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Origin and Advances of the

Equilibrium-Point Hypothesis
Article in Advances in Experimental Medicine and Biology February 2009
Impact Factor: 1.96 DOI: 10.1007/978-0-387-77064-2_34 Source: PubMed

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The Equilibrium-Point Hypothesis Past, Present

and Future
Anatol G. Feldman and Mindy F. Levin

Abstract This chapter is a brief account of fundamentals of the equilibriumpoint hypothesis or more adequately called the threshold control theory (TCT).
It also compares the TCT with other approaches to motor control. The basic
notions of the TCT are reviewed with a major focus on solutions to the
problems of multi-muscle and multi-degrees of freedom redundancy. The
TCT incorporates cognitive aspects by explaining how neurons recognize that
internal (neural) and external (environmental) events match each other. These
aspects as well as how motor learning occurs are subjects of further development of the TCT hypothesis.

Introduction
We begin with an explanation of two fundamentals of the equilibrium point
(EP) hypothesis the EP concept and the notion that changes in threshold
positions of the body or its segments underlie EP shifts and motor actions.
From the biophysical viewpoint, motor actions result from shifts in the
equilibrium state that the organism and the environment tend to achieve in
the process of the mutual interaction. Such shifts can be elicited voluntarily, by
the organism, or involuntary, following changes in environmental forces. It is
essential to emphasize that the equilibrium state is conditioned by both the
organism and the environment and therefore the organism can only influence
but not entirely predetermine it: the environment is an equal player in achieving
this state.
The notion of EP was introduced to characterize the equilibrium state in
terms of output, mechanical variables such as the equilibrium positions of body
A.G. Feldman (*)
Department of Physiology, University of Montreal, School of Physical
and Occupational Therapy, McGill University; Center for Interdisciplinary
Research in Rehabilitation, Montreal Rehabilitation Institute and Jewish
Rehabilitation Hospital, Canada
e-mail: feldman@med.umontreal.ca

D. Sternad (ed.), Progress in Motor Control,

DOI 10.1007/978-0-387-77064-2_38, Springer ScienceBusiness Media, LLC 2009

699

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A.G. Feldman and M.F. Levin

segments and the muscle torques at these positions. In particular, the EP of a

single joint is a two-dimensional vector which represents the values of both joint
angle and net joint torque balancing the external forces in the equilibrium state.
The view that the EP and equilibrium position are identical concepts is incorrect. For example, during isometric torque production, the equilibrium position
is constrained by the environment and cannot be changed by the nervous
system. Contrary to what the above point of view implies, the system can shift
the EP, even in isometric conditions, by influencing its other component the
equilibrium values of muscle torques by changing specific parameters
described below. This makes the EP hypothesis applicable to any motor actions
whether or not they result in motion.
Indeed, the concept of the equilibrium state is not unique for biological
systems: other systems, including stones, naturally reach such a state if stability
conditions are met. Moreover, occasional changes in the environment can elicit
a shift in the EP, and, as a consequence, motion to another EP. Such changes
elicit involuntary motions of the organism or its segments. For example, the EP
that characterizes the interaction of the arm with the environment abruptly
changes when the load (e.g., a heavy book) held on the palm of the hand is
suddenly fell off or removed by another person, resulting in an involuntary
motion of the arm to another equilibrium position (unloading reflex). Living
systems are unique in the ability to influence the EP and thus elicit motor
actions, even if the environment remains unchanged.
Physiologically, the nervous system may influence the EP by shifting the
threshold positions of the body segments at which muscles begin to be recruited.
In other words, the nervous system has the means changing thresholds
positions of shifting the EP to produce motor actions. In such a way, the
nervous system forces the organism to find another state of equilibrium in the
interaction with the environment. Depending on the pattern of the threshold
shifts and the environmental conditions, the system may produce different
motor actions achieves the desired isometric torque or hand position, hits a
ball or appropriate piano key during the transition from one EP to another,
establishes the desired body configuration or a sequence of them during dancing, etc. If the action is executed in a satisfactory way, the specified central
shifts in the threshold positions can be stored in motor memory and reproduced
in similar environmental conditions. If not, the system may modify the central
shifts in thresholds until the same or another motor goal is reached.
The two fundamentals of the hypothesis, the EP concept and the notion that
changes in threshold positions underlie EP shifts and motor actions are empirically well-established facts. In this situation, it is more appropriate to call these
fundamentals as comprising the threshold control theory (TCT), rather than
hypothesis. As any scientific theory, it can eventually be disproved. However,
since Galileo, science become cumulative (Ferris 1977) that means that, even
rejected, well-established scientific theories are not vanished but continue to
exist as subsets of more advanced theories, as is the case in the relationship
between Newtons mechanics and theory of relativity. The fact that the TCT not

The Equilibrium-Point Hypothesis

701

only has survived numerous attempts of rejection during last 43 years but also
has been continuously advanced by solving several essential problems in motor
control (see below) suggests that its explanatory and predictive power is far
from having been exhausted.
In many aspects, the TCT challenges traditional views on how motor actions
are controlled and produced, which explains why the theory, in essence, simple
is often poorly understood and misinterpreted (Feldman and Latash 2005). We
will list five aspects of the TCT that conflict with traditional approaches to
motor control.
First, the TCT implies that neural control levels are not involved in the
specification of movement trajectories, muscle activation, forces and torques,
nor do they specify the EP the values of these variables emerge following the
central shifts in the threshold positions and interactions within the organism
and between the organism and the environment. Thus, the TCT rejects the idea
motivated by mechanics and robotics, that the nervous system is directly
involved in programming of EMG activity and mechanical variables describing
the motor output.
Second, the TCT implies that by specifying threshold positions of body
segments the neural control levels only narrow the set of possible EPs and the
repertoire of possible motor actions but do not specify per se a unique EP or
motor action. For example, in response to the same shifts in the threshold value
of a joint angle, the motor output may be different, depending on external
conditions: if there are no obstacles, the joint will move to another position or,
otherwise, generate an isometric torque. In other words, neural control levels
only diminish the redundancy in the possible EPs and motor actions, while a
unique sequence of EPs or a unique motor action emerge in the process of the
interaction of different neuromuscular components of the organism between
themselves and with the environment. This notion conflicts with the traditional
idea that solutions to redundancy problems in motor control rely on internal
computational procedures that compares different motor actions, selects and
specifies one of them based on some optimality criterion.
Third, in the cases when external forces acting on body segments are zero, the
threshold position (R) may coincide with the actual position (Q) of these
segments but generally these positions are different. This difference implies an
important notion. Each actual position, Q, can be considered as a point in the
space of all physically possible positions (postures) of the body. In other words,
body postures can be considered as coordinates in the space of all-possible body
configurations. By specifying an R posture, the nervous system defines the
origin point in this space (frame of reference). Because of the threshold nature
of the R posture, other body postures becomes non-equivalent: anatomically
and neurophysiologically, some muscles (usually called agonists) at a given
posture, Q, appear as being stretched above the thresholds of activation and
resist the deviation from the threshold, R posture whereas other muscles
(antagonists) remain silent. Physically, this imply that muscles react depending
on some measure (metrics) characterizing the closeness of a given posture to

