Browsing by Author "Yin, Allen"
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Item Open Access Representation of Whole-body Navigation in the Primary Sensorimotor and Premotor Cortex(2018) Yin, AllenTraditionally, 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.