References
9.
1. Dart,
C., and
tassium
current
2.
coronary
Deussen,
endothelial
Arch.
406: 608-614,
1986.
D. K., M. Kessler,
and S. K. Knauff.
blood
flow
and oxygen
supply
Regulation
in skeletal
Land.
role
and
543-594,
7. Marshall,
J. M., J. Lloyd,
and R. Mian.
The
vasopressin
on the arterioles
and venules
muscle
of the rat during
systemic
hypoxia.
Lond.
470: 473-484,
1993.
8. Marshall,
J. M., and J. D. Metcalfe.
vascular
changes
induced
in the
systemic
hypoxia.
/. Physiol.
407:
10.
Mian,
T.
Thomas,
muscle
vasodilatation
Lond.
R., and
individual
J. M.
arterioles
during
and
T.
ATP-sensitive
J. Physiol.
Turner.
in the
1-9,
Marshall.
rat
link
potas-
in systemic
1993.
Responses
venules
hypoxia.
A
K+ channels,
472:
and
systemic
of the
of
in
/.
cardio1994.
12.
13.
R.,
and
14.
observed
of rat skeletal
/. Physiol.
M.
venules
of rat skeletal
Lond.
436:
Lond.
muscle
in
muscle
436:
R., and
J. M. Marshall.
responses
induced
485-
in systemic
Mian,
Marshall,
K+ and
vasodilation
hypoxia.
Ralevic,
R.,
The
and
Regulation
of
Vascular
G. M. Rubanyi.
New
R. M.
J.
of adenosine
and
venules
Berne,
the
Interactions
Tone,
York:
J. G.
Lond.
in determining
rat by systemic
endothelial
and
in
of rat
J. Physiol.
75: 407-410,
1990.
and G. Burnstock.
from
adenosine
production
Am. J. Physiol.
225:
catand
hypoxia.
P. Kumar.
substances
and
role
hypoxia.
adrenoreceptors
induced
in
Exp. Physiol.
V., J. Lincoln,
U.S. Ryan
p. 297-328.
Rubio,
p2
of
arterioles
1991.
in arterioles
skeletal
muscle
493:499-511,1991.
roles
in
by systemic
499-510,
dilator
R., J. M.
The
evoked
Mian,
EndotheliaI,
1988.
Marshall.
responses
Physiol.
vasoactive
15.
J.
in
between
muscle
influence
of
of skeletal
/. Physiol.
385-403,
Mian,
echolamines
Analysis
of the cardiorat by graded
levels of
Lond.
and
hypoxia.
11.
system
in the cardiovascular
response
hypoxia
in the anesthetized
rat with PacO,,
(Abstract).
/. physiol.
Land. 452: 319, 1992.
Lond.
470: 463-472,
1993.
J. M. Peripheral
chemoreceptors
regulation.
Physiol.
Rev. 74:
sium
420:
Louwerse,
A. M., and J. M. Marshall.
The
role
vasopressin
in the regional
vascular
responses
evoked
the spontaneously
breathing
rat by systemic
hypoxia.
Physiol.
6, Marshall,
vascular
J. M.,
adenosine,
497,1991.
muscle
in dogs during
hypoxemia.
/. physiol.
431-446,
1990.
Louwerse,
A. M., and J. M. Marshall.
The
renin-angiotensin
to systemic
maintained
5.
popig
from
artery.
/. physio/.
Land.
46: 767-786,
1993.
A., G. Moser,
and j. Schrader.
Contribution
of
cells
to cardiac
adenosine
production.
Pf/uegers
3. Harrison,
of capillary
4.
N. B. Standen.
Adenosine-activated
in smooth
muscle
cells isolated
Marshall,
between
of
cells.
In:
edited
Dekker,
Dobson.
in cardiac
and
938-953,
1973.
Release
skeletal
by
1992,
Sites
of
muscle.
The Size Pri
After AlI These Years
Timothy
C. Cope and Martin
J. Pinter
Orderly
recruitment
of motor
units is viewed
by many
as a fundamental
motor
control
strategy.
The size principle
is an idea that attempts
to explain
how orderly
recruitment
operates.
Does the size principle
work?
We
summarize
how the size principle
came about, consider
its mechanisms,
and probe its limits.