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A.G. Feldman and M.F. Levin

the threshold posture, R. By shifting this origin point of this configurational

frame of reference, the system pre-determines where, in spatial coordinates,
neuromuscular elements should work and produce motor actions. Thereby,
neural control levels do not instruct which and how neuromuscular elements
should work. Each of them (including motoneurons and muscles) appears to be
either in supra-threshold, or sub-threshold state and activated or not depending
on the deviation of the actual posture of the body from its threshold posture.
Indeed, the idea that motor actions are produced in appropriate frames of
reference is not new (e.g., Colby 1998). A new idea implied by the TCT is that
the properties of neuromuscular elements are frame-dependent. As a consequence, the nervous system has the capacity to elicit motor actions by shifting
such frames by influencing their origins. These neural frames are thus different
from mathematical frames or systems of coordinates that are usually used to
describe motor actions: these actions remain the same regardless of our choice
of the mathematical frame in which they are described. To emphasize the
difference from mathematical frames, the spatial frames of reference used by
the nervous system are called physical or action-producing frames of reference
(Feldman and Levin 1995).
Forth, according to the TCT, the pattern of shifts in the threshold positions
that produced a desirable motor output in specific conditions can be stored in
motor memory and reproduced when the system recognized that the conditions
are the same. However, the pattern of threshold shifts becomes inadequate when
the conditions change. The system can either modify the central pattern of
threshold shifts to reach the same motor goal or change the motor goal by
switching to a quite different pattern of shifts. Motor memory is thus associated
with storing, memorizing and reproducing the condition-specific central patterns
of threshold shifts that yielded the desired motor output. Learning is also based
on recognition of changes in the environment and appropriate adjustments of the
control patterns of threshold shifts to reach the same or another motor goal.
Five, although the TCT has mainly been developed in relation to motor
control, it has important implications for perception. In particular, the TCT
implies that by resetting threshold positions to elicit a motor action, the nervous
system simultaneously adjusts spatial thresholds of sensory systems involved in
this action. In other words, the frames of reference for action and perception are
identical so that shifts in threshold positions of body segments result not only in
motor action but also in resetting of the origins of spatial frames of reference in
which sensory signals are adequately interpreted. This notion has been illustrated for kinesthesia (position sense and sense of motion) by demonstrating
that afferent proprioceptive signals per se deliver ambiguous kinesthetic information and that the ambiguity disappears if the central control signals underlying resetting of the threshold limb position are taken into account (Feldman
and Latash 1982). The sensation that the environment remains motionless
during walking may also result from central shifts in the origin of frames of
reference associated with the environment by appropriate efferent influences on
visual and vestibular signals (see below). Indeed, the notion that frames of

The Equilibrium-Point Hypothesis

703

reference for action and perception are united is reminiscent of the suggestion
that action and perception are related (Gibson 1966).

Relation to Other Approaches to Motor Control

Before elaborating on the basic concepts underlying the TCT, we would like to
identify the relationship between this theory and other contemporary
approaches to motor control the dynamic systems theory and internal
model theory of motor control.
The TCT is a specific form of dynamic systems theory. In particular,
although each EP is associated with a static (steady) state of the system, the
notion of EP shifts is essentially dynamical. It implies that the nervous system
may change specific neuro-mechanical parameters muscle activation thresholds to globally change a major dynamic characteristic of the interactions
within the organism and between the organism and the environment the
steady state emerging from this interaction. The presence of an EP essentially
influences the dynamics of motor behavior especially when the system is far
from the EP. At the same time, recent developments of the TCT strengthen,
rather than diminish, the empirical nature of the hypothesis. Anchored on basic
physiological principles, the EP hypothesis resists the existing tendency of
applying some aspects of dynamic systems theory to motor behavior without
assurances that these aspects are biologically feasible.
The TCT resists another tendency that, based on robotics, suggests that
movement control is eventually reduced to computations and specifications of
motor commands, i.e., electromyographic (EMG) patterns that provide the
desired mechanical output (trajectories, forces, stiffness, damping, position,
velocity and acceleration). Such suggestion is usually combined with the
assumption that the necessary computations are produced by internal inverse
or forward models imitating input-output relationships in the system. The
tendency to consider motor control in a purely mechanical-EMG framework
persists despite a century of neurophysiological studies of motor behavior of
animal and humans that point to the contrary. One clear lesson resulting from
these studies is that although motor actions are described in terms of mechanics
and EMG patterns, the question of how these actions are controlled cannot be
answered in these terms.
From what is presently known about the properties of neurons and motoneurons it would not be difficult to conclude that if the nervous system were
able, with or without internal inverse or forward models, to theoretically
compute and program muscle torques and EMG patterns required for motor
actions, it would still be unable to physically create these torques and EMG
patterns at the effector level. In other words, the theoretical values of torques
could not be physically produced unless they were transformed into appropriate
signals to be delivered to motoneurons. To achieve this, the system needs to

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A.G. Feldman and M.F. Levin

transform the computed torques into individual muscle forces, transform the
muscle forces into individual forces of motor units, transform forces into EMG
signals, transform EMG signals into postsynaptic potentials of hundreds of
individual motoneurons, decompose these potentials into millions of individual
synaptic potentials descending to motoneurons, and so on for interneurons
terminating on motoneurons. In other words, the system would need to solve an
exponentially increasing number of redundancy problems arising at each level
of these inverse transformations. Because of the strong non-linearity of neural
elements (electrical thresholds), some of the inverse transformations appear
impossible (Ostry and Feldman 2003). Thus, the programmed specification of
torques and EMG patterns with or without internal models appears physiologically unrealistic.
One major implication of the TCT is that muscle forces are emergent,
non-programmed variables (see above). The hypothesis acknowledges that,
physiologically, control processes can be expressed in terms of changes in the
membrane potentials of motoneurons and that in the presence of positional
feedback arising from muscle receptors, control processes result in shifts of the
threshold muscle length (l) at which muscles begin to be activated (Feldman
1986). Shifts in the threshold length are ambiguously related to the EMG
signals: the muscle is activated or not depending on the difference (and the
rate of its change) between the actual and the threshold length. The existence of
muscle activation thresholds and the possibility of their central regulation result
from a specific form of integration of afferent and central influences on motoneurons (see below). In other words, the TCT implies that nervous system
controls motor actions by changing neuro-mechanical parameters to which
neither mechanical variables, nor motor commands (EMG signals or their
efference copies) belong.
There are attempts to justify the internal model approach by claiming that it
offers explanations of predictive and anticipatory powers of the brain, most
often manifested during motor learning. While considering these aspects, it is
worth mentioning that Michael Turvey (personal communication) attracted
our attention to the existence of a modern classification of predictive systems
(Dubois 2001). Strong predictive systems are those in which predictive properties are inherent in the systems natural dynamics and thus do not rely on
internal models. Weak predictive systems are based on internal models of
themselves. Typically, proponents of internal models underestimate the possibilities of natural dynamic systems and consider observations of predictive and
anticipatory motor behavior as unequivocal evidence of such models (for
review see Ostry and Feldman 2003). They thus disregard the option that
biological systems may manifest strong predictive and anticipatory properties
in the absence of any internal models. In contrast, this option is offered by the
EP hypothesis, as illustrated in several studies from Ostrys and Gribbles
groups (for references see Ostry and Feldman 2003) as well as by empirical
studies of adaptation to changing external forces (Weeks et al. 1996; Foisy and
Feldman 2006). The claim that predictive, forward models are necessary to

