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Motor Cortex in Voluntary Movements
Section II
Neuronal Representations
in the Motor Cortex
Copyright © 2005 CRC Press LLC
 
3
Motor Cortex Control
of a Complex
Peripheral Apparatus:
The Neuromuscular
Evolution of Individuated
Finger Movements
Marc H. Schieber, Karen T. Reilly, and
Catherine E. Lang
CONTENTS
ABSTRACT
Rather than acting as a somatotopic array of upper motor neurons, each controlling
a single muscle that moves a single finger, neurons in the primary motor cortex (M1)
act as a spatially distributed network of very diverse elements, many of which have
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© 2005 by CRC Press LLC
Copyright © 2005 CRC Press LLC
 
outputs that diverge to facilitate multiple muscles acting on different fingers. More-
over, some finger muscles, because of tendon interconnections and incompletely
subdivided muscle bellies, exert tension simultaneously on multiple digits. Conse-
quently, each digit does not move independently of the others, and additional muscle
contractions must be used to stabilize against unintended motion. This biological
control of a complex peripheral apparatus initially may appear unnecessarily com-
plicated compared to the independent control of digits in a robotic hand, but can be
understood as the result of concurrent evolution of the peripheral neuromuscular
apparatus and its descending control from the motor cortex.
3.1 INTRODUCTION
Unlike a robotic hand that has been designed by human engineers, the primate hand
has evolved from the pectoral fin of a primordial ancestor. What began as intercon-
nected bony rays supporting a fin evolved into a hand with digits capable of relatively
independent motion. During this evolution, the pressures of natural selection con-
currently influenced both the peripheral musculoskeletal apparatus and the central
mechanisms for its neural control. The resulting biological hand, which has reached
its most sophisticated form in primates, especially humans, nevertheless retains many
structural and functional features of the ancestral appendage. To understand how the
motor cortex participates in controlling finger movements, we must appreciate cer-
tain aspects of how the peripheral apparatus of a biological hand works. Here, we
will consider first the motion of the fingers themselves, then the functional organi-
zation of the muscles that move the fingers, and then how M1 controls finger
movements. Because M1 plays a particularly crucial role in controlling fine, indi-
viduated finger movements, we will focus on features that affect the independence
of finger movements.
3.2 THE LIMITED INDEPENDENCE
OF FINGER MOVEMENTS
Modern amphibians and reptiles have forelimbs with distinct digits, but do not use
these digits to grasp objects. Further along the phylogenetic scale, mammals such
as rats and cats can be observed to mold the digits of the forepaw to grasp objects.
1–3
Although nonhuman primates, and especially humans, are clearly capable of more
sophisticated finger movements, the vast majority of what nonhuman primates and
humans do with their fingers consists simply of grasping objects. In grasping, all
the digits are in motion simultaneously. Independently controlling the 15 different
joints of the 5 digits presents a formidable problem for the nervous system, but
analysis suggests that most control of the fingers in grasping could be simplified.
Only 2 principle components — mathematical functions describing simultaneous
motion of the 15 joints in fixed proportion to one another — account for most of
the motion of the 15 joints.
4,5
Copyright © 2005 CRC Press LLC
The first principle component corresponds roughly to
the simultaneous motion of all the joints in the opening and closing of all the digits.
The second principle component corresponds roughly to the degree of flexion of the
fingertips toward the palm or extension of the fingertips away from the palm.
Together, these two principle components account for 84% of the variation in finger
joint positions used by humans in grasping a wide variety of common objects. Most
of the finger movements used in grasping thus could be controlled by scaling just
2 principle components, a process much simpler than independently controlling
15 joints. Whether the nervous system actually employs such a simplifying scheme
to control grasping, and if so, where in the nervous system the scheme is imple-
mented, remains unknown as yet.
Beyond grasping, the fine finger movements used in manipulating small objects,
typing, or playing musical instruments are performed much less frequently. Although
the fingers commonly are assumed to be moving independently during such tasks,
recordings show again that these sophisticated performances entail simultaneous
motion of multiple digits.
6,7
8–11
The crucial role of M1 in controlling fine, individuated movements of the fingers
is evident from the common observation that such movements are the first affected
