Tension sensitivity of the heart pacemaker neurons in the isopod crustacean Ligia pallasii
,*
Department of Biological Sciences, University of Calgary, Calgary,
Alberta T2N 1N4, Canada
Present address: Department of Biology, Georgia State University, Atlanta, GA
30303, USA
* Author for correspondence (e-mail: akira{at}gsu.edu)
Accepted 23 September 2002
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Summary |
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Key words: heart pacemaker, cardiac ganglion, proprioceptive feedback, single neuron reflex, stretch sensitivity, tension sensitivity, crustacean, isopod, Ligia pallasii
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Introduction |
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In a variety of rhythmic motor systems, proprioceptive feedback plays
important roles, such as changing the amplitude and the frequency of ongoing
movement and cycle-by-cycle correction of rhythmic behaviors
(Rossignol et al., 1988).
Proprioceptive feedback is generally formed by afferent mechanosensory
neurons, or proprioceptors, that are found even in peripherally located
central pattern generators (CPGs) such as the crustacean stomatogastric
nervous system (Simmers and Moulins,
1988
; Katz et al.,
1989
). In crustacean hearts, it has long been proposed that the
pacemaker activity of the CG neuron is strongly affected by rhythmic
ventricular movement through an unknown feedback system within the heart
(Carlson, 1906
;
Maynard, 1960
;
Holley and Delaleu, 1972
;
Kuramoto and Ebara, 1984
,
1985
; Cooke,
1988
,
2002
). As there are no sensory
neurons in the heart, it has been assumed that the CG neurons themselves
possess mechanosensitivity. Alexandrowicz
(1932
) reported that dendrite
processes of the CG neurons near the ganglion trunk differ from their major
peripheral processes and that they are sensitive to mechanical stimulation. He
suggested that these fine dendrites mediate the stretch-induced responses of
the CG neurons. Since then, several investigators have attempted to show the
direct effects of continuous stretch or inflation of the heart on the
heartbeat rhythm (e.g. Maynard,
1960
; Kuramoto and Ebara,
1984
,
1985
;
Wilkens, 1993
). However,
direct evidence for the cycle-by-cycle feedback from the heart muscle to the
neurons has not been presented. In the present study, we investigated the
effects of passive stretch and active muscle contraction on the bursting
activity of CG neurons by using opened heart preparations obtained from the
isopod crustacean Ligia pallasii.
The Ligia tubular heart is composed of a single layer of striated
muscle fibers aligned in a right-hand spiral
(Fig. 1A;
Alexandrowicz, 1953;
Yamagishi and Ebara, 1985
).
Unlike decapod hearts, the heart muscle possesses myogenicity that is usually
hidden by the neurogenic drive from the CG
(Yamagishi and Hirose, 1997
;
Yamagishi et al., 1998
). The
Ligia CG is composed of six neurons that lie longitudinally along the
midline of the inner dorsal wall (Fig.
1B). All of the six CG neurons are endogenous bursters and they
fire synchronously due to strong electrical coupling between them
(Yamagishi and Ebara, 1985
).
In addition to the pacemaker function, they also function as the glutamatergic
motoneurons innervating the heart muscle
(Sakurai et al., 1998
) and
they exhibit both spike-mediated and graded neuromuscular transmission to the
heart muscle (Sakurai and Yamagishi,
2000
). Taking advantage of such simplicity, together with
knowledge of the Ligia heart obtained from previous studies, we
report here that contraction of the heart muscle affects the bursting activity
of CG neurons by directly affecting their membrane potential. Some of the
present results were previously published in an abstract form
(Sakurai and Wilkens,
2000
).
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Materials and methods |
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Heart preparations
Isolated heart preparations were made as described elsewhere
(Sakurai et al., 1998;
Sakurai and Yamagishi, 2000
).