The Equilibrium-Point Hypothesis

705

overcome the destabilizing effects of feedback delays has also been rejected by a
recent demonstration that threshold control manifests predictive properties
allowing the system to achieve stability despite substantial feedback delays
(Pilon and Feldman 2006). Pilon et al. (2007) have also demonstrated that the
experimental observations of an anticipatory increase in the grip force during
arm motion and correlation between the grip and load forces can also be
produced in the absence of any internal models.
Thus, the TCT does not conflict with dynamic systems theory, but rather, is a
part of it. On the other hand, the TCT rejects, as physiologically unrealistic, the
notion that motor control is reduced to computation and programming of
motor commands and mechanical variables characterizing the motor output.
It also suggests that natural dynamic systems, to which biological organisms
belong, may manifest predictive and anticipatory properties in the absence of
any computational inverse or forward internal models of the organism interacting with the environment.

Past
Original Findings in Humans
The TCT resulted from an experimental comparison of involuntary arm movements elicited by unloading with voluntary arm movements produced intentionally by subjects.
Figure 1 shows the manipulandum that was used in experiments in which
changes in forearm position, torque, and EMG activity of biceps (BB) and
triceps brachii (TB) muscles resulting from unloading of the forearm were
recorded (Asatryan and Feldman 1965). Loads (weights) were hung on ropes
that were attached via pulleys to the manipulandum by small electromagnetic
locks. Subjects initially established a specified position while counteracting a
certain load torque. The combination of the current torque and position was
visible as a point on a large display of an oscilloscope and the subject was
required to bring it to the target point (an initial EP) on the same display. Once
the EP was established, the subject was required to close the eyes and an
electrical pulse was delivered to one of the two electromagnetic locks. The
load thus was suddenly decreased, resulting in motion of the forearm to another
combination of the static torque and position (a new EP). Then the initial load
was restored, the subject established the same initial EP, and the trial was
repeated with the same or a different randomly chosen final load. It was thus
possible to record a set of EPs resulting from unloading from the same initial
EP. The tonic EMG activity of pre-loaded muscles was not the same for
different EPs it monotonically decreased with the decreasing amount of the
residual load (Figs. 2 and 3). Together with the initial EP, the the final EPs
comprised a monotonic but non-linear torque-angle curve the displacement of

706

A.G. Feldman and M.F. Levin

a
b

Fig. 1 Manipulandum that was used in unloading experiments that revealed that intentional
movements of the arm involve resetting of the threshold elbow angle. Horizontal forces
(weights) were applied to a lever (a) of the manipulandum via ropes, pulleys and small
electromagnetic locks (b). The elbow angle was measured with a potentiometer (c) and the
elbow torque was measured with a ring strain-gauge (d)

a
BB
TB

Angle
Torque
1s
d

40 0

10 Nm

Fig. 2 Unloading of pre-loaded elbow extensors. EMG activity of extensors (triceps brachi,
TB) and flexors (biceps brachii, BB) are shown together with the elbow angle and torque. In
repeated trials, subjects specified the same joint angle while compensating the same net load
torque. The amount of unloading in different trials (af) was randomly selected by choosing
different initial combinations of weights hung on the electromagnetic locks (see Fig. 1) and by
unlocking one or two of them. Note that the tonic EMG activity of TB progressively decreases
with the decreasing amount of the residual load. Similar unloading experiments were repeated
after subjects made intentional transition to different (up to seven) initial combinations of
elbow position and torque

The Equilibrium-Point Hypothesis

a

707
c

BB
TB
Torque
5 Nm 500
Angle
f

Torque (Nm)

6
4
2
0
60

1s

80 100 1200

Elbow angle

Fig. 3 Unloading of pre-loaded elbow flexors. Abbreviations as in Fig. 2. Panel h shows a

static torque-angle characteristic obtained in the unloading experiment. Open circle shows the
initial combination of the elbow angle and net muscle torque. Horizontal bars on the curve
show standard deviations from the mean position established after unloading in repeated
trials

the arm increased with the increasing amount of unloading (Fig. 3 h). The
subjects were instructed not to intervene voluntarily, i.e., behave in a natural
way without trying to intentionally modify the effects of unloading. The behavior of the arm was similar to that of a mass-spring system in response to
changes in load and, therefore, this arm behavior was called spring-like.
As mentioned above, the purpose of these experiments was to try to understand what variable(s) was changed by the nervous system when an intentional
movement was made to another position, rather than describe how the arm
reacted to unloading. With this purpose, after recording one torque-angle
curve, the subject was asked to establish a new initial EP, thus producing a
voluntary action. Then, the unloading trials were repeated with the new initial
EP, yielding a similar torque-angle curve. We thus recorded a family of torqueangle curves starting from different initial EPs (Fig. 4, filled dots) in each of 7
subjects. This family was complemented by an additional torque-angle characteristic recorded during slow passive rotation of the manipulandum when the
subject was instructed to fully relax elbow muscles, using EMG feedback
(passive-torque-angle characteristic; Fig. 4, dashed curve).
The spring-like responses of the arm to unloading suggested that there was
some parameter that subjects were reluctant to change (kept invariant) when
unloading was done but they were forced to change this parameter when
instructed to intentionally move the arm to another initial EP and thus establish
another torque-angle relationship. The suggestion of the existence of a parameter specifically related to intentional actions followed from the mono-parametric

708

A.G. Feldman and M.F. Levin

Torque (Nm)

60
0

100

160
Elbow angle

Muscle length (x)

Fig. 4 A family of static torque-angle characteristics (solid curves) obtained in unloading

experiments (see Figs. 2 and 3). Each of the filled circles shows the respective mean initial
combination (EP) of the joint angle and torque established by the subject before unloading.
Open circles show the combinations of the same variables (final EPs) established after
unloading. For each characteristic, the tonic EMG activity decreased with the decreasing
load (see Figs. 2 and 3). The dashed curve shows the passive torque-angle characteristic
measured in a separate experiment by rotating the manipulandum when the subject was
instructed to completely relax his muscles. Note that each solid curve merges with the passive
characteristic at a specific position (l) that is different for different curves. This implies that
the voluntary motor action responsible for the transition from one torque-angle characteristic
to another was associated with a change in the threshold joint angle

structure of the family of curves. Mathematically, a family of curves is

mono-parametric if each individual curve crosses a straight line drawn
through it at a different point. This was the case for the recorded family
of curves. Note that the family is mono-parametric despite the changes in
the shape of the curves.
In any single torque-angle curve we recorded, one could only observe variables that changed with the transition from one point of the curve to another
but the parameter that remained invariant during such transitions was hidden.
For example, both the net joint torque and position were not constant for a
given curve. Moreover, the tonic levels of EMG activity of elbow muscles for
different points of each curve were also different (Figs. 2 and 3). Since the
muscle torques were different for different points of each curve, it was obvious
that the difference in the tonic EMG levels for different points of each curve is a