T
wo observations
have intrigued
scientists
interested
in movement
and the neuromuscular system. One is the specialization
of motor
units, each composed
of an a-motoneuron
and
the skeletal muscle fibers it supplies; both nerve
and muscle portions of motor units exhibit wide
but correlated
variation
among several physiological properties.
An expression
of this correlated variation
is the divisibility
of motor units
into types [one slow (S) type and two or three fast
T. C. Cope
is in the
Dept.
of Physiology,
Atlanta,
GA 30322,
USA.
M. J. Pinter
Anatomy
and Neurobiology,
Medical
vania,
Philadelphia,
PA 19729,
USA.
280
NIPS
Volume
10
l
December
1995
Emory
is in
College
University,
the Dept.
of
of Pennsyl-
(F) types], distinguishable
by multiple
parameters (2). The other interesting
observation
is that
motor units are activated or recruited
in accord
with their physiological
properties.
This orderly
recruitment,
observed
in a variety of skeletal
muscles
in several animal
species, has been
termed the size principle
by Henneman
(11).
After almost 30 years of close scrutiny, the size
principle
remains a cornerstone
in our understanding
of movement
control,
and it retains
considerable
interest
because
the systematic
behavior
it describes
is one of the best-characterized examples of how activity is coordinated
among members
of neuronal
assemblies.
Here
0886-1714/95
$3.00
0 1995
Int.
Union
Physiol.
Sci./Am.
Physiol.
Sot.
we discuss the size principle,
consider
its underlying
mechanisms,
and examine
how (and
whether)
it can be integrated
into recent thinking
about more specialized
motor-unit
recruitment.
The phenomenon
Motoneurons
follow one after another in generating their first action potentials
as they are
brought to threshold
by excitatory
synaptic
input. This sequence
holds in repeated presentations of the same excitatory
stimulus,
and the
sequence is the same among those motoneurons
recruited by different sources of excitation,
both
reflex and volitional.
Thus motoneurons
are
generally
recruited
into activity
in a regular,
nonrandom
sequence.
The recruitment
sequence is correlated
with a
variety of motor-unit
properties.
Correlations
are
found with both the conduction
velocity of and
the current generated
by action potentials
traversing the motoneuron’s
axon. Motoneurons
exhibiting
slower
conduction
velocity
and
smaller action current are recruited before those
with faster and larger values. This rank ordering
is of interest because conduction
velocity
and
current magnitude
depend on the caliber of the
axons; small axons conduct slowly, produce less
current,
and are recruited
sooner than larger
axons. Making
the assumption
that axon and
soma size are correlated,
Henneman
(11) developed the size principle,
the precept that small
motoneurons
are recruited
before larger ones
(Fig. 2A).
Several other parameters
correlate
with recruitment
sequence,
for example, the force produced by isometric twitch and tetanic contractions of motor units; weaker
motor units are
recruited
before more forceful ones. Some have
argued
that this is yet another
expression
of
motoneuron
size to the extent that smaller motoneurons,
those with slower conduction
velocity, produce
less tension because they contact
fewer muscle fibers. Other properties
shown to
correlate
with recruitment
sequence
include
twitch
contraction
time (slower
units are recru ited before faster ones) and fatigabi I ity, (fatigue-resistant
units are recruited
before fatiguesusceptible
ones).
Predicting
recruitment
order. All of the motor-unit
measures mentioned
are equally good
predictors
of recruitment
sequence when motor
units are recruited
in reflexes evoked by natural
stimulation,
e.g., muscle stretch and skin pinch
(see Refs. 6, 7). However,
in the decerebrate
cat
preparation
from which
these data were collected, natural
stimulation
is not effective in
recruiting
all units, and electrical
stimulation
of
afferent fibers at high frequencies
is needed to
study the recruitment
order of units with high
thresholds.
Using the latter approach,
Zajac (15)
reports that, among higher threshold
units, recruitment
sequence
is poorly predicted
by axonal conduction
velocity but well predicted
by
motor-unit
force, just as it is over the entire range
of unit thresholds.
The author (15) concluded
that poor prediction
of order by conduction
velocity was characteristic
of type F motor units.
A test of that notion (7) has since shown that
conduction
velocity is an excellent
predictor
as
shown by Bawa et al. (I), even among those type
F units that can be recruited
in stretch reflexes.
Taken together,
these studies lead to the conclusion
that predictions
of recruitment
order
based on conduction
velocity
apply to motor
units over much of the recruitment
range but
break down for a subset of type F units with high
recruitment
threshold
(see below).