After decapitation, the animal was pinned ventral side up in the experimental
chamber and the heart was exposed by removing the ventral carapace, ventral
nerve cord and visceral organs. At this point, the maximum and minimum values
of the diameter of a beating tubular heart were measured at the seventh body
segment under the microscope to calculate changes in the circumference. The
calculated values were later used to determine the physiological range of the
width changes imposed on the opened heart by stretches
(Fig. 2B). Next, the heart was
opened by longitudinal incision of its ventral wall. The preparation was then
pinned dorsal side up and the heart was exposed from the dorsal side along the
midline. The suspensory ligaments were all removed except for the pericardial
septum. After these treatments, the opened heart became a membranous muscular
sheet suspended from the remained lateral rims of the tergites by pericardial
septum. The preparation was then laid across two Sylgard stages with the
ventral side up. The tergites were all pinned firmly onto the stages
(Fig. 1C). One stage was fixed
onto the bottom of the chamber and the other was connected to a servomotor
(Model 300 Ergometer, Cambridge Technology, Cambridge, MA, USA) with a steel
wire. For intracellular recordings from the CG neuron, the posterior region of
the ganglionic trunk was desheathed to expose the somata. Then, the posterior
half of the heart wall was pinned extensively onto the fixed stage to prevent
movement by stretching (Fig.
5A). After these procedures, the preparation was left for at least
2 h in running saline to restore regular heartbeat.
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|
Stretching the heart wall
By moving the unfixed stage, the opened heart could be either stretched or
slackened. Direction of the stretch was carefully adjusted to be in parallel
with the muscle fibers. The control position of the unfixed stage was adjusted
to set the width of the opened heart to be the median value of the calculated
circumferential changes. At the control position, the heart muscle was under
moderate tension. To produce brief stretches and sinusoidal stretches, square
pulses and sinusoidal waveforms were generated by a conventional function
generator; they were sent to the servomotor input. The square pulses were
smoothed by a hand-made RC circuit to prevent abrupt stretches that would
cause severe damage to the heart and surrounding connective tissues. In most
recordings, the magnitude of the applied stretch was shown by the command
output from the RC circuit, which was calibrated later as the distance of the
displacement of the unfixed stage. In some experiments the changes in the
opened heart width was directly measured under the microscope during the
experiments, as the actual dimension change was slightly less than the
amplitude of the displacement due to elasticity of connective tissues
(Fig. 2B).
Solutions
Throughout the experiments, the experimental chamber was continuously
perfused with aerated physiological saline of the following composition: NaCl
577 mmol l-1, KCl 14 mmol l-1, CaCl2 25 mmol
l-1, MgCl2 21 mmol l-1,
Na2SO4 4.5 mmol l-1 and Tris 5 mmol
l-1 (Yamagishi and Ebara,
1985). The pH was adjusted to 7.4-7.6 using HCl. In some
experiments, tetrodotoxin (TTX; Sigma), Joro spider toxin (JSTX; Sigma) and
picrotoxin (Sigma) were added to the saline. They were made up in saline just
before use.
Electrophysiology
Conventional glass capillary microelectrodes filled with 3 mol
l-1 KCl (resistance, 15-30 M) were used for recording
intracellular electrical activity of the heart muscle and the CG neuron. The
tension of the heart muscle was recorded by connecting the unfixed stage to a
Pixie force transducer (developed by R. K. Josephson and D. Donaldson;
reported by Miller, 1979
).
Although we attempted to measure the isometric tension generated by the heart,
the muscle still shortened a small amount due to elasticity of the muscle
itself and the surrounding connective tissues. The electrical signals were
sent to a personal computer via an A/D converter with commercial data
acquisition software (Experimenter's WorkBench, DataWave, Longmont, CO,
USA).
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Results |
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The EJP burst frequency decreased with increased stretch amplitude; however, the EJP burst frequencies showed a nonlinear relationship with the dimension changes of the heart (Fig. 2B). Stretches that changed the opened heart width within the physiological dimension range (shown by a horizontal bar in the graph) had little effect on the ganglionic burst frequency. The stretch-induced inhibition became apparent when the heart was stretched more than the estimated diastolic dimension.
Brief stretches caused phase shifts in ganglionic bursting
activity
To determine whether there is any cycle-by-cycle feedback from the heart
muscle to the CG, we examined the effects of brief stretches applied at
various times during the inter-burst period
(Fig. 3). A brief stretch
produced either phase advance or phase delay of the ganglionic burst cycle,
depending on the phase of the cycle in which it was presented.
