Serotonergic modulation of nonspiking local interneurones in the terminal abdominal ganglion of the crayfish
Division of Biological Sciences, Graduate School of Science, Hokkaido University, 060 Sapporo, Japan
e-mail: tn110{at}hucc.hokudai.ac.jp
Accepted 24 June 2002
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Summary |
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Sensory stimulation elicited depolarizing or hyperpolarizing potentials in the nonspiking interneurones and excitatory postsynaptic potentials (EPSPs) and spikes in the spiking interneurones. The sensory responses of spiking interneurones increased during bath application of serotonin and were reduced after 20-30 min of washing with normal saline. In the nonspiking interneurones, the amplitude of both depolarizing and hyperpolarizing potentials increased without any direct correlation with the serotonin-mediated potential change. This effect of serotonin was long-lasting and continued to enhance the responses of the nonspiking interneurones after washing. This postserotonin enhancement persisted for over 1 h.
Key words: crayfish, Procambarus clarkii, serotonin, interneurone, nonspiking
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Introduction |
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Nonspiking local interneurones are widely distributed in the central
nervous system of the arthropods and are essential neural elements producing
and modulating movements (e.g. Burrows,
1992; Nagayama et al.,
1984
,
1994
). In the terminal
abdominal ganglion of the crayfish, there are approximately 30 pairs of
nonspiking interneurones that have unilateral and bilateral anatomy (Nagayama
and Hisada, 1987
,
1988
;
Nagayama et al., 1997
). The
majority of these nonspiking interneurones have a unilateral structure and are
classified into PL and AL groups by their gross morphology and somatic
position. The PL interneurones are further classified into three identified
sets of interneurones while the AL interneurones form three subgroups
(Nagayama et al., 1997
). The
PL and AL interneurones play a major role in gaining control of the activity
of motor neurones innervating the uropod muscles, by receiving both peripheral
and central inputs and controlling the tonic background activity of the uropod
motor neurones (Nagayama,
1997
; Namba et al.,
1994
). To understand further the underlying organizational
principles on which these circuits are based, it is important to understand
how serotonin affects the activity of the nonspiking interneurones and
modulates their synaptic responses. We have, however, little information about
serotonergic modulation of nonspiking interneurones in arthropods. In this
paper I show for the first time that nonspiking interneurones are depolarized
or hyperpolarized by bath application of serotonin, although spiking
interneurones of both intersegmental and local groups are not affected
significantly. Furthermore, the synaptic interactions between sensory
afferents and nonspiking interneurones are enhanced and prolonged by
serotonin.
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Materials and methods |
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To monitor uropod motor activity and to stimulate sensory afferents
innervating the exopodite, the soft cuticle overlying the uropod muscles was
removed along the lateral edge of the protopodite and exopodite. The
underlying hypodermis, ventral blood vessel, and connective tissue were
removed to expose the muscles and nerves. Motor neurones innervating the
uropod muscles all originate in the terminal abdominal ganglion. They were
identified according to the criteria previously described
(Nagayama et al., 1983;
Nagayama, 1999
). The exopodite
reductor motor neurone exits from the second nerve root. The activity of this
motor neurone was recorded at the bifurcation to the reductor and adductor
exopodite muscles with the use of an extracellular suction electrode. To
stimulate the sensory afferents innervating the exopodite electrically,
another suction electrode was placed on the second root sensory bundle
ipsilateral to the recording electrode for the motor neurones.
Intracellular recordings were made in the terminal ganglion neuropil with
glass microelectrodes filled with either 2 mol l-1 potassium
acetate (40-50 M) or a 3% solution of Lucifer Yellow CH dissolved in
0.1 mol l-1 lithium chloride (100-200 M
). Penetrations of
nonspiking local interneurones were confirmed by criteria previously described
(Nagayama et al., 1997
).
Stable and long recordings (more than 1 h) are prerequisite for experiments of
bath application, so the responses of nonspiking interneurones were mainly
characterized by using microelectrodes filled with potassium acetate. Since
the PL and AL nonspiking interneurones form opposing parallel connections in
the local circuit (Nagayama and Hisada,
1987
; Namba et al.,
1994
), they are physiologically identified by the combination of
their response to sensory stimulation and output effect upon reductor motor
neurone. Penetrations of intersegmental ascending interneurones and spiking
local interneurones were confirmed by the intracellular injections of Lucifer
Yellow. They were later identified by their gross morphology according to
criteria based on Nagayama et al.