The Equilibrium-Point Hypothesis

709

manifestation of the known EMG-force relationship (Lippold 1952). The fact

that different curves were separated in the angular space implied that the shifts
resulted from changes in a parameter having a spatial dimension.
One could see that the angular positions at which the unloading curves
branch off the torque-angle curve of the passive, relaxed muscles of the joint
(dashed curve in Fig. 4) were different for different curves. This implied that the
intentional transition from one torque-angle curve to another (voluntary movement) was elicited by shifts in the threshold angular position, i.e. the position at
which the elbow muscles began to generate active torque. EMG analysis confirmed this conclusion: the parameter that distinguished one unloading curve
from another was the threshold joint angle, i.e. the joint angle at which the
motoneurons of corresponding elbow muscles began to be recruited. The
torque-angle curves were called invariant (ICs) because each of them was
identified by an invariant value of the threshold. The term did not imply that
the shape of the curves was the same (it actually varied but in a thresholdcoupled way).
The suggestion that the specification of a torque-angle curve resulted from
the fixation of a centrally controlled parameter was further supported in several
ways. First, by orienting the ropes with weights differently with respect to the
manipulandum at the same initial EP we could make the torques after unloading either increasing or decreasing functions of the elbow angle (Fig. 5, dashed
lines S1 and S2, respectively). We thus obtained two different sets of final EPs in
repeated unloading trials. Despite the difference in these sets, they comprised
the same, single torque-angle curve, IC (Fig. 5a, solid line). This implied that the
parameter(s) defining the spring-like behavior was preserved despite substantial
changes in the slope of the load characteristics employed during this experiment. Second, the range of perturbations that did not disturb this invariance
was expanded by using double-, instead of single-step unloading (Fig. 5bd). It
was also found that the invariant behavior ceased when comparatively sharp
perturbations were used. This was the case when, after unloading, a sudden
loading of the arm was produced. In these cases, the effects of unloading were
irreversible (non-equifinality; Fig. 5 g), even if the subjects were instructed not
to intervene. It was necessary to make special precautions (soft loading) to
restore the invariant behavior and equifinality in unloading-loading trials
(Fig. 5e,f). Note that the clear demonstration of non-equifinal behavior (and
more recent observations of such behavior in other studies) were quite consistent with the TCT and did not preclude it from further elaboration. The
conversion of the non-equifinal to equifinal behavior shows that the invariant
behavior can be achieved in a certain range of perturbations.

Experiments in Decerebrated Cats

Before the experimental demonstration of threshold control in humans (Asatryan
and Feldman 1965), it was Matthews (1959) who revealed that the threshold of the
stretch reflex in the hind limb muscles of decerebrated cats can be modified by

710

A.G. Feldman and M.F. Levin

a

Torque (kg)

0.6
0.5

500

320

380

320

150

0.4
0.3

20

S2

0.2
0.1

100

g
S1

500

580

90

400

110 130

Elbow angle ()
b

(10; 10)
50
(5; 15)

(10; 10) (10; 10)

180
(15; 5)

440
(5; 15)

(10; 10)

120
(5; 15)

(10; 10)

140
(15; 5)

c
140

100

440

240

50

7.5
130
0 90
Nm

d
1s

Fig. 5 Invariant properties of the torque-angle curves obtained by the unloading method. a:
Arm unloading was produced from the same initial torque-angle combination (initial EP,
upper dot). Different load characteristics (dashed lines S1 and S2) were used to produce final
torque-angle combinations (final EPs, the point of intersection of lines S1 and S2 with the solid
curve). Despite the essential change in the load characteristics, the different final EPs comprise
a single torque-angle characteristic (solid curve). bd: The same final EP can be obtained
despite the temporal variations of the pattern of unloading. The numbers in brackets in each
panel in b and c show the weights (in N) removed in each of two sequential unloadings; the
bottom number shows the interval (in ms) between the two unloadings. In d, full unloadings
were produced by removing the two weights simultaneously. eg: the unloading effect can be
reversed (e, f) or not (g) depending on whether or not the loading after unloading was
produced in a smooth or an abrupt way, respectively

changing the activity of g-motoneurons that influence muscle spindles and, via
afferent feedback, -motoneurons (Fig. 6).
Matthews also found that the threshold could be changed by continuous
(tonic) stimulation of cutaneous nerves (skin reflexes) or afferents responsible
for the crossed extensor reflex. These findings showed that the stretch reflex
could not be considered as producing stereotyped responses to perturbations
but represented a well-organized, parametrically tunable and thus flexible
structure. At the time when the experiments were done, the dominating view
was that EMG patterns were basically generated independently of reflexes and
that the latter only modulated the centrally specified EMG output (the servoassistant hypothesis). This may explain why Matthews was unable to suggest
that threshold control was a fundamental characteristic of any central influences on -motoneurons, not only mediated by g-motoneurons but also those
targeting -motoneurons pre- or post-synaptically or via spinal interneurons.

The Equilibrium-Point Hypothesis

711

1400

a
b

1200

Active tension (g)

1000
800
c
600
400

200

0
0

6
8
Extension (mm)

10

12

14

a
1 kg
1 sec
b
0.5 mV

Fig. 6 Experiments by Methews (1959) showing that g-motoneurons influence the threshold
of the stretch reflex. In the upper panel, an increase in the reflex threshold of the soleusgastrocnemius muscles in the decerebrated cat is illustrated by shifts of the tension-extension
curve from initial position a to the right (be) when the g-fibers in the muscle nerve are
progressively blocked by an anesthetic. In the lower panel, the same effect is illustrated by
showing that a greater lengthening of the muscles is required to evoke EMG activity in the
muscles when g-fibers are blocked (lower traces, compare with upper traces obtained without
anesthesia)

Feldman and Orlovsky (1972) not only reproduced Matthews results but
also showed that many descending systems (including the vestibulo-, reticuloand cortico- and rubro-spinal systems) have the capacity to modify muscle
activation thresholds (Fig. 7; see also Nichols and Steeves 1986; Capaday
1995). The experiments demonstrating threshold position control in humans
and decerebrated cats provided a solid empirical foundation for the EP
hypothesis.