In contrast,
the force produced
by motor units accurately
predicts order over the entire range of recruitment thresholds
and stands as the best predictor,
although
some question remains about whether
high-threshold
units are recruited
in the same
order by electrical
stimulation
at high frequencies as they are by other means, e.g., volitionally
or reflexively.
The mechanism of orderly
//. . . motoneurons
are
generally
recruited
into activity in a re !gular, nonrandom
sequence. ”
recruitment
A motor
unit is recruited
when
sufficient
depolarizing
current
is provided
by synaptic
pathways
to enable the motoneuron
to begin
firing action potentials.
A motoneuron’s
recruitment threshold
is thus determined
by the interaction between the organization
and strength of
synaptic inputs and by the factors that determine
the motoneuron’s
intrinsic
responsiveness
to
synaptic currents. It follows that a collection
of
motoneurons
exhibiting
an orderly recruitment
behavior
must feature either a correspondingly
orderly
organization
of synaptic
input, an orderly organization
of intrinsic
motoneuron
excitability,
or a suitable
combination
of both
factors. We must now consider
the relative
contributions
of these factors in determining
orderly recruitment.
Intrinsic excitability
of motoneurons.
A number of studies have examined
how intrinsic
excitability
is distributed
among motoneurons
and how this distribution
is related to factors,
such as conduction
velocity or motor-unit
force,
that define motor-unit
recruitment
order. In these
studies, the minimum
amount of current needed
to evoke a single action
potential
(rheobase
current)
has served as the primary
index of
intrinsic
motoneuron
excitability.
The most
Volume
10 * December
1995
NIPS
//. . . orderly
recruitment is a built-in
feature of motoneuron
populations.
It
282
NIPS
common
and important
result is the indication
that orderly recruitment
is a built-in feature of the
investigated
motor nuclei. However,
some uncertainty
remains
concerning
how well motoneuron
intrinsic
excitability
is related to recruitment
order, which
particular
motoneuron
properties
are most important
in determining
this
excitability
spectrum,
and whether
a classification scheme such as motor-unit
type is at all
useful in relating
the motoneuron
excitability
spectrum to motor-unit
recruitment.
In a comprehensive
study of the relationships
between
motoneuron
electrical
and motor-unit
mechanical
properties,
Fleshman et al. (8) found
that rheobase current was positively
correlated
with both conduction
velocity and tetanic force
across motor units in the cat medial gastrocnemius (MC) muscle. Thus those motoneurons
that
are generally
recruited
first during the stretch
reflex (smallest force motor units and slowest
conducting
motor axons) also require the least
amount of current to initiate an action potential.
Evidence such as this suggests the existence of a
functional
structuring
within
motoneuron
populations that directly
links intrinsic motoneuron
excitability
(as defined by rheobase
current) to
those properties
that have defined
orderly
recruitment
(conduction
velocity and motor-unit
force). These correlations
are the basis for the
view that orderly recruitment
is a built-in feature
of motoneuron
populations.
Two additional
considerations
regarding these
correlations
have served to refine and, in one
instance, challenge
notions about how “orderly” orderly
recruitment
actually
is. The first
concerns
the correlations
between
measures of
motoneuron
excitability
and predictors
of motor-unit recruitment
order. Although
Fleshman et
al. (8) demonstrated
correlations
between
rheobase current,
conduction
velocity,
and motorunit force within data derived from the entire MG
sample (i.e., across all motor-unit
types), they did
not find evidence
for these relationships
within
data groups
formed
according
to motor-unit
type. Also associated
with this pattern was an
absence
of within-type
correlations
between
rheobase current and other motoneuron
electrical properties
(such as input resistance) that are
expected
to occur for biophysical
reasons. Because of these negative findings,
these authors
suggested that motor-unit
recruitment
might be
random within
types and only become orderly
when
considered
from the standpoint
of the
entire motor-unit
population.
Motor-unit
type
was thus viewed as the principal
factor around
which recruitment
would
be organized.
Subsequent studies, however,
have provided convincing evidence against this provocative
notion and
Volume
10
l
December
1995
some of the data upon which
it was based.
