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First published online June 27, 2008
Journal of Experimental Biology 211, 2193-2195 (2008)
Published by The Company of Biologists 2008
doi: 10.1242/jeb.010868
JEB Classics |
PARALLEL `PHASIC' AND `TONIC' MOTOR SYSTEMS OF THE CRAYFISH ABDOMEN
University of Toronto
h.atwood{at}utoronto.ca
|
;
Kennedy and Takeda, 1965a) on
crustacean motor systems established a general principle of motor control:
there is a division of labour among available motor neurons and muscle fibres.
The investigators recognized two types of muscle in the crayfish abdomen,
which they categorized as slowly contracting or `tonic' (capable of sustained,
fatigue-resistant, graded contractions), and rapidly contracting or `phasic'
(producing very rapid, twitch-like, non-sustained contractions). The two types
of muscle are anatomically separated and supplied by two sets of motor neurons
with very different physiological properties. The motor neurons of the tonic
musculature exhibit a lot of spontaneous impulse activity and are responsible
for postural adjustments and everyday locomotion. In contrast, the motor
neurons of the phasic musculature are silent most of the time, but when
recruited for vigorous escape activity they fire a few impulses at a time in
intermittent bursts, producing relatively brief episodes of intense movement.
Many variations on this theme have since been found throughout the animal
kingdom, but in selecting the musculature of the crayfish abdomen, Kennedy and
Takeda presented an extremely clear-cut case of complete separation of phasic
and tonic motor systems, with anatomically distinct sets of muscles innervated
by separate groups of specialized motor axons (now often referred to as
`phasic' and `tonic' motor axons).
To appreciate the significance of this major contribution, we have to go
back to the era in which the study was developed. Earlier physiological work
on crustacean muscles, starting in the 19th century, had been on limb muscles,
each innervated by a small number of excitatory and inhibitory neurons.
Several of these muscles receive dual excitatory innervation: two motor axons
supply the entire muscle, one producing a faster contraction than the other
[hence the terms `fast axon' and `slow axon' generally in use at the time
(Wiersma, 1961a)]. Staining of
crustacean muscle axons with Methylene Blue revealed profuse parallel
branching of axon terminals, with all observed muscle fibres receiving both
`fast' and `slow' axons, plus an inhibitory axon
(van Harreveld and Wiersma,
1937). Electrical recordings from these muscles showed larger
responses to `fast' axon stimulation in the majority of dually innervated
muscle fibres, and for a while it was accepted that all of the crustacean
muscle fibres were similar, and could each produce a fast or slow contraction
depending on which of the two axons was stimulated. This view was promoted in
an influential monograph on comparative neuromuscular physiology by Graham
Hoyle, in which he wrote: `... in arthropods there is in most, if not all,
instances, only one kind of muscle fibre'
(Hoyle, 1957). However, this
assertion was soon disproved by the discovery of muscle fibres with different
electrical properties in crab leg muscles
(Atwood, 1963) and by the
recognition of even more distinctive differences among muscle fibres of the
crayfish abdomen (Abbott and Parnas,
1965; Kennedy and Takeda,
1965a; Kennedy and Takeda,
1965b). In limb muscles, fibres with different electrical and
mechanical characteristics are often mixed together
(Atwood et al., 1965) while in
the crayfish abdomen, massive `twitch' muscles form the bulk of the
musculature, and a separate thin sheet of superficial muscle fibres, much
different in properties and appearance, constitutes the `tonic' musculature
responsible for abdominal postural adjustments.
Most previous studies on neuromuscular systems of crustaceans had been
concerned with the details of innervation and synaptic transmission. While
these features were assessed in the abdominal flexor muscles by Kennedy and
Takeda in their 1965 JEB publications
(Kennedy and Takeda, 1965a;
Kennedy and Takeda, 1965b),
they also had a larger aim: to discover the uses to which the two systems are
put during normal behaviour, and the mechanisms of their recruitment in the
central nervous system. The investigators demonstrated the different
behavioural roles of the two motor systems through simple but elegant
experiments. When they cut all the nerve branches supplying the superficial
(tonic) flexor muscles in an isolated abdomen, all abdominal flexor tone
disappeared and the abdomen became limp and passive. Conversely, when they cut
the nerve branches to the deep (phasic) flexors in a separate specimen, the
rapid tail flip (normally used in backward escape swimming) could not be
elicited, but slow abdominal flexion persisted. The two motor systems are
clearly linked to different behavioural acts: postural adjustments and
reflexes for the tonic system, and vigorous escape responses for the phasic
system.
The isolated crayfish abdomen also proved to be an excellent experimental
preparation for investigation of synaptic transmission at neuromuscular
junctions and of nerve impulse traffic in identified motor axons. In
unstimulated abdomens, Kennedy and Takeda observed continuous ongoing action
potentials in the motor nerves to the slow flexor muscles, and complete
silence in the much larger nerves to the fast flexor muscles
(Kennedy and Takeda, 1965a).