Fig. 3A shows representative
records showing the effects of brief stretches (200 ms duration, 0.7 mm
amplitude) applied at two different phases of the burst cycle. When the
stretch was presented immediately after the first EJP, the second EJP in the
burst was suppressed and the following burst cycle was advanced
(Fig. 3Ai). By contrast, when
the stretch was presented at a later phase, the occurrence of the next burst
was delayed (Fig. 3Aii). The
phaseresponse curve increased monotonically as the stretch was applied
at later phases of the burst cycle (Fig.
3B). The graph shows the occurrence of both phase advance and
phase delay, with a null point located between 20% and 50% of the burst
interval (N=3).
|
Repetitive brief stretches entrained the ganglionic bursting activity to either higher or lower frequencies than the free-run burst rate. (Fig. 4). In the preparation shown in Fig. 4A, the free-run burst rate was in the range of 1.44-1.61 Hz. Brief stretches (duration, 300 ms; amplitude, 0.7 mm) were applied at (i) 1.0 Hz, (ii) 1.3 Hz, (iii) 1.7 Hz and (iv) 2.0 Hz. When the stretches were applied at frequencies slightly lower (Fig. 4Aii) or higher (Fig. 4Aiii) than the free-run frequency, the EJP bursts became entrained to the applied stretches. The CG bursts could not follow the stretches applied at 1.0 Hz and 2.0 Hz, and the burst rhythm became irregular (Fig. 4Ai,iv). The EJP bursts had one-to-one relationships with the brief stretches from 1.1 Hz to 1.8 Hz (Fig. 4B).
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Throughout the experiments, we often noticed that the brief stretches also
caused hyperpolarizing deflections in the heart muscle (e.g.
Fig. 3Aii). This phenomenon
probably resulted from a sudden cessation of tonic transmitter release from
the CG neurons (cf. Sakurai and Yamagishi,
2000), which was induced by a stretch-induced hyperpolarization
(see below). However, we cannot exclude the possibility that the heart muscle
may also respond to stretch in the same way as do molluscan heart muscles
(Irisawa, 1978
;
Jones, 1983
). In this study we
made no further investigation into this problem.
Membrane potential responses of CG neurons to passive stretch
We next examined the membrane potential response of the CG neuron to the
stretch. As the six CG neurons are all electrically coupled, local signals
evoked in one neuron can propagate electrotonically to all the other neurons
(Yamagishi and Ebara, 1985;
Yamagishi et al., 1989
).
Taking advantage of this, we applied stretches to the anterior half of the
heart while recording the stretch-induced response from one of the CG neurons
in the posterior half (Fig.
5A). To observe the responses clearly, preparations with a
bursting rate of <0.5 Hz were selected for the experiments. The stretches
were applied during the inter-burst period when the membrane potential became
flat.
Stretching the heart wall produced a hyperpolarizing membrane potential change in the CG neuron (Figs 5, 6). When brief stretch pulses were applied repeatedly at 5 s intervals, the CG neuron exhibited a hyperpolarizing response during each stretch (Fig. 5B). Each hyperpolarizing response was always followed by a rebound burst discharge. As a result, the weakly active CG neuron exhibited rhythmical bursts that were time-locked to the brief stretches. Sinusoidal stretches caused sinusoidal membrane potential changes reflecting the stimulus waveform (Fig. 5C,D). The CG neuron became hyperpolarized at the peak of the sinusoidal stretch and was depolarized and often fired action potentials at the trough of the stretch.
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The amplitude of the hyperpolarizing responses increased with increased stretch amplitude (Fig. 6A-C). In normal saline, the hyperpolarizing response became maximum at the beginning of the stretch, and then the membrane slowly depolarized during the stretch (Fig. 6Bi). Relaxation of the heart wall from the control position (downward deflection of the stimulus trace) also induced a burst discharge (Fig. 6Ai) or a slow depolarization (Fig. 6Bi). The rebound burst discharges appeared earlier with increased duration and/or amplitude of the stretches (Fig. 6Ai,D). The hyperpolarizing responses were still observed when neural firing was completely blocked by 1 µmoll-1 TTX (Fig. 6Aii). In TTX, the membrane potential stayed at a relatively constant level during the stretch (Fig. 6Bii), and no depolarizing response was induced upon relaxation. In TTX, the hyperpolarizing responses were evoked only when the stretch amplitude became more than 0.2 mm (Fig. 6C). Similar results were obtained from all four preparations examined.