Recruitment
was perfectly ordered
by conduction velocity for type S pairs of motor units in the
reflexively
activated
soleus muscles of cats (I)
and by motor-unit
force for like-type
pairs of
motor units in electrically
activated
plantaris
muscles of cat (15). Also, Gustafsson
and Pinter
(9) were able to demonstrate
the expected correlations
between
rheobase
current and input
resistance
within
groups of motoneurons
that,
although
not classified
according
to motor-unit
type, possessed average properties
very similar
to the typed groups of Fleshman et al. (8).
The second consideration
concerns how well
intrinsic
excitability
is related to recruitment
order among
motoneurons.
As noted earlier,
several studies of recruitment
in decerebrate
preparations
have clearly demonstrated
that the
order is quite accurately
predicted
by conduction velocity,.motor
units with lower conduction
velocity being recruited first in as many as 97%
of the tested pairs (1). This high degree of accuracy
leads to the expectation
that a measure
of
intrinsic
excitability
such as rheobase
current
should
be highly correlated
with conduction
velocity if such orderly recruitment
is based, at
least in part, on a systematic variation of intrinsic
excitability
among
the recruited
motoneuron
population.
The problem
is that this correlation
has usually
not been as good as expected.
Fleshman et al. (8), for example,
found a correlation of -0.38
between
rheobase and conduction velocity among cat MC motoneurons,
while
the data of Gustafsson
and Pinter (9) indicate a
similar extent of correlation
among untyped cat
hindlimb
motoneurons.
An important
factor to consider
for resolving
this apparent
problem
is that the motoneurons
sampled
in studies of recruitment
vs. studies of
intrinsic electrical
properties
are not likely to be
identical.
Whereas
an intracellular
study of
rheobase
current and conduction
velocity has
potential
access to all motoneurons,
evidence
indicates
that as much as 25% of the MC
motoneuron
population
in decerebrate
cats cannot be recruited during the stretch reflex (7). This
“nonrecruitable”
group features motoneurons
that possess fast conduction
velocities
and that
innervate forceful motor units. From other work,
we know that these ccl Is are also Ii kely to possess
high rheobase currents and are thus among those
motoneurons
with the lowest intrinsic excitability (8, 9).
These results suggest that it may be more
meaningful
to consider how well intrinsic excitability (rheobase current) and conduction
velocity are correlated
in the “recruitable”
motoneuron group, a subset that might reside in the lower
neuron in the steady state, rheobase current (I,&
is related to these parameters
by Ohm’s law
50
100
Conduction
FIGURE
1.
Plot
ity for cat hindlimb
Pinter
(9).
An additional
relationship
is defined that clarifies the contributions
of cell surface area (A,,,)
and specific membrane
resistivity (R,) to R,,.
Thus
of rheobase
motoneurons.
velocity
current
Data
(m/s)
vs. conduction
from
Gustafsson
and
Substitution
of E9. 2 into E9. I yields
1RH
75% of the rheobase current range. The overall
relationship
between
rheobase current and conduction
velocity among cat MC motoneurons
suggests that this correlation
is probably better in
the lower range of rheobase than in the higher.
This may be seen in Fig. 1, where the linear
relationship
between
these variables
would
clearly
improve
if rheobase
data >I 8-20
nA
were ignored.
Direct
experimental
evidence
(requiring
a combined
study of recruitment
and
intrinsic motoneuron
properties)
will be needed
to establish
how well both rheobase
and conduction velocity predict order among recruitable
motoneurons.
Available
evidence,
however,
is
quite compatible
with the notion that motoneuron intrinsic excitability
plays an important
role
in determining
recruitment
order among those
motoneurons
that can be activated
during the
stretch reflex.
The recruitment
sequence
among those motoneurons
possessing the highest values of rheobase current (lowest intrinsic excitability)
under
conditions
of natural stimulation
is not vet clear
and may never be because of experimental
difficulties in examining
the issue. It does not seem
unreasonable,
however, to speculate that the contributions
of variations
in intrinsic excitability
to
recruitment
sequence would be just as important
among this group of motoneurons.
Indirect support
for this would be the demonstration
of a correlation
between
rheobase current among these nonrecruitable motoneurons
and associated motor-unit
force which, as noted above, is likely to be a better
overall predictor of recruitment
order than axonal
P
conduction
velocity.