Having made this observation, Kennedy and Takeda went on to record the action
potentials from exposed intact nerves and showed that slow flexor axons could
be induced to change their activity by various stimuli applied to the abdomen,
demonstrating that the central nervous system mediates a wide range of
reflexive control (motor responses elicited by sensory stimulation).
The fast flexor axons are recruited by a completely separate interneuron
network, the `giant fibre' interneurons, within the central nervous system.
These interneurons form four axon tracts, and it is their large size that
ensures the rapid impulse conduction velocity required for fast reflexes.
Stimulation of any one of these large interneurons (or very strong sensory
input to head or tail of intact animals) commands a tail-flip response due to
direct and rapid excitation of the `phasic' motor neurons
(Wiersma, 1961b). Hence, these
giant interneurons are often termed `command' interneurons because they
`command' a well-defined behavioural act (for reviews, see
Kupfermann and Weiss, 1978;
Wine and Krasne, 1982). The
interneuronal networks that regulate the tonic system's reflexes do not excite
the `phasic' motor neurons. Thus, the two motor systems are controlled by
separate groups of interneurons, and form two parallel control systems with
very little interaction, either peripherally or centrally.
Elucidation of the mechanisms through which interneurons activate motor
neurons was an obvious additional target for research, and the crayfish
`phasic' motor system rapidly yielded results. Takeda and Kennedy began
investigations into the activation of flexor motor neurons within the central
nervous system by recording from their cell bodies in situ with sharp
intracellular microelectrodes, and observing their electrical responses to the
stimulation of input pathways (Takeda and
Kennedy, 1964). They and subsequent investigators found that other
interneurons besides the `giant' interneurons could activate the `phasic'
motor neurons. Eventually it was determined that the rapid flexion involved in
the escape responses shows variation according to which central pathways are
active. In an intact animal, strong stimulation of the tail produces a
different swimming response from stimuli applied to the head, because
different interneuronal pathways are activated (reviewed in
Wine and Krasne, 1982). Many
additional details of central control were added over the next two decades
(for reviews, see Wine and Krasne,
1982; Page, 1982).
Behaviourally, escape swimming is generally more stereotyped and rapid than
the much more variable and subtle movements that are regulated by the tonic
axons and their associated networks of interneurons.
An additional goal of Kennedy and Takeda's work
(Kennedy and Takeda, 1965a;
Kennedy and Takeda, 1965b) was
to clarify the functional role of peripheral inhibition. Most crustacean
muscles are innervated by one or two inhibitory axons, but the biological
functions of peripheral inhibition were not very well understood in the early
1960s. An important JEB paper by Brian Bush showed that reflexes involved in
claw opening and closing include firing of peripheral inhibitory axons to
weaken contractions of antagonistic muscles that would interfere with the
reflex activity (Bush, 1962).
Kennedy and Takeda found that both phasic and tonic flexor muscles receive
inhibitory innervation, and they addressed the question of the role of these
inhibitory axons by recording from them and their innervated muscles during
reflex activities (Kennedy and Takeda,
1965a; Kennedy and Takeda,
1965b). In both sets of muscles, peripheral inhibition did not
have much effect on the amplitude of excitatory postsynaptic potentials (the
electrical responses of the muscle fibre membrane, generated by
neurotransmission at excitatory synapses, that are responsible for eliciting
contraction of the muscle fibre), but it did shorten their time courses. This
observation led to the conclusion that inhibition serves to repolarize the
muscle fibres following excitation, thereby speeding muscle relaxation in
preparation for a subsequent contraction, and improving the temporal precision
of movement. The inhibitory axon of the slow flexor muscles is often recruited
during central suppression of activity in the excitatory axons
(Kennedy and Takeda, 1965b),
indicating central inhibition of excitatory motor neurons along with central
activation of the inhibitory neurons, and also a major role for the inhibitory
neuron in the rapid termination of ongoing contractions. Improvement of
temporal precision is also attributed to inhibitory axons of crustacean limb
muscles (Bush, 1962), which
suppress electrical activity most strongly in slowly contracting muscle fibres
(Atwood, 1973). Although
central mechanisms of recruitment for peripheral inhibitory neurons differ in
limb and abdominal motor systems, the general role of improving the temporal
precision of movement can be assigned to inhibitors in both cases.
The parallel phasic and tonic motor systems of the crayfish abdomen were
not the first to be discovered, since it had been known for some time that
slow (tonic) and fast (twitch) muscle fibres with separate innervation occur
in muscles of amphibians (Kuffler and
Vaughan Williams, 1953; Tasaki
and Mizutani, 1944). However, the amphibian studies lacked a
behavioural context, which the crustacean studies supplied. The principle of
differential recruitment of phasic and tonic motor systems for specific acts
was subsequently found to apply in mammals as well. For example, in the medial
gastrocnemius muscle of the cat, only about 25% of the motor unit pool
innervating slow-twitch muscle fibres is used for posture and walking; about
60% of the motor unit pool innervating `fast fatigable' muscle fibres is used
only for demanding efforts such as jumping
(Burke, 1980). Apparently,
evolutionary forces have resulted in this disproportionate allocation of
muscle fibre types in many muscles of different species. A premium is put on
large fast muscles or motor units that can be kept in reserve for demanding
situations.
