Representation of Whole-body Navigation in the Primary Sensorimotor and Premotor Cortex

Nicolelis, Miguel A L

Yin, Allen

2019-04-02T16:27:04Z

2019-04-02T16:27:04Z

2018

Biomedical Engineering

Traditionally, brain-machine interfaces (BMI) recorded from neurons in cerebral

cortical regions associated with voluntary motor control including primary motor

(M1), primary somatosensory (S1), and dorsal premotor (PMd) cortices. Wheelchair

BMI where users’ desired velocity commands are decoded from these cortical neu-

rons can be used to restored mobility for the severely paralyzed. In addition,

spatial information in these areas during navigation can potentially can incorpo-

rated to bolster BMI performance. However, the study of spatial representation

and navigation in the brain has traditionally been centered on the hippocampal

structures and the parietal cortex, with the majority of the studies conducted in

rodents. Under this classical model, S1, M1, and PMd would not contain allocen-

tric spatial information. In this dissertation I show that a significant number of

neurons in these brain areras do indeed represent body position and orientation

in space during brain-controlled wheelchair navigation.

First, I describe the design and implementation of the first intracortical BMI

for continuous wheelchair navigation. Two rhesus monkeys were chronically im-

planted with multichannel microelectrode arrays that allowed wireless recordings

from ensembles of premotor and sensorimotor cortical neurons. While monkeys

remained seated in the robotic wheelchair, passive navigation was employed to

train a linear decoder to extract wheelchair velocity from cortical activity. Next,

monkeys employed the wireless BMI to translate their cortical activity into the

ivwheelchair’s translational and rotational velocities. Over time, monkeys improved

their ability to navigate the wheelchair toward the location of a grape reward. The

presence of a cortical representation of the distance to reward location was also

detected during the wheelchair BMI operation. These resutls demonstrate that

intracranial BMIs have the potential to restore whole-body mobility to paralyzed

patients.

Second, building upon the finding of cortical representation of the distance

to reward location, I found that during wheelchair BMI navigation the discharge

rates of M1, S1, and PMd neurons correlated with the two-dimensional (2D) room

position and the direction of the wheelchair and the monkey head. The activities

of these cells were phenomenologically similar to place cells and head direction

(HD) cells found in rat hippocampus and entorhinal cortices. I observed 44.6%

and 33.3% of neurons encoding room position in the two monkeys, respectively,

and the overlapping populations of 41.0% and 16.0% neurons encoding head di-

rection. These observations suggest that primary sensorimotor and premotor cor-

tical areas in primates are likely involved in allocentrically representing body po-

sition in space during whole-body navigation, which is an unexpected finding

given the classical model of spatial processing that attributes the representation of

allocentric space to the hippocampal formations.

Finally, I found that allocentric representation of body position in space was

not clear during passive wheelchair navigation. Two rhesus monkeys were pas-

sively transported in an experimental space with different reward locations while

neuronal ensemble activities from M1 and PMd were recorded wirelessly. The ac-

tivities of the recorded cells did not clearly represent the position and direction

of the wheelchair. These results suggest active navigation might be a prerequisite

for primary sensorimotor and PMd participation in the allocentric representation

of space.

In summary, dorsal premotor and primary sensorimotor cortical correlates of

body position and orientation in space were found in rhesus monkeys during

the operation of an intracortical wheelchair BMI for navigation. These findings

contradict the classical dichotomy of localized spatial processing, support a dis-

tributed model of spatial processing in the primate brain, and suggest both con-

text and species differences are important in neural processing. The incorporation

of the allocentric spatial information present in these cortical areas during brain-

controlled wheelchair navigation can potentially improve future BMI navigation

performance.

https://hdl.handle.net/10161/18221

Neurosciences

Biomedical engineering

BMI

Motor cortex

Place cells

Premotor cortex

Primates

Spatial navigation

Representation of Whole-body Navigation in the Primary Sensorimotor and Premotor Cortex

Dissertation