712

A.G. Feldman and M.F. Levin

DN PYR DN+PYR

DN

b
1.2

Force (kg)

4.5
3
2
0

12.5

2.5

15
15 + .3
12
10
15 + 2
7
0

10 12.5 + 2
0 2

0
0

20

15

15

d
20 mm

Length (mm)

0
5

DN DN+TA

Length
Force

EMG

1 kg

1s

Fig. 7 The vestibulo- and cortico-spinal pathways as well as heteronymous reflexes may
influence the threshold position at which muscles are activated (Feldman and Orlovsky
1972). a: Continuous (tonic) stimulation (30/s) of the vestibular Deiters nuclei (DN) decreases
the activation threshold length of the plantaris muscle as shown by shifts of the tensionextension curve to the left (numbers near the curves show the strength, in Volts), of bipolar
stimulation of the DN; the trace without a number is the tension-extension curve for the
inactive muscle. b: Tonic stimulation of the pyramidal tract decreases the effect of stimulation
of the DN (curve DNPYR) by increasing the activation threshold (shifting the curve to the
right). c: Stretching the antagonist muscle (the tibialis anterior, TA) by hanging a 3-kg load to
its tendon detached from the bone when the DN is stimulated results in an increase in the
activation threshold of the plantaris muscle (curves DNTA). d: Electromyographic demonstration of a decrease in the activation threshold of the plantaris elicited by tonic stimulation
of the DN (upper curves: no DN stimulation; lower curves: with DN stimulation)

Physiological Nature of Threshold Position Control

Descending control signals are electrical in nature and it is necessary to
explain how they are converted into a position-dimensional quantity the
threshold muscle length or, at a joint level, threshold angle. Such conversion is
accomplished at the level of the motoneuronal membrane in the presence of
electrical threshold and proprioceptive feedback (Fig. 8a). Specifically, when
the muscle is gradually stretched, the motoneuronal membrane potential
increases according to proprioceptive feedback (Fig. 8b, lower diagonal
line). At a certain muscle length, l, the membrane potential defining the
electrical threshold is reached and the motoneuron begins to generate action
potentials. When additional, central facilitation converges on the motoneuron, its membrane potential is elevated (vertical arrow) and the same
muscle stretch (upper diagonal line) elicits motoneuronal recruitment at a
shorter muscle length, l. Thus the measure of the independent, central

The Equilibrium-Point Hypothesis

713
b

MN

Afferent
input

a
Output

Membrane potential

V+
Central
Input

Vi

xi

xi

Muscle length (x)

c
V+
Vi

Fig. 8 Schematic diagrams that explain the physiological origin of the control of threshold
position resulting from changes in the membrane potential of motoneourons. a: The threshold position at which a neuron is recruited becomes controllable only if central control
inputs are combined with position-dependent afferent feedback at the level of the neuronal
membrane. The existence of electrical threshold at which the neuron is recruited is an
additional condition of the existence of threshold control in a spatial domain. b: In the
absence of a control input, stretching the muscle results in an increase in the membrane
potential and eventually recruitment of motoneurons at a certain, threshold muscle length,
l. Control inputs to the motoneurons (vertical arrows) can increase the membrane potential, resulting in a decrease in the threshold muscle length l. c: Threshold muscle length may
also be changed by inpiuts from the brain stem by influencing the electrical threshold (V) of
motoneurons

influence on the motoneuron is the shift in the threshold muscle length. Note
that threshold muscle length can be regulated centrally, even if the electrical threshold of the motoneuron remains constant. It has recently been
shown that electrical threshold of motoneurons can also be modified by
some inputs from the brain stem (Fedirchuk and Dai (2004) which might
be an additional source of shifting in the threshold length, l (Fig. 8c).
Note that the electrical control signals to motoneurons could not be
decoded into the spatial dimensional threshold in the absence of proprioceptive feedback. Therefore, threshold position control does not exist in
proprioceptively deafferented subjects. As a result, deafferentation results
in substantial motor deficits (see e.g. Levin et al. 1995).
Control levels must be able to elicit activation or, conversely, relaxation of
the muscle at any length within the biomechanical range [x, x]. To meet these
requirements, the threshold must be able to be regulated in a range [l, l] that
exceeds the biomechanical range. In some subjects with hemiparesis and cerebral palsy, the range of threshold regulation is reduced, resulting in weakness,
spasticity, and deficits in inter-joint coordination (Levin et al. 2000; Jobin and
Levin 2000).

714
Fig. 9 Basic rules describing
threshold control, EMG and
force regulation for a single
muscle

A.G. Feldman and M.F. Levin

Threshold control of muscle activation and force
Threshold muscle length:
* = v + + (t)
Muscle is active if the current muscle length (x) exceeds the threshold
length, *:
x* > 0
Muscle activation is proportional to
A = [x*]+
Muscle force:
F = f (A, v, t)
Motor action results from the tendency to diminish the gap between x
and *, i.e., reach a
min A
The range of regulation, [, +], is greater than the biomechanical
range of changes in the muscle length, [x, x+].

Figure 9 lists basic rules underlying the threshold position control, EMG
activity and muscle force regulation for a single muscle. In particular, physiological data indicate that the threshold length is comprised of several additive
components with only one component controlled centrally (Matthews 1959;
Feldman and Orlovsky 1972; Feldman 2007). To reflect these findings, we use
the symbol l* for the composite (net) threshold whereas symbol l is reserved
for its central component:
l l  v   "t

(1)

where l and  are controllable parameters;  is a temporal parameter related to

the dynamic sensitivity of muscle spindle afferents (Feldman and Levin 1995); v is
the velocity of change in the muscle length (v = dx/dt);  is the shift in the threshold resulting from reflex inputs such as those responsible for the inter-muscular
interaction (Fig. 7c) and cutaneous stimuli (e.g., from pressure-sensitive receptors
in the finger pads during grasping); (t) represents temporal changes in the threshold resulting, in particular, from intrinsic properties of motoneurons.
Let the net threshold, l*, be the threshold muscle length for the first motoneuron from which recruitments of motor units of a muscle starts. Then the
muscle begins to be activated if the difference between the actual and the net
threshold length is not negative, i.e. when x l* 0. Otherwise the motoneuron
and the whole muscle are silent. In a supra-threshold state, the frequency and
number of recruited motoneurons increases with the increasing difference
between the actual and the threshold muscle length, so that the activity of the
muscle (EMG magnitude) is proportional to A, where
A x  l 
Here[u]=u if u  0 and 0 otherwise.

(2)

The Equilibrium-Point Hypothesis

715

Rank-Ordered Motoneuronal Recruitment in the Context

of the Threshold Control Theory
Different motoneurons of a muscle are recruited in the order defined by their
individual thresholds (l1*, l2*, etc.). The lowest threshold, l* = l1*, simultaneously represents the activation threshold for the muscle. Note that here we
have a reformulation of the size-principle (Henneman and Mendell 1981) that
states that motoneurons are recruited in the order defined by their anatomical
sizes. Although the new formulation is consistent with the original one but
reformulated in terms of activation thresholds, the principle of rank-ordered
motoneuronal recruitment becomes embedded in a broader context of the TCT.