(1993a
,b
).
For bath application of serotonin, the chamber (8 ml volume) was constantly perfused with fresh saline at a rate of 4 ml min-1 using a microtube pump (MP-3; Eyela, Tokyo, Japan). After physiological characterisation, interneurones were rested for more than 2 min with a continuous perfusion of normal saline. Serotonin of the required concentration was dissolved in normal saline and then perfused for 3-5 min. The preparations were then washed out with normal saline. In some preparations, small quantities of serotonin at concentrations of 0.1 µmol l-1 were applied via pressure microinjection from micropipettes into the lateral neuropil of the terminal ganglion near the intracellular recording site. The tips of micropipettes were broken manually under a microscope to be approximately 5 µm in outer diameter and serotonin was ejected from the penetrated micropipette by N2 gas pressure controlled by pneumatic picopump (PV830, WPI) at 69-138 kPa for 100 ms.
All recordings were stored on a PCM data recorder and displayed on a Gould electrostatic chart recorder. Interneurones in which the response did not recover after washing were excluded from the results. The results are based on 15 stable recordings from nonspiking interneurones and 10 spiking interneurones of both ascending (8) and local (2) groups from 75 crayfish.
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Results |
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Fig. 1B shows the response of the reductor motor neurone during serotonin perfusion. The motor neurone showed a continuous hyperpolarization with no spikes after bath application of 1 mmol l-1 serotonin that recovered by washing with normal saline. The input resistance of the motor neurone, measured by brief pulses of 1 nA hyperpolarizing current, was reduced by 20-30% (23±5.8%, mean ± S.D., N=3) during membrane hyperpolarization mediated by serotonin.
Hyperpolarizing and depolarising response of nonspiking interneurones
during bath application of serotonin
During bath application of serotonin at 100 µmol l-1 for 3-5
min, 9 out of 15 nonspiking local interneurones showed a membrane
hyperpolarization while the remaining six interneurones showed a
depolarization accompanied by a decrease in the spike frequency of the
reductor motor neurone. Fig. 2A
shows an example of serotonin-mediated hyperpolarization of a nonspiking
interneurone. The membrane potential began to shift negatively during
serotonin application and reached 30 mV in amplitude after 7 min from the
beginning of serotonin perfusion. This sustained hyperpolarization of the
interneurone was maintained for approximately 10 min, recovered gradually and
returned to the initial level after approximately 60 min of washing. The
effective period of serotonin-mediated depolarization of the nonspiking
interneurones was rather shorter than that of serotonin-mediated
hyperpolarization, and the membrane potential of the interneurones frequently
recovered to initial levels within 20 min of washing
(Fig. 2B). The peak amplitude
of hyperpolarization of the nonspiking interneurones was 18.6±5.7 mV
(N=9) and the time course of recovery was 47±19 min, which
were statistically different (P<0.05, student t-test)
from those of serotonin-mediated depolarization of the nonspiking
interneurones. The peak amplitude of depolarization was 12.8±3.3 mV
(N=6) and the time couse of recovery was 26±11 min. To compare
the effect of serotonin more quantitatively, small quantities of serotonin of
0.1 µmol l-1 in concentration were ejected directly into the
neuropil near the recording site of the nonspiking interneurones
(Fig. 2C,D). Serotonin-mediated
hyperpolarization of the nonspiking interenurones
(Fig. 2C) ranged between 20 and
94 ms (46±29.7 s, mean ± S.E.M., N=5), which was
significantly longer (P<0.05, student t-test) than the
serotonin-mediated depolarization of the nonspiking interenurones
(Fig. 2D) that ranged between 5
and 23 s (13.8±7.0 s, N=5).