If variations
of intrinsic
excitability
among
motoneurons
function
importantly
in determining recruitment
order, then which cellular factors are most important
in determining
the range
of intrinsic excitability
as measured by rheobase
current? A variety of cellular
factors determine
motoneuron
rheobase
current
(9). Two of the
most important
are motoneuron
voltage threshold (VT,-,) and input resistance
(RI,,,). In the
simplest case of a uniformly
polarized,
spherical
(2)
RIN = &JAN
veloc-
=
(hH
x
AN>/Rh4
(3)
Equation 3 demonstrates
how three critical factors can theoretically
contribute
to forming the
range of motoneuron
intrinsic excitability,
and
available evidence indicates that all three factors
participate.
In accordance
with the predictions
of the
original
size principle,
studies demonstrate
that
motoneurons
that innervate
the most forceful
motor units, and thus likely possess the fastest
conduction
velocities
and largest rheobase currents (lowest intrinsic excitability),
are about two
to three times larger on average
than their
counterparts
at the lower end of the excitability
spectrum
(2). Other
evidence
indicates
that
voltage thresholds
may be higher (for long current pulses) and membrane
resistivity
lower
among motoneurons
with the lowest intrinsic
excitability
(9). The combined
effect of these
factors is evident from E9.3; the range of intrinsic
excitability
is expanded
and threshold
differences between
motoneurons
increased
beyond
that achievable
by varying only one factor. Some
have argued that variations
of specific
membrane properties
(e.g., RM)are most important
in
establishing
the range of motoneuron
excitability ($14); others have taken the position that size
(AN) is equally important
(10). Perhaps the best
way to summarize
the evidence
that has accumulated since the size principle
was first formulated is to state that a range of intrinsic motoneuron excitability
exists within investigated
motor
nuclei,
that this range is established
by the
coordinated
variation
of a constellation
of cellular factors (including
cell size) among individual motoneurons,
and that all these mechanisms
operate such that orderly recruitment
becomes
the default mode of motor-unit
recruitment.
Role of synaptic input. If intrinsic excitability
sets the default mode of motor-unit
recruitment,
then how best to view the role of synaptic input
in the process of setting recruitment
thresholds?
Because the basic order appears more or less
prespecified,
it seems reasonable
to propose that
synaptic input systems are concerned
with quantitative features of this order. One important
Volume
10
l
December
1995
“A variety of cellular
factors determine
motoneuron
rheobase
current . . . ”
//
the size princi,;d prescribes
...
which units. . . must
be recruited
to
achieve a specified
amount of force.”
quantitative
feature is recruitment
gain, defined
as the number of motoneurons
recruited
for a
given level of synaptic input (2, 13). An increase
of recruitment
gain, for example, would reflect a
compression
of the range of recruitment
thresholds such that an increased number of motoneurons could be recruited
by subsequent
synaptic
input. In a modeling
study, Kernel1 and Hultborn
(13) demonstrated
how the activity of identically
distributed synaptic inputs can combine to change
average recruitment
threshold but not recruitment
gain across a motoneuron
pool; changes of the
latter require synaptic input systems that are differentially distributed
across the pool.
An important
issue that arises when attempting to relate concepts and experimental
findings
is how the organization
and efficacy of particular
synaptic systems should be expressed. Heckman
and Binder (10) have made a compelling
argument for expressing the efficacy of synaptic input
systems not in traditional
terms of transmembrane voltage but rather in terms of the amount
and polarity of current that actually reaches the
spike-generating
mechanisms
located near the
motoneuron
cell body. To emphasize
the functional
importance
of this portion
of the total
injected current, these authors (IO) have termed
this quantity the “effective”
synaptic current (I,,,)
and have provided
steady-state
estimates of I,
during experimental
activation
of several reflex
systems, including
the muscle spindle afferent
(la) system responsible
for the tonic-vibration
reflex. An important
advantage of expressing the
efficacy and distribution
of synaptic
input in
terms of a current is that these properties
can be
directly compared
with the distribution
of rheobase thresholds
for the recipient
population
of
motoneurons.
For the la afferent system, estimates of I,,, demonstrate
that motoneurons
possessing the lowest rheobase
currents
(highest
intrinsic excitability)
receive more effective synaptic current
than do motoneurons
with the
highest rheobase current (lowest intrinsic excitability). The effect of this type of distribution
of
synaptic input superimposed
on the spectrum of
intrinsic
motoneuron
excitability
would
be to
expand the overall range of recruitment
thresholds (i.e., decrease
recruitment
gain) and thus
enhance
threshold
differences
between
motoneurons,
perhaps increasing
the “orderliness”
of orderly recruitment.