Many studies on reflex control of swimming and abdominal movement followed
the initial studies of Kennedy and Takeda
(Kennedy and Takeda, 1965a;
Kennedy and Takeda, 1965b).
Gradually, a fairly complete circuit for crayfish escape behaviour, mediated
by the phasic motor system, was worked out by a number of investigators, many
of whom worked in Donald Kennedy's laboratory at Stanford University (reviewed
by Wine and Krasne, 1982).
Details of circuits involved in postural control were also elucidated
(reviewed by Page, 1982). In
addition to stimulating research on dual motor systems, their regulation by
the central nervous system, and patterns of connectivity between motor neurons
and muscle, the studies on the crayfish abdomen launched by Kennedy and Takeda
(Kennedy and Takeda, 1965a;
Kennedy and Takeda, 1965b) also
gave rise to easily made preparations widely used in teaching laboratories as
an introduction to hands-on neurophysiology. This lasting legacy has been
invaluable for many generations of students, and will continue.
Footnotes
Harold Atwood discusses Donald Kennedy and Kimihisa Takeda's 1965 papers describing the crayfish `phasic' motor system, involved in escape behaviour, and the `tonic' system, involved in postural control. Both papers can be accessed from http://jeb.biologists.org/content/vol43/issue2
References
Abbott, B. C. and Parnas, I. (1965). Electrical
and mechanical responses in deep abdominal extensor muscles of crayfish and
lobster. J. Gen. Physiol.
48,919
-931.
Atwood, H. L. (1963). Differences in muscle fibre properties as a factor in `fast' and `slow' contraction in Carcinus.Comp. Biochem. Physiol. 10,17 -32.[Medline]
Atwood, H. L. (1973). Crustacean motor units. In Control of Posture and Locomotion (ed. R. B. Stein, K. G. Pearson, R. S. Smith and J. B. Redford), pp.87 -104. New York: Plenum Press.
Atwood, H. L., Hoyle, G. and Smyth, T. (1965).
Mechanical and electrical responses of single innervated crab-muscle fibres.
J. Physiol. 180,449
-482.
Burke, R. E. (1980). Motor unit types: functional specialization in motor control. TINS 3, 255-258.[CrossRef]
Bush, B. M. H. (1962). Peripheral reflex
inhibition in the claw of the crab, Carcinus maenas. J. Exp.
Biol. 39,71
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Hoyle, G. (1957). Comparative Physiology of the Nervous Control of Muscular Contraction. Cambridge: Cambridge University Press.
Kennedy, D. and Takeda, K. (1965a). Reflex
control of abdominal flexor muscles in the crayfish. I. The twitch system.
J. Exp. Biol. 43,211
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Kennedy, D. and Takeda, K. (1965b). Reflex
control of abdominal flexor muscles in crayfish. II. The tonic system.
J. Exp. Biol. 43,229
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Kuffler, S. W. and Vaughan Williams, E. M.
(1953). Small-nerve junction potentials. The distribution of
small motor nerves to frog skeletal muscle, and the membrane characteristics
of the fibres they innervate. J. Physiol.
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Kupfermann, I. and Weiss, K. R. (1978). The command neuron concept. Behav. Brain Sci. 1, 3-39.[Medline]
Page, C. H. (1982). Control of posture. In The Biology of Crustacea, Vol.4 (ed. D. C. Sandeman and H. L. Atwood), pp.33 -59. New York: Academic Press.
Takeda, K. and Kennedy, D. (1964). Soma potentials and modes of activation of crayfish motoneurons. J. Cell. Comp. Physiol. 64,165 -181.[Medline]
Tasaki, I. and Mizutani, K. (1944). Comparative studies of the activities of the muscle evoked by two kinds of motor nerve fibres. Part I. Myographic studies. Jap. J. Med. Sci. 10,237 -244.
van Harreveld, A. and Wiersma, C. A. G. (1937). The triple innervation of crayfish muscle and its function in contraction and inhibition. J. Exp. Biol. 14,448 -461.[Abstract]
Wiersma, C. A. G. (1961a). The neuromuscular system. In The Physiology of Crustacea, Vol.2 (ed. T. H. Waterman), pp.191 -240. New York: Academic Press.
Wiersma, C. A. G. (1961b). Reflexes and the central nervous system. In The Physiology of Crustacea, Vol. 2 (ed. T. H. Waterman), pp. 241-279. New York: Academic Press.
Wine, J. J. and Krasne, F. B. (1982). The cellular organization of crayfish escape behavior. In The Biology of Crustacea, Vol. 4 (ed. D. C. Sandeman and H. L. Atwood), pp. 241-292. New York: Academic Press.
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