From thought to action: The brain–machine interface in posterior parietal cortex

Abstract

A dramatic example of translational monkey research is the development of neural prosthetics for assisting paralyzed patients. A neuroprosthesis consists of implanted electrodes that can record the intended movement of a paralyzed part of the body, a computer algorithm that decodes the intended movement, and an assistive device such as a robot limb or computer that is controlled by these intended movement signals. This type of neuroprosthetic system is also referred to as a brain-machine interface (BMI) since it interfaces the brain with an external machine. In this review, we will concentrate on BMIs in which microelectrode recording arrays are implanted in the posterior parietal cortex (PPC), a high-level cortical area in both humans and monkeys that represents intentions to move. This review will first discuss the basic science research performed in healthy monkeys that established PPC as a good source of intention signals. Next, it will describe the first PPC implants in human patients with tetraplegia from spinal cord injury. From these patients the goals of movements could be quickly decoded, and the rich number of action variables found in PPC indicates that it is an appropriate BMI site for a very wide range of neuroprosthetic applications. We will discuss research on learning to use BMIs in monkeys and humans and the advances that are still needed, requiring both monkey and human research to enable BMIs to be readily available in the clinic.posterior parietal cortex | brain-machine interface | monkey | tetraplegia | intention E arly scientific research in motor-related areas of monkey cortex established how intended movements are represented (1). Of particular interest to this paper is the posterior parietal cortex (PPC; Fig. 1), which, through cortical connections, is situated between primary sensory and motor cortical areas and provides a bridge for sensorimotor transformations for sensoryguided movements. In the 1970s, using technology that enabled recording of single neurons from awake, behaving monkeys, the neurophysiology of this area was first explored at the fine grain of the response properties of neurons (2, 3). A variety of sensorimotor properties were found that included sensory-related properties of vision, somatosensation, and attention and movement-related properties including eye movements, fixation, reaching, and hand manipulation of objects. Subsequent studies showed that planningrelated signals are found within PPC, which reflect the intention to move particular body parts (4, 5). The PPC is an area of cortex shared by monkeys and humans and thus monkeys make an ideal animal model for insights into the functions of human PPC.Basic science results from motor cortex (6-10) and PPC (11) of monkeys have been translated into preclinical monkey models of neuroprosthetics. In our studies, approved by the Caltech Institutional Animal Care and Use Committee, monkeys were implanted chronically with microelectrode arrays that recorded the activity of populations of neurons in the PPC (11). In the...

Posterior parietal cortex contributions to cross-modal brain plasticity upon sensory loss

“…It allows the patient to have more control over planned movements. On top of that, the involved PPC sub-regions, like the parietal reach region, have the ability to direct both body sides upon single area stimulation [78,79]. Its capability of partially mixed encoding in which neurons respond to multiple variables only adds to its strength [80,81].…”

“…PPC area 5, the parietal reach region, AIP and LIP, located in the intraparietal sulcus [34, 79,83] or area MMA in mice show the most potential as implant targets [39]. However, just as for sensory type implants, a double approach could lead to the best outcome.…”

“…Adding an implant in the somatosensory cortex, which is connected with touch sensors on the prosthetic device, can foresee in feedback to the PPC related to peripersonal space and body position, enabling a more precise control ( Fig. 4B) [79,[84][85][86]. This is also observed in hemiplegic upper limb paralysis due to stroke, where the amount of somatosensory feedback will contribute to the patients rehabilitation outcome via robot training [87].…”

Neural encoding of actual and imagined touch within human posterior parietal cortex

“…We recorded from on average 101.6 ± 7.2 neurons ( Figure 1—figure supplement 1 ) over 14 sessions in the PPC (left hemisphere) of a tetraplegic human participant (spinal injury at levels 3–4; C3/4). In previous work, we referred to the implant area as the anterior intraparietal cortex, a region functionally defined in NHPs ( Aflalo et al, 2020 , Aflalo et al, 2015 ; Rutishauser et al, 2018 ; Zhang et al, 2017 ; Zhang et al, 2020 ; Andersen et al, 2019 ; Sakellaridi et al, 2019 ). Here, we refer to the recording site as the PC-IP, acknowledging that further work is necessary to definitively characterize homologies between human and NHP anatomy.…”

From basic brain research to treating human brain disorders

“…They trace the course of basic research on monkeys that identified the brain circuits underlying limb movement, and identified the brain location where stimulation should reduce tremor, and did. The next two articles by Kennedy and Schwartz (14) and by Andersen, Aflalo, and Kellis (15) provide dramatic examples, showing how understanding the organization of the monkey brain's control of limb movements led to the development of prosthetic devices that enable paralyzed human patients to control artificial arms with activity from their own brains. This is possible because of the similarity of the functional anatomy of the parts of monkey and human brain that control of limb movement; these structures are strikingly different in rodents.…”