Kinesthesia: United Frames of Reference for Action and Perception

It is known that the sense of position and motion of limb segments (kinesthesia) is
based on proprioceptive signals, particularly, from muscle spindle afferents transmitted to the brain. We describe several experimental findings showing that
kinesthesia would be deficient if it relied only on proprioceptive afferent feedback.
First, at different isotonic single-joint positions, the activity of muscle spindle
afferents remains the same (Hulliger et al. 1982) although the positions are
adequately perceived as different. Second, during isometric force production,
the activity of muscle spindle afferents increases in proportion to force (Vallbo
1974) but the limb is adequately perceived as motionless. Third, by vibrating the
tendon of a muscle, one can artificially increase the activity of muscle spindle
afferents as if the muscle were lengthened, resulting in the illusion of a change in
the joint angle in the respective direction (typical kinesthetic illusion). Sometimes,
however, tendon vibration elicits the illusion of motion in the opposite direction
(inverted kinesthetic illusion), i.e., contrary to that indicated by proprioceptive
feedback. There are thus cases showing that position sense cannot rely on proprioceptive information alone something else is necessary, but what is it?
Physiologically, during isotonic motion, the agonist muscles are actively shortening. Thereby, the activity of muscle spindle afferents of these muscles would
decrease if their efferent, g-innervation remained constant. The fact that the
activity of muscle spindle afferents remains constant during slow isotonic motion
(Hulliger et al. 1982) simply means that the activity of g-motoneurons increases
with the muscle shortening during such a motion. As a result, the potential drop
in the signals from muscle spindle afferents during muscle shortening is neutralized by the increasing central signals to g-motoneurons. These central, rather
than afferent signals provide adequate position sense during isotonic motion.
Both efferent (central) and afferent signals should be taken into account to
explain why, during isometric force production, the joint angle is perceived as
unchanged: taken in isolation, the increasing central influences to g-motoneurons
would signal muscle shortening whereas the increase in the activity of muscle spindle
afferents would signal muscle lengthening. Taken together at some brain level, the

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A.G. Feldman and M.F. Levin

changes in the muscle length signaled by the central and afferent components of
position sense cancel each other so that the joint angle is perceived as unchanged.
Typical kinesthetic illusions are explained by influences of tendon vibration
on the afferent component of position sense whereas inverted kinesthetic illusions are explained by the influences of vibration on the central component
(Feldman and Latash 1982).
One can assume that -motoneurons and g-motoneurons are facilitated in
parallel and this facilitation sets a threshold length (l) for each muscle or a
threshold joint angle (R) for all muscles of the joint (see below). In this case,
the same threshold angle provides a referent position for motor actions and for
interpretation of proprioceptive signals in position sense, thus giving an illustration of the notion that action and perception are provided in united spatial frames
of reference (Fig. 10). Note that the threshold position, R, should be understood
as the origin of the united frame of reference for motor action and position sense,
rather than as a copy of motor commands (efference copy) considered in
traditional approaches to action and perception. Also note that there is a spatial
equivalent of proprioceptive signals at the level of perception these signals can
be graded in proportion to the deviation of the joint from the R position, an
aspect of position sense that is essential for the explanation of how some anticipatory actions are produced.
Position sense

Joint torque

Load

central
component

R
afferent
component

Joint angle (Q)

Fig. 10 United frames of reference for motor actions and position sense exemplified for a
single joint. By setting a certain threshold joint angle (R), the system constraints the set of
possible equilibrium points the points of a static torque-angle characteristic. A specific
equilibrium point from this redundant set (e.g., point a) emerges following the interaction of
muscle with the load. In order to identify and thus adequate perceive the actual joint angle
(e.g., for point a), the system needs to take into account the threshold, R position (central
component of position sense) and the deviation from it signaled by proprioceptive signals
recalibrated in terms of position (afferent component of position sense). Motor actions are
produced by shifting the R position thus simultaneously resetting the central component of
position sense relative to which proprioceptive signals are interpreted. Sense of effort can be
generated based on a recalibration of the same afferent signals (including those delivered by
afferents form muscle spindles and tendon organs) in terms of force or torques

The Equilibrium-Point Hypothesis

717

Joint torque

arm + load torque

arm torque

Joint angle (Q)

Fig. 11 Preventing changes in the arm position when the load (e.g. a book held on the palm of
the hand) is removed by the subject himself. Subjects can specify an R position so that,
deviated from the R position by gravity, the arm arrives at an actual position (Q). When
somebody places a book on his palm, the arm is deviated to position Q0 . The change in the arm
position elicited by the load is stored in motor memory. While removing the book with the
other arm, the subject can produced a similar but opposite changes in the R position (arrow)
so that the arm remains at approximately the same position (Q0 ) as before the unloading

Anticipatory Actions
In restaurants, we often see waiters lifting a heavy beer stein from the tray while
steadily holding the latter. Indeed, they anticipate a change in the load and do
something to prevent motion of the arm when the load is lifted. Similarly, if a heavy
book held on the palm of the hand is suddenly removed by the subject himself, the
arm motion is usually prevented, in contrast to the case when the book is suddenly
removed by another person. To qualitatively explain this behavior, we need to take
into account that subjects initially specify an R position and the arm arrives at an
equilibrium position Q. This position changes to Q0 when the book is added. The
changes in the proprioceptive signals expressed in terms of changes in the position
resulting from adding the book can be remembered. While lifting the book, the
subject can simultaneously change the R position by the distance defined by these
remembered afferent signals. In other words, by influencing the R, the subject may
compensate the loss of the afferent contribution into position sense elicited by
unloading and thus keep the arm at approximately the same position (Fig. 11).

Present
Different Forms of Threshold Position Control
The TCT underwent some recent developments by applying the scheme in Fig. 8
to different neurons. For example, suppose there are neurons that receive
afferent facilitation in proportion to the distance (aperture) between the

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A.G. Feldman and M.F. Levin

thumb and the index finger, for example, during the task of gripping an object
between them. Then, similarly to the scheme described for motoneurons, independent, central inputs can be interpreted as setting the threshold position
(threshold or referent aperture) for activation of the muscles involved in the
grip (Fig. 12a). Thereby, the grip force will depend on the distance between the
actual aperture (Qa) defined by the size of the object) and the threshold aperture
(Ra) specified by the control inputs. The feasibility of these notions has been
demonstrated by simulation of the elevation of the grip force during arm
motion (Pilon et al. 2007). Similarly, suppose there are neurons that receive
afferent facilitation in proportion to the elbow angle. Then independent, central
inputs to these neurons can be interpreted as setting the threshold elbow angle
for activation of all muscles spanning the joint. In other words, the notion of
threshold position implies the existence of the joint angle at which all muscles
from this group, regardless of their biomechanical functions, reach their activation thresholds (Fig. 12b), as experimentally was confirmed (Ostry and Feldman
2003; Foisy and Feldman 2006).