A primary role of synaptic input is to select the
particular
subsets of motor units that are active
under certain conditions.
In addition to differing
in mechanical
properties
such as speed of contraction and force output, motor units also differ
in the direction
of their force output. Exploiting
such differences
probably
makes important
conVolume
10
l
December
1995
tributions
to the precision
as well as the flexibility of motor control. It may, in fact, be useful
to consider the notion of such selective control
to be the next level up from orderly recruitment
in a hierarchy
of motor
control
strategies.
Whereas
the underlying
mechanism
of such
selectivity would clearly be the province
of the
organizational
features of synaptic
input systems, additional,
and somewhat
contentious,
issues arise when contemplating
this possibility,
such as how active groups of motoneurons
are
formed and whether orderly recruitment
and the
size principle
continue to apply; these points are
considered
in more detail below.
Functional value and limitations
of the size principle
Despite the difficulty of proving that the size
principle
represents some practical adaptation
of
the neuromuscular
system, certain benefits have
become axiomatic.
Henneman
and Mendell
(11)
pointed out that the size principle
simplifies
the
computational
task of organizing
the numerous
motor units comprising
muscles (several hundred units for large muscles) by establishing
a
law of combinations;
the size principle
prescribes exactly which
units, arranged
in rank
order, must be recruited
to achieve a specified
amount of force. An objection
to this reasoning
is that the task of selection
may not be so
daunting
if the central nervous system addresses
not tens or hundreds
of motor units but, rather,
only a couple of types of motor units, i.e., S and
F types. There is, however,
no direct demonstration of a recruitment
scheme based solely on
type; available evidence shows that recruitment
is tightly ordered even among units belonging
to
the same type, S or F (see above).
Recruitment
ordered
by motor-unit
size also
seems to benefit aspects of tension production.
It ensures that the most frequently
used units, the
ones most easily recruited,
are those that are
resistant to fatigue.
This recruitment
strategy
enhances
energy efficiency.
Another
benefit is
the provision for smooth accumulation
of whole
muscle
force.
Henneman
and Mendell
(11)
recognized
the advantage that would be gained
from size-ordered
recruitment
of a population
of
motor units that tended to have a disproportionately larger number of weak units. In this case,
newly recruited
units, arranged
from weak to
strong, would contribute
nearly constant increments in force throughout
the range of whole
muscle force; as tension builds slowly with the
progressive
recruitment
of many weak units,
each one contributes
a relative amount of force
that is similar to the force contributed
by the few
Motoneuron
Number
Recruitment
Order
Size Principle?
123456
A l O@(‘)()(-) ‘-+2+3
c
FIGURE
2.
6 motoneurons
Evidence
(motor
oeo..(-J
for or against
units)
ranked
size
from
principle
small
P--!-+2
taken
to large
from
“size,”
strong units recruited
when whole muscle force
approaches
its maximum.
Although
discussion
is
outside
the scope of this article,
the reader
should recognize
that the force contributed
by
each unit also depends
on motoneuron
firing
rate (2).
In addition
to these advantages,
the size
principle
has limitations.
It cannot
by itself
accommodate
tasks and conditions
that require
that recruitment
be organized
around something
other than motor-unit
force or its correlates.
Particular movements
may require, for example,
the selective
activation
of units that produce
different
directions
of joint torque.
The size
principle
does not incorporate
this aspect of
motor-unit
function,
but rather fixes the direction
of movement
as well as total force and other
parameters
contributed
by the recruited
units,
and there is no way of varying that contribution.
In other words, the size principle,
operating
by
itself, would
restrict the central nervous system
to a single degree of freedom in the control of any
one group of motor units.
Additional
degrees of freedom are gained by
segregating
motor units into groups, called task
groups by Loeb and co-workers
(5) and defined
as the set of motor units recruited in order during
one phase of motor activity. Control
over the
direction
of movement
results from the unique
joint actions of the different
task groups.
An
excellent
illustration
comes from the biceps
femoris muscle of the cat. The anterior portion of
this muscle,
which
extends
the hip, can be
activated independently
of the posterior portion,
which flexes the knee. Still more evidence
for
differential
control comes from studies showing
that human subjects recruit different motor units
. within
single muscles depending
on the direction of joint movement
(discussion
and citations
in Refs. 3 and 4). For example, motor units in one
region of the biceps brachii muscle are recruited
in elbow flexion, and units in another region are
recruitment
order
e.g., increasing
observed
conduction
in 3 different
situations
velocity
or contraction
for same
force.
recruited
in forearm
supination.