In one preparation, we examined the effect of Ca2+-free saline and picrotoxin (1 mmoll-1), both of which block inhibitory synaptic input from the extrinsic cardioinhibitory neurons (H. Yamagishi, personal communication), on the stretch-induced hyperpolarization. The stretch-induced response was little affected by either treatment, suggesting that the hyperpolarizing response was not mediated by local activation of the inhibitory neurons or any other unknown inhibitory synapses.
Effects of heart muscle contraction on membrane potential activity of
the CG neurons
The preceding experiments have demonstrated the effects of artificially
applied stretches to the heart wall. However, it was still unclear whether the
increased tension or the increased dimension of heart muscle caused the
hyperpolarizing responses of CG neurons. To solve this problem, we next
attempted to determine the relationship between the active muscle tension and
the membrane potential of the CG neuron.
In the Ligia heart, we could not produce measurable muscle tension
by directly injecting a depolarizing current into a muscle fiber due to very
low input resistance. Instead, we took advantage of the myogenicity of the
heart muscle. The myogenicity can be pharmacologically isolated from the
ganglionic drive by blocking the CG-evoked EJPs in the heart muscle with 10
µmoll-1 JSTX (Yamagishi et
al., 1998; Sakurai and
Yamagishi, 2000
). Moreover, the myogenic contraction is little
affected by tetrodotoxin TTX, which blocks ganglionic bursting activity
(Yamagishi and Hirose, 1997
).
By using JSTX in combination with TTX, we examined the effects of spontaneous
muscle contraction on the membrane potential of the CG neuron.
The spontaneous muscle contraction caused a hyperpolarizing membrane potential change in the CG neuron (N=12). Fig. 7 shows representative recordings of the membrane potential activity of the CG neuron and the isometric tension of the heart muscle obtained successively from a single preparation. In this preparation, the CG neuron exhibited regular bursting activity (burst frequency, 0.84-0.88 Hz) in the normal saline. Each CG burst caused a twitch of the heart muscle, showing a transient increase in tension (Fig. 7A). After application of 10 µmoll-1 JSTX, the periodic contraction of the heart muscle was temporary abolished, but the CG neuron still fired regularly at a slightly lower frequency (0.79-0.82 Hz) than the control frequency (Fig. 7B). Approximately 5 min after the application of JSTX, the heart muscle started to exhibit myogenic contraction independently from the CG burst (Fig. 7C). At this moment, the contraction occurred in several loci in the heart wall at different rhythms. Under such conditions, the CG burst became irregular and the pacemaker potential of the CG neuron appeared to be interrupted by periodic hyperpolarizing deflections. The hyperpolarizing deflections in the CG neuron corresponded with the periodic increases in tension of the heart muscle (indicated by lines in Fig. 7C). The hyperpolarizing deflections became more apparent when the CG neuron depolarized.
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When the CG burst was abolished by the addition of 1.0 µmoll-1 TTX, the hyperpolarizing deflections in the CG neuron were seen more clearly corresponding to each muscle contraction (Fig. 7D). Following washout of TTX, the recovered burst discharges tended to occur shortly after each hyperpolarization, as if they were evoked by post-inhibitory rebound (Fig. 7E). In this condition, the bursting activity of CG neurons appeared to be entrained by the myogenic activity of the heart muscle. Thus, the spontaneous muscle contraction had similar effects to the brief stretch, both causing an initial hyperpolarization that was immediately followed by a burst discharge in the CG neuron. This relationship lasted for approximately 40 min after washout of JSTX until the muscle became driven again by the CG burst (not shown). These results strongly support the idea that muscle contraction during the heartbeat affects the pacemaker activity of the CG neurons.
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Discussion |
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In the opened heart preparation made from the isopod tubular heart, the CG is located on a single layer of muscle fibers, and all neural processes are constantly exposed to the freshly perfused saline. Thus, the mechanical stimulation to the heart does not cause changes in delivery of fresh saline. Furthermore, we demonstrated that a brief stretch could phase shift the CG burst cycle (Fig. 3), and that repetitive brief stretches could either accelerate or slow down the ganglionic bursting via repetitive phase advances or phase delays (Fig. 4). These results strongly support the idea that mechanical stimulation to the heart wall affects the pacemaker activity of the CG neurons on a cycle-by-cycle basis.
