensory and emotional integration as well as modulating internally generated perceptual states. In this case series, we report the emergence of subjective musical hallucinations (MH) after electrical stimulation of the ACC in two patients with refractory chronic pain. In an N-of-1 analysis from one patient, we identified neural activity (local field potentials) that distinguish MH from both the non-MH condition and during a task involving music listening. Music hallucinations were associated with reduced alpha band activity and increased gamma band activity in the ACC. Listening to similar music was associated with different changes in ACC alpha and gamma power, extending prior results that internally generated perceptual phenomena are supported by circuits in the ACC. We discuss these findings in the context of phantom perceptual phenomena and posit a framework whereby chronic pain may be interpreted as a persistent internally generated percept.

Cross-Sensory Stimuli Modulate Reactions to Aversive Sounds.

We propose that cross-sensory stimuli presenting a positive attributable source of an aversive sound can modulate negative reactions to the sound. In Experiment 1, participants rated original video sources (OVS) of eight aversive sounds (e.g., nails scratching a chalkboard) as more aversive than eight positive attributable video sources (PAVS) of those same sounds (e.g., someone playing a flute) when these videos were presented silently. In Experiment 2, new participants were presented with those eight aversive sounds in three blocks. In Blocks 1 and 3, the sounds were presented alone; in Block 2, four of the sounds were randomly presented concurrently with their corresponding OVS videos, and the other four with their corresponding PAVS videos. Participants rated each sound, presented with or without video, on three scales: discomfort, unpleasantness, and bodily sensations. We found the concurrent presentation of videos robustly modulates participants' reactions to the sounds: compared to the sounds alone (Block 1), concurrent presentation of PAVS videos significantly reduced negative reactions to the sounds, and the concurrent presentation of OVS videos significantly increased negative reactions, across all three scales. These effects, however, did not linger into Block 3 when the sounds were presented alone again. Our results provide novel evidence that negative reactions to aversive sounds can be modulated through cross-sensory temporal syncing with a positive attributable video source. Although this research was conducted with a neurotypical population, we argue that our findings have implications for the treatment of misophonia.