This kind of
behavior
appears in nearly all human muscles
examined,
so it is widespread
and not a peculiar
feature of a few muscles. Although
direct proof
is lacking, the strong implication
of the human
studies is that motor units are assembled
into task
groups for purposes
of achieving
specific biomechanical
actions.
Although
it is evident
that control
of limb
biomechanics
relies on selection
of the appropriate group of motor units, the composition
of
a group is not easily defined. Anatomic
boundaries do not always provide the basis for definition, because even within structurally
delimited
portions of muscles there is evidence
for independent
activation
of more than one group. A
further difficulty
arises from uncertainty
about
whether
motoneurons
belong to one and only
one group. The inability to recognize
the criteria
by which motor-unit
groups are formulated
foils
attempts
to arrive at unequivocal
conclusions
from some motor-unit
recruitment
data. Consider the following
findings
(discussion
and
citations
in Ref. 3): when human subjects are
instructed
to engage triceps surae muscles in
ankle extension
and in controlled
ankle flexion,
it is observed that some of the motor units that
were easily recruited
in extension
were silent
during
flexion,
while
others were selectively
active in flexion. Another example
comes from
decerebrate
cats in which skin pinch silences or
decelerates
ongoing
firing of units with slow
conduction
velocity and accelerates
the firing of
or recruits units with faster conduction
velocity.
Two interpretations
of these observations
seem
equally
defensible
(Fig. 2B). One rests on the
assumption
that all motoneurons
supplying
a
single muscle belong to a single fixed group.
Under this condition,
selective
inactivity
of a
usually low-threshold
unit advocates a violation
of the size principle.
An alternative
interpretation depends on the assumption
that motor-unit
Volume
10
l
December
1995
“Additional
degrees
of freedom are
gained by segregating
motor units into
groups . . .”
// . . . the size principle is . . . one of the
most fundamental
principles
in the organization
of motorunit behavior.
. .I’
groups can be reconstituted.
Under this condition, silence of the low-threshold
unit represents
exclusion
of that unit from the group, but all
active units obey the size principle.
The consequence
of this indecision
is that there is no
resolution of the extent to which reversal of the size
principle
is an option in the control of movement.
The weight of available evidence sways us and
others (4, 11) away from indecision
and toward
the conclusion
that there are no genuine
violations of the size principle.
When
it can be
unequivocally
tested, i.e., when it is judged only
for motor units that are active, the size principle
holds in the great majority of cases. Reversals of
the size principle
(Fig. 2C) have been reported
occasionally,
e.g., when units are activated
by
electrical
stimulation
of the skin in human subjects (description
and citation
in Ref. 4). However, the functional
importance
of this finding is
dubious
in light of the failure of tactile stimulation of the skin to reverse the recruitment
order
of units with disparate
thresholds
either in humans (12) or in decerebrate
cats (6). We are
willing,
therefore, to conclude
provisionally
that
there are no functionally
meaningful
violations
of the size principle.
From this standpoint,
even
apparent
violations
(Fig. 2C) could reflect the
coactivation
of different motor-unit
groups, with
each group independently
organized
by the size
principle.
References
1. Bawa,
P., M. D. Binder,
Recruitment
highly
Volume
10
l
December
1995
with
2.
functional
organization.
The Nervous
Physiol.
345-422.
Burke,
3.
and
Motor
1981,
sect.
R. E. Selective
Dahlem
Issues,
and
complex
muscles
histochemical
cal heterogeneity
of the
and
predictors
1138,1991.
Fleshman,
8.
of order.
J. W.,
10.
The
fond.
.
357:
Segmental
Henneman,
Bethesda,
.
MD:
unit
motor
Cutaneous
properties
1983,
.
G. W.
.
and
.
and
W.
investigation
motoneurons.
of
/.
Neural
mechanisms
of motoneurons.
In:
edited
by M.
Oxford
Univ.
D. Binder
Press,
Functional
1990,
organi-
pool and its inputs.
In: Handbook
Nervous
System.
Motor
Control.
Physiol.
and
D.,
and
gain:
motor
Sot.,
1981,
sect.
Cutaneous
control
H. Hultborn.
a mechanism
relation
in the
1, vol.