Membrane potential response of the CG neurons to tension of the heart
muscle
The CG neuron showed a hyperpolarizing membrane potential change in
response to a stretch applied to the heart muscle (Figs
5,
6) and during a spontaneous
muscle contraction (Fig. 7). A
common event underlying the passive stretch (expansion) and the active
contraction (shortening) is the increase in tension of the heart muscle.
Therefore, we conclude here that increased muscle tension, no matter how it is
produced, causes hyperpolarization in the CG neuron and consequently inhibits
the ganglionic pacemaker activity.
In weakly active CG neurons, the stretch and muscle contraction induced
rebound excitation upon release from the stretch (Figs
2,
5,
6). The latency of the rebound
burst discharge shortened with increased amplitude and duration of the
stretches (Fig. 6C). It is
likely that the tension-induced hyperpolarization and the rebound bursting are
the underlying mechanisms of the stretch-induced inhibition and the following
rebound acceleration of the CG burst rate
(Fig. 2), phase shifting
(Fig. 3) and the entrainment of
the CG burst cycle (Fig. 4).
The sequences of phase shifting and entrainment of the ganglionic bursting
activity are probably similar to those of the inhibitory synaptic inputs onto
endogenous burster as described elsewhere (e.g.
Maynard, 1961; Pinsker,
1977a
,b
).
In general, proprioceptors become excited in response to passive stretch or
active contraction of the muscles upon which their sensory processes project
(e.g. Wiersma et al., 1953;
Kuffler, 1954
;
Eyzaguirre and Kuffler, 1955
;
Eckert, 1961
;
Eagles, 1978
;
Proske, 1981
;
Parsons, 1982
;
Hartman, 1985
). Primary
transduction of receptor neurons is generally believed to be linked to the
opening of ionic channels (Edwards,
1983
). It has been shown in abdominal stretch receptors in
crayfish that the stretch-activated channel has low cation selectivity,
including sodium, potassium, calcium and magnesium (Nakajima and Onodera,
1969a
,b
;
Brown et al., 1978
;
Erxleben, 1989
;
Rydqvist and Purali, 1993
).
Our data showed that the tension-induced responses of the CG neuron were in
the hyperpolarizing direction (Figs
5,6,7),
and the responses became more apparent when the CG neuron was depolarized
(Fig. 6C). These results
indicate that the tension-induced hyperpolarization was produced by increased
ion conductance with the reversal potential located at a more hyperpolarized
level than the resting potential. In addition, TTX-sensitive sodium
conductance may also be activated directly by tension or indirectly
via the tension-induced hyperpolarization, as (1) relaxation from a
stretch induced a burst discharge or a slow depolarization in the CG neuron,
but no such response was induced in TTX
(Fig. 6A), and (2) the
stretch-induced hyperpolarization gradually decreased in amplitude during the
stretch but stayed relatively constant in TTX
(Fig. 6B). Such inward current
may contribute to the rebound excitation and the phase-advance of the CG burst
cycle. In this study, no further attempts were made to identify which ion
channels mediate the hyperpolarizing responses of the CG neurons. To
characterize the tension-sensitive ion conductances, pharmacological analyses
using ion-channel blockers and ion-substitution experiments under voltage
clamp are further needed.
At present, it is still unknown where the tension-sensitive sites are
located in the processes of the CG neurons. In Ligia exotica, fine
dendrite processes were observed emerging from the ganglionic trunk region
(Sakurai and Yamagishi, unpublished observation). These proximal dendrites
appeared similar to the hypothetical stretch-sensitive dendrites described in
the decapod CG by Alexandrowicz
(1932). Detailed anatomy of the
CG neurons should further be examined.
Functional significance of stretch sensitivity of the CG neuron
In the open circulatory system of crustaceans, the heart functions as a
suction force pump suspended in the pericardial cavity by the elastic
ligaments (Maynard, 1960).
Tension of the heart muscle becomes maximum during systole, when the muscles
generate the maximum force to overcome the vascular resistance and to extend
the suspensory ligaments. By contrast, diastolic expansion is produced by the
elastic recoil of the suspensory ligaments. The muscle tension will decline
until it equals the recoiling force of the ligaments, which also declines as
the heart dilates. Therefore, in an intact beating heart, the tension-induced
hyperpolarization in the CG neurons most likely occurs during the systolic
contraction, whereas the rebound excitation occurs during diastole.