and the last to recover when lesions affect M1 or its output via the corticospinal
tract.
From this perspective, the
fingers can be hypothesized to have a fundamental level of control that produces
general opening and closing of the hand for grasping.
14
This fundamental control
might be accomplished by rudimentary neuromuscular structures in the periphery
and driven reliably by subcortical centers in the nervous system. As evolution
progressed, a capability for more sophisticated control of the fingers may have
developed on top of this fundamental level. This more sophisticated control required
both subdivision of the peripheral neuromuscular apparatus and evolution of a
computationally more complex layer of control, in which M1 plays a major role.
15
3.2.1 B
IOMECHANICAL
F
ACTORS
The fingers of a robotic hand are mechanically independent, but the fingers of a
biological hand are coupled to a measurable degree by a number of biomechanical
factors. Some degree of mechanical coupling between adjacent digits is produced
by the soft tissues in the web spaces between the fingers. Cutting this tissue in
cadaver hands reduced the extent to which adjacent digits moved along with a
passively moved digit.
16
juncturae tendinium
between
the different finger tendons of
extensor digitorum communis
(EDC) are well known.
17
(FDP) to the four different fingers also
are interconnected in the palm, both by thin sheets of inelastic connective tissue and
by the origins of the lumbrical muscles.
flexor digitorum profundus
In macaque monkeys, these interconnec-
tions between the tendons of multitendoned muscles are more pronounced than in
humans.
18
19
In the macaque FDP, tendon interconnections have been shown to cause
Copyright © 2005 CRC Press LLC
Even when specifically asked to move just one finger,
both nonhuman primates and human subjects show some degree of simultaneous
motion in other, noninstructed digits, whether moving the fingers isotonically, or
applying forces isometrically.
Lesions of the motor cortex, besides rendering movements weak and slow,
reduce the ability to move a given body part without concurrent motion of adjacent
body parts, as illustrated for the fingers in Figure 3.1 .
12,13
Additional coupling is produced by interconnections
between the tendons of certain muscles. In humans, the
The tendons of
Control
Motor cortex lesion
CMC
thumb
PIP
Index
MCP
DP
MIDDLE
ring
little
100
degs
10 sec
Loss of individuation after a motor cortex lesion. In these joint position traces,
a control subject (left column) and a subject with a motor cortex lesion (right column) were
instructed to move the middle finger back and forth while keeping the other fingers still. Joint
position traces from the thumb are on top, followed by the index, middle, ring, and little
(bottom) fingers. The thick lines show metacarpophalangeal (MCP) joint movement, the thin
lines show proximal interphalangeal (PIP) joint movement, and the dotted lines show distal
interphalangeal (DIP) joint movement, except for the thumb, where the dotted line shows
carpometacarpal (CMC) joint movement. Joint position traces for the middle finger show that
both subjects moved the middle finger as instructed. The control subject on the left made
highly individuated movements of the middle finger with minimal changes in joint position
of the noninstructed fingers. In contrast, the subject with a motor cortical lesion (in the
contralateral precentral gyrus hand knob, extending into the white matter beneath) produced
substantial changes in joint position of the index and ring fingers simultaneously with the
middle finger movement.
tension exerted at one point on the proximal aponeurosis of the insertion tendon to
be distributed to the distal insertions on multiple digits.
20
Because of this biomechanical coupling of the digits, muscle activity intended
to move one digit will tend to move adjacent digits as well. To move one digit more
individually then, additional muscles may be activated to check the coupled motion
of the adjacent digits. Such stabilizing contractions have been observed in the
electromyographic (EMG) activity of finger muscles in both monkeys and humans.
As a monkey flexes its little finger, for example,
extensor digiti secundi et tertii
(ED23) contracts to minimize simultaneous flexion of the index and middle fingers.
21
In humans, the portion of FDP that acts chiefly on the middle finger contracts as
the subject extends either the index or the ring finger, apparently to minimize coupled
extension of the middle finger ( Figure 3.2 ) .
22
Additional requirements for stabilizing contractions result from the fact that the
extrinsic finger muscles act across the wrist joint as well. When FDP and/or the
(FDS) contract, for example, they exert torque not only
about the interphalangeal and metacarpophalangeal joints of the fingers, but also
Copyright © 2005 CRC Press LLC
FIGURE 3.1
flexor digitorum superficialis
356521560.001.png

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