Membrane potential

Aperture neuron

Aperture (Qa)
b

Elbow neuron

Elbow angle (Qe)

Fig. 12 Different forms of threshold position control a: If some neurons receive afferent
signals that monotonically related to the distance (aperture) between the index finger and the
thumb then central inputs can control the referent (threshold) value (Ra) of the aperture at
which the neurons (aperture neurons) and appropriate hand muscles begin to be recruited.
b: Similarly, if neurons receive afferent inputs that monotonically depend, say, on the elbow
joint angle, then the effect of control inputs is measurable in terms of a change in the threshold
angle at which these neurons (elbow neurons) begin to be recruited. Note that the diagrams
in a, b (see also Fig. 8) not only implies the existence of different neurons that provide different
forms of threshold position control but also explain the important cognitive ability of neurons
to identify when the central and afferent events delivered to the inputs of these neurons (the
actual and threshold positions) match each other. Thereby the neurons act depending on the
degree of the discrepancy between these events

The Equilibrium-Point Hypothesis

Level

719

Table 1 Different forms of threshold position control

Control form

A single motoneuron or muscle

Muscles spanning a single joint
Several joints of the arm

All skeletal muscles

Effectors or whole body in the environment

threshold muscle length, l

threshold joint angle
threshold configuration of the hand
threshold aperture of fingers
threshold arm configuration
threshold or referent body configuration
threshold localization of effectors or whole
body in the environment

These examples shows that the notion of threshold position with appropriate modifications can be referred to different neurons and different levels of
the neuromuscular system, as exemplified in Table 1. At the level of the arm,
threshold position can be defined for its several segments (threshold aperture,
threshold configuration of the hand) or for the whole arm (threshold configuration of the arm; Archambault et al. 2005; Foisy and Feldman 2006). Threshold
position can also be defined for all skeletal muscles of the body (threshold or
referent body configuration), the notion that underlies the explanation of how all
muscles of the body are controlled without redundancy problems (Lestienne et al.
2000; St-Onge and Feldman 2004).
The list of possible threshold positions can be continued by having in mind
that motor actions are often directed to objects in an external space (e.g., a tea
cup on the table). In these cases, the position of effectors (e.g. the hand) or the
whole body should be associated with the environment, rather than with body
parts. The concept of effector neurons that control levels may use to shift the
threshold localization of the effectors or the whole body in the environment is
defined at this level (Table 1).

Solutions to the Redundancy Problems in the Control of Multiple

Muscles and Abundant Degrees of Freedom
The central nervous system can flexibly change the way motor actions are
performed (the phenomenon of motor equivalency; Lashley 1951; Bernstein
1967) by taking advantage of the redundancy in the number of degrees of
freedom of the body. The EP hypothesis implies, however, that control neural
levels actually do not solve the redundancy problem they only constrain the
possible coordination between different degrees of freedom whereas a solution
to the redundancy problem emerges following actual interactions of the neuromuscular elements between themselves and between these elements with the
environment. In other words, motor actions are guided by the nervous system
without concerns about redundancy problems at any neural level. This important
implication of the EP hypotheses is worth emphasizing.

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A.G. Feldman and M.F. Levin

In fact, redundancy problems exist even at the level of single joint control and
here too, these problems are solved automatically without any explicit efforts
of the nervous system. Specifically, at the level of a single joint, the control
process is practically finished with the specification of the threshold angle for
activation of agonist and antagonist muscles. Neither levels of activation, nor
muscle forces, torques, or even a final EP are pre-determined by these control
signals. The IC of the joint defined by these signals is a collection of possible EPs
without indication of how a single EP is selected from this redundant set (see
above). How is the redundancy problem actually solved? Once the thresholds
are specified, the control levels allow different muscles (including flexors and
extensors) to interact between themselves, at mechanical and neural levels, and
with external forces. This interaction itself reduces the redundant number of
EPs to a single EP (Fig. 13).
The notion that neural control levels per se do not solve redundancy problems is crucial to the understanding of how multiple muscles of the body are
controlled. Specifically, it has been suggested that muscles of the whole body are
controlled as a coherent unit by a global factor the difference between the
actual, emerging configuration of the body and its threshold (referent) configuration modulated by the nervous system (Table 1). This allows the nervous
system to guide multiple muscles without redundancy problem: each skeletal
muscle of the body is only activated if its current muscle length at the current
body configuration exceeds the threshold muscle length defined by the referent
body configuration. This global factor in combination with local anatomical,
biomechanical and reflex factors determines whether a muscle is recruited or

Load:

isometric
b

spring-like

Joint torque

c
zero
a
R

Joint angle (Q)

Fig. 13 A redundancy problem and its solution at the level of single-joint control. By shifting
the threshold joint angle, the nervous system only predetermines a specific torque-angle
characteristic that represents a set of possible equilibrium points (EPs). A specific EP (a, b,
or c), i.e. the final combination of the position or torque is established in the process of the
interaction of the joint segments with the external forces (loads). Thus, control levels of the
nervous system only diminish the set of possible motor actions whereas the redundancy
problem yielding a unique motor action from this set emerges following the interaction of
the neuromuscular components between themselves and with the environmental forces

The Equilibrium-Point Hypothesis

721

not (see Levin and Dimov 1997 and Feldman et al. 2007 on how coactivation of
opposing muscle groups influences this process). Experimental confirmations
and modeling of several movements involving substantial number of muscles,
including human walking and sit-to-stand movements, based on these notions,
have been provided (Gunther and Ruder 2003; St-Onge and Feldman 2004;
Archambault et al. 2005; Pilon et al. 2007; Feldman et al. 2007).
The notion that interactions within the neuromuscular system and between
this system and the environment play a decisive role in solving the redundancy
problem equally refers to the redundancy problem at the level of mechanical
degrees of freedom. To describe this solution, we need to characterize a general
principle guiding these interactions. Threshold control implies that given an
appropriate task-specific form of threshold position (R), the neuromuscular
elements are activated and tend to diminish the activity and internal interactions as well as the interaction between the system and the environment in order
to diminish the difference of the actual position of the body from the referent
position (R) to reach, if possible, an equilibrium state. In this state, the difference between Q and R values becomes minimal in the limits determined by
internal and external constraints. This process is a manifestation of the principle
of minimal action in the functioning of the neuromuscular system (cf. Gelfand
and Tsetlin 1971). It guides the motor action in the following way (Fig. 14).
Neural control levels select an (leading) form of threshold position control,
Rl, which is most appropriate for a given motor task. By changing this threshold, they change the activity (Al ) of appropriate neurons at this level. This
activity influences the form of threshold control, Rs , in neurons of subordinate
levels. The activity, As , of these neurons eventually influences the l thresholds
of motoneurons of muscles. A motor action emerges following the control
influences and the tendency to minimize the activity at other levels. The process
goes until external and internal constraints (e.g. intentional or mechanical
restrictions of the mobility of some degrees of freedom) limit the depth of the
minimization. In the absence of constraints, the system may reach an absolute
minimum at which the referent (threshold positions) are reached at all neuromuscular levels, as indicated by the bottom line in Fig. 14.
Figure 15 illustrates how, in qualitative terms, threshold control and the
principle of minimal action guide the motion of the hand to a cup. The movement is produced by shifting the referent coordinates (R) of the hand by
influencing neurons that receive afferent inputs related to the actual coordinates
(Q) of the hand in space (see the bottom section of Table 1). The movement will
proceed until the difference between these variables becomes minimal, which
occurs when neurons of subordinate levels, including motoneurons, also minimize their activity (Fig. 15). In each trial, there will be no uncertainty in
choosing one coordination pattern of a set of many other patterns each
time, the minimizing process will produce a unique coordination pattern. If
necessary, with additional corrective shifts in R, the target will be reached. The
coordination pattern leading to the same motor goal (motor equivalency) can,
indeed, naturally vary with task repetitions, history-dependent changes in the

722

A.G. Feldman and M.F. Levin

The principle of minimal action
control

Al = [Ql R*l]+
min

(l: leading level)

As = [Qs R*s]+
Am = [x *]+

(s: subordinated level)

(motoneuronal level)

Absolute minimum:

Al = As = Am = 0
Ql = Rl ; Qs = Rs ; x = for all muscles

Fig. 14 Principle of minimal action and its capacity to guide multiple muscles and degrees of
freedom without redundancy problems. Different forms of threshold position control are
tools that the nervous system can select by influencing respective neurons in order to reach the
motor goal. Like usual tools in everyday life, these forms do not represent the motor goals.
This strategy is reminiscent of using the steering wheel to direct the car motion: the focus is on
the direction of car motion, rather than on the means (turning the steering wheel) used to
accomplish this. Once the choice of the appropriate (leading) form (Rl) is made, the nervous
system influences respective neurons to guide the body or its segments to reach the goal. By
generating the activity (Al) depending on the difference between the actual and the referent
position at this level, these neurons influence the referent position (Rs) at subordinate neural
levels. The activity (As) neurons at these levels eventually influence the individual thresholds
of muscle and motoneurons. The functioning of the whole system is guided by the tendency to
reach activity minima at all levels, in the limits defined by internal and external constraints.
Because of the minimization principle, the system produces a unique action without concerns
with redundancy problems. Because of variation in the properties of neuromuscular elements
(e.g., due to fatigue, intentional or mechanical restrictions of the mobility of some degrees of
freedom), the emerging action can vary with movement repetition. With appropriate choice of
the leading form of threshold position control, the goal (e.g. reaching for a cup, see Fig. 15)
can be achieved comparatively easy either by a single shift in the Rl or after additional
corrections. The system may use several forms of threshold position control to reach several
motor goals (for example, to reach a cup on the table while simultaneously leaning the trunk
to better hear a person on the opposite side of the table)

system (e.g., due to fatigue), task constraints (e.g. intentional involvements or

mechanical restrictions of some degrees of freedom of the body). If some
degrees of freedom are suddenly obstructed, other degrees of freedom will be
modified to reach the same activity minimum and thus reach the goal
(cf. chapter by Kelso in this volume). One prediction of this minimization
strategy for pointing movements the invariance of the hand trajectory regardless of the number of degrees of freedom involved in the action has been tested
and confirmed by Adamovich et al. (2001). Indeed, the observation that sounds
may not be affected by sudden mechanical perturbations of jaw movements (see
chapter by Kelso and Latash in this volume) is explicable by the principle of
minimal action.
Several minimization principles have been suggested for movement production (e.g., the smoothness criterion that well describes movement trajectories;
Hogan and Flash 1987). Formulated in terms of output mechanical variables,

The Equilibrium-Point Hypothesis

723
R*s

Qs
Rl*

Ql

Fig. 15 Reaching for a cup guided by shifts in the referent hand position and by the principle
of minimal action. Some spinal and supraspinal neurons projecting to motoneurons mono- or
poly-synaptically may integrate somatosensory, visual and vestibular inputs and proprioceptive signals from muscle, joints and skin receptors to receive information about coordinates
(Q) of the hand in an external frame of reference (FR). Like for motoneurons, independent,
control influences on these neurons can be measured by the amount of shifts in the threshold
(referent) position (R) of the hand (hand neurons). Such neurons may or may not be
recruited depending on the difference between Q and R. In the task of reaching for a cup
control levels shift the R to move the hand in the desired direction. As long as the hand
approaches the cup, it is not essential whether or not the actual and referent trajectories of the
hand coincide. Reaching for a cap is thus controlled by shifting the origin R of the leading FR
in which the hand position (Q) is localized. According to the principle of minimal action (see
Fig. 14), the activity of hand neurons influences the referent body configuration set by changes
in the membrane potentials of subordinate neurons. The output of the latter, in turn,
influences the threshold lengths of individual muscles and eventually of motoneurons. The
activity of neural elements in each FR tends to minimize (min) the discrepancy between the
actual and referent coordinates, forcing the arm and other body segments to move until the
hand reaches a final position at which a minimum in the system, in the limits of intrinsic and
external constraints, is reached. Because of the weights of the body segments, the absolute
minimum (zero activity at all subordinated levels will not be reached: the body will continue to
move until at some equilibrium position, Q, the activity of appropriate muscles will produce
torques balancing the weight torques. The system may correct the Rl until the resulting hand
position becomes convenient for grasping the cup

these principles lack the essential element describing forms of threshold positions underlying motor control. Therefore, their applicability and explanatory
power are restricted, as would be the case if optimization of motor behavior
implied by EP control were considered without identifying control variables
threshold positions. These principles may appear to be reduced forms of the
more general principle of minimal action.
A similar relationship exists between the threshold control theory and the
synergy concept which was formulated without consideration of the relationship between neural control variables and emerging output variables (see chapters
by Kelso and Latash in this book). It remains to be seen whether or not the
synergy concept can be reformulated in the framework of the TCT.

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A.G. Feldman and M.F. Levin

Future
Both empirical and modeling studies have also demonstrated the usefulness of
the TCT in the explanation of learning, memory, kinesthesia, and neurological
movement disorders (Feldman et al. 2007) and no doubt these aspects of the
TCT are worthy of further development. Even these future advances will not
spell the end of the development of the TCT. Where can one go from here? Note
that the scheme in Fig. 8 is not just an explanation of the physiological origin of
threshold control. It implies that motoneurons and many other neurons are
cognitive devices that recognize when the values of respective physical variables
delivered to their inputs from sensory receptors match the centrally specified,
referent values of the same variables. Moreover, these devices signal to muscles
or other neurons the degree of the discrepancy between these variables and thus
tend to diminish the discrepancy, as the principle of minimal action suggests.
Threshold control thus provides a principal answer to the question of how the
nervous system can identify that some internal (referent) and external (physical)
events match each other: motoneurons and neurons are skillful in this function.
The development of these, cognitive aspects of the TCT might be beneficial for
the understanding of the functioning of different brain structures. Indeed, the
cognitive aspects can be developed within the TCT based on the notion that
frames of reference for action and perception are united (see Introduction).
The history of the EP hypothesis and its development might be a good
illustration of the notion that problems cannot be solved by thinking within
the framework in which the problems were created (Albert Einstein; a quote
from Pound 2004). In essence, the posture-movement problem and redundancy
problems in multi-muscle and multi-joint control appeared as such within the
mechanical framework. As soon as thinking went beyond the mechanical
framework by taking into account threshold position control and the principle
of minimal action, these problems are solved in a natural way. Thereby, it came
out that neural control levels are not pre-occupied in solving these problems:
these levels guide motor actions by specifying where, rather than which and
how, neuromuscular elements should work and rely on the capacity of these
elements and the environment to yield each time a unique action.
Recommended reading for students: Von Holst and Mittelstaedt (1950/1973);
Matthews (1959); Feldman and Orlovsky (1972); Nichols and Steeves (1986);
Feldman and Latash (1982); Hogan and Flash (1987); Latash (1993); Feldman
and Levin 1995; Won and Hogan N (1995); Gribble et al. 1998; Levin (2000);
Ostry and Feldman (2003); St-Onge and Feldman (2004); Feldman (2008); Foisy
and Feldman (2006); Feldman et al. 2007; Pilon et al. (2007)

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