The actual sequence of events in a beating heart is schematically drawn in
Fig. 8A. The CG burst causes a
transient increase in the muscle tension via excitatory neuromuscular
transmission (a). The increased muscle tension then returns the
hyperpolarizing feedback to the CG neurons (b-). This
tension-induced hyperpolarization may help terminate ongoing burst and thus
may play a role in preventing sustained bursting that will cause a harmful
systolic arrest. The tension-induced hyperpolarization may also act as a
common inhibitory input to all of the six CG neurons to enhance their
synchronized bursting activity (e.g.
Kandel et al., 1969;
Pinsker, 1977b
), although it
has been shown previously that the synchronization of the membrane potential
activity is produced mainly by the strong electrical coupling
(Yamagishi and Ebara, 1985
).
By contrast, relaxation of the muscle induces a following discharge in the CG
neuron b+), which can consequently keep the heart rate slightly
higher than the free-run burst rate by causing repetitive phase advances in
the CG burst cycle. This idea is supported by the fact that the burst
frequency of the CG neuron slightly decreased when the muscle contraction was
temporary abolished by JSTX (Fig.
7B). Altogether, the tension-induced feedback may contribute to
the establishment of a regular rhythm and the optimum motor output for ongoing
heartbeat.
|
There have been a number of studies of extrinsic cardioregulation in
crustaceans (Maynard, 1960;
Prosser, 1973
;
Cooke, 2002
). In Ligia
exotica, heart rate and contraction force of the heart muscle are both
regulated by the cardioregulatory axons (CI, CA1 and CA2) projected from the
central nervous system (Yamagishi et al.,
1989
; Sakurai and Yamagishi,
1998a
,b
).
Together with the present results, the heart rate and the contraction force
are optimized intrinsically via the tension-sensitive feedback of the
CG neurons themselves (short-range feedback), whereas the total cardiac output
is extrinsically controlled from the central nervous system through the
extrinsic regulatory neurons and neurohormones (long-range feedback) in
response to various behavioral changes and metabolic demands. It will be
interesting to determine how the tension sensitivity of the CG neurons is
modified by the extrinsic regulatory inputs.
The CG neuron forms a single neuron reflex arc
In the Ligia heart, all of the six CG neurons act as the primary
pacemaker for the heartbeat by exhibiting endogenous bursting activity
(Yamagishi and Ebara, 1985).
They also function as the glutamatergic motoneurons innervating the heart
muscles (Sakurai et al.,
1998
). Together with the present results, we conclude here that
the CG neurons are multifunctional neurons that possess tension sensitivity in
addition to their pacemaker and motor functions.
There have been several examples of the multifunctional neurons that are
suggested to form a `single neuron reflex arc' (in the Hydra nervous
system, Westfall and Kinnamon,
1978; Westfall et al.,
1991
; in the pharynx of the nematode Caenorhabditis
elegans, Raizen and Avery,
1994
; Avery and Thomas,
1997
). The neurosecretory cells possessing a sensory function have
also been reported in various animals (in the leech Hirudo
medicinalis, Wenning et al.,
1993
; in the lobster Homarus,
Pasztor and Bush, 1989
; in the
carotid body of mammals, González
et al., 1992
; reviewed by
Wenning, 1999
). A number of
sensory neurons are known to function as elements of the pattern generator
circuits (e.g. crayfish locomotion, Sillar
et al., 1986
; locust flight,
Pearson et al., 1985
; lamprey
swimming, Grillner et al.,
1991
). Having sensory receptors as functional elements of the
pattern generator provides the automatic regulation of rhythmical motor output
appropriate for the mechanical state of motor organ in various external
conditions (Pearson, 1993
). To
our knowledge, this study is probably the first report that
electrophysiologically demonstrated single multifunctional CPG neurons having
mechanosensitivity in addition to the endogenous pacemaker function and the
motoneuronal function. By having a sensory-motor function without any
intermediate synapses, the CG neurons may form the single neuron reflex arc
within the heart.
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Acknowledgments |
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References |
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