II,
facilitation
of human
of
fingers
in
in Health
York: Raven,
role
F. E. Coupling
produced
by motor
Synaptic
of importance
effects
for
of motoneuron
pools?
of motoneuron
membrane
determination
165-181.
Zajac,
of recruitment
edited
Oxford
the
Press,
1990,
p. 96-l
11.
on
the
Res.
prop-
order.
In: The
by M. D. Binder
and
Univ.
Press, 1990,
p.
of recruitment
units:
Brain
“size
order
to the
principle
sis” revisited.
In: The Segmental
Motor
System,
by M. D. Binder
and L. M. Mendell.
New York:
Univ.
A.
motor
unit
in the cat. /.
1984.
York:
Segmental
Motor
System,
L. M. Mendell.
New York:
15
1127-
Sypert,
L. M. Mendell.
Am.
507:176-179,199O.
Pinter,
M. J. The
erties
66:
p. 253-261.
Kernell,
recruitment
input-output
14
in the
are equally
precision
grip. In: Motor
Control
Mechanisms
and Disease,
edited
by J. E. Desmedt.
New
13
of
1981.
I. New
units
roles
recruitment
resistance,
motoneurons
pt. 1, chapt.
11, p. 423-507.
Kanda,
K., and J. E. Desmedt.
large
Functionally
J. NeurophysioL
System,
E., and
Univ.
and mechaniactivation.
Exp.
unit
453-483,
Motor
in
by M.
V. The
M. J. Pinter.
An
among
cat spinal
zation
of motoneuron
of Physiology.
The
12
Oxford
C. J., and M. D. Binder.
the orderly
recruitment
and L. M. Mendel
p. 182-204.
11
York:
T. C. Cope.
46:1326-1338,
Heckman,
underlying
edited
G. E. Loeb.
J. B. Munson,
B., and
properties
Freund.
70: 1433-l
439, 1993.
Motor
unit recruitment
in
Friedman.
Rheobase,
input
type in medial
gastrocnemius
Neurophysiol.
In:
recruitment
fiber-type
regionalization
in differential
muscle
decerebrate
cat. J. Neurophysiol.
T. C., and B. D. Clark.
7. Cope,
the decerebrate
cat: several
H.-J.
System,
hindlimb.
Brain
Res.85:
300-313,
1991.
B. D., S. M. Dacko,
and
6. Clark,
stimulation
fails to alter
motor
p.
Concepts
and
New
cat
Am.
10,
units.
Control:
Motor
L. M. Mendell.
MD:
of motor
by D. R. Humphrey
Press, 1990,
p. 75-95.
5. Chanaud,
C. M., C. A. Pratt,
good
Bethesda,
II, pt. 1, chapt.
UK: Wiley,
1991,
p. 5-21.
B., and P. Bawa.
Motor
unit
D. Binder
and
of Physiology.
Motor
In: The Segmental
/.
physiology
Control.
1, vol.
is
velocity.
1984.
anatomy,
Reports.
edited
reflexes
conduction
recruitment
Workshop
Chichester,
4. Calancie,
humans.
E. Henneman.
In : Handbook
System.
Sot.,
and
in stretch
their
Neurophysiol.
52: 41 O-420,
Burke,
R. E. Motor
units:
Physiol.
Does the size principle
work after all these
years? Extensive study has failed to unequivocally demonstrate
functionally
meaningful
exceptions while providing
abundant
confirmation
of the phenomenon
of size-ordered
recruitment.
Thus the size principle
is well established
and
can be thought of as one of the most fundamental
principles
in the organization
of motor-unit
behavior,
with the formulation
of motor units
into task groups being another. As for the mechanism, however,
available
evidence
suggests
that the correlations
of motoneuron
size with
factors such as intrinsic excitability
and recruitment order are probably
not strong enough
to
convince
everyone that cell size is the decisive
independent
variable.
In fact, this lack of 100%
correspondence
will likely incite continued
exploration
of the cellular
strategies
involved
in
manipulating
a number of factors to accomplish
the orderly operation
of motoneuron
ensembles.
Nevertheless,
the fact remains
that size is a
correlated
factor, so from the perspective
of
mechanisms
that underlie
orderly recruitment,
the size principle
seems to work
just fine,
especially
as a rubric.
P. Ruenzel,
of motoneurons
correlated
9. Gustafsson,
threshold
Final perspectives
NIPS
order
force
hypotheedited
Oxford