|
Five out of six nonspiking interneurones that showed serotonin-mediated depolarization made inverting connections with the reductor motor neurone. Thus, they could decrease tonically occurring spikes of the reductor motor neurone by their depolarization of the membrane potential. For example, depolarizing current (2nA) injected into one of these interneurones reduced the number of spikes of the reductor motor neurone (Fig. 3A). After bath application of 100 µmol l-1 serotonin (for 5 min), the membrane potential of this interneurone was depolarized by approximately 12 mV, staying at that depolarized level for several minutes, then gradually declining to the initial level within 15 min after washing (Fig. 3C, filled circles). When the interneurone was depolarized by serotonin, the spike frequency of the reductor motor neurone decreased simultaneously (Fig. 3C, open circles). The spike activity of the motor neurone decreased during sustained membrane depolarization of the interneurone and gradually increased following the recovery of the membrane potential of the interneurone. Before serotonin perfusion, the passage of a 1 nA hyperpolarizing current into this interneurone had no effect upon the activity of the reductor motor neurone (Fig. 3B). At the peak of serotonin-mediated depolarization (3 min after washing, 8 min total), the same current injected into the interneurone caused an increase in the spike frequency of the motor neurone (from 7.25 impulses s-1 to 10 impulses s-1; Fig. 3Di). An increase in the spike frequency of the motor neurone continued to be observed during the falling phase of depolarization of the interneurone (Fig. 3Dii). After the resting membrane potential recovered to the initial level after 10 min of washing, the same hyperpolarizing current injected into the interneurone had no significant effect upon the motor neurone (Fig. 3Diii). Thus, the membrane depolarization of the nonspiking interneurones mediated by serotonin contributed to reduce the spike discharge of the reductor motor neurone during bath application of serotonin.
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Five out of nine interneurones that showed serotonin-mediated hyperpolarization made noninverting connections with the reductor motor neurone. Their excitatory effect upon the motor neurone was cancelled by the serotonin-mediated hyperpolarization. The remaining four nonspiking interneurones that showed a serotonin-mediated hyperpolarization made inverting connections with the reductor motor neurone. Two of them had bidirectional effects upon the motor neurones, which suggested that they released inhibitory transmitter continuously at resting potential. The serotonin-mediated hyperpolarization of these interneurones thus increased the spike activity of the reductor neurone in part by decreasing the amount of inhibitory transmitter.
Modulation of sensory responses of the nonspiking interneurones
during bath application of serotonin
The interneurone shown in Fig.
2A received depolarizing postsynaptic potentials of approximately
6 mV in amplitude in response to the electrical stimulation of the second
nerve root sensory bundle, which contains mechanosensory afferents that
innervate the exopodite (Fig.
4A). The amplitude of the depolarizing postsynaptic potentials
increased to approximately 10 mV after 8 min of serotonin perfusion (5 min
after washing) superimposed on a membrane hyperpolarization of approximately
30 mV in amplitude (Fig. 4B).
This change in the size of the postsynaptic potentials is characteristic of
typical chemical synaptic transmission. After 20 min of washing, the
serotonin-mediated hyperpolarization of the interneurone began to recover
gradually (Fig. 2A), but the
amplitude of the depolarizing postsynaptic potentials in the interneurone
during sensory stimulation increased further. The amplitude of depolarizing
postsynaptic potentials was approximately 20 mV, with a membrane
hyperpolarization of 15 mV after approximately 45 min of washing
(Fig. 4C). Despite the membrane
potential being restored to its initial level after approximately 60 min of
washing, the depolarizing postsynaptic potentials during sensory stimulation
remained large (Fig. 4D). At
the same time, the spike frequency of the reductor motor neurone also
increased during sensory stimulation in comparison with the response of the
motor neurone before serotonin perfusion (cf. top traces in
Fig. 4A and D). This
enhancement in amplitude of the depolarizing postsynaptic potentials was
observed in all nonspiking interneurones (N=4) that showed
serotonin-mediated hyperpolarization. Only one out of six nonspiking
interneurones that showed serotonin-mediated depolarization received
depolarizing postsynaptic potentials from the sensory afferents
(Fig. 5). Before bath
application of 100 µmol l-1 serotonin (3 min), the depolarizing
postsynaptic potentials were approximately 7 mV in amplitude
(Fig. 5A). After serotonin
perfusion, the postsynaptic potentials firstly slightly decreased in amplitude
superimposed on a serotonin-mediated depolarization
(Fig. 5B). The interneurone was
depolarized by 10 mV in amplitude after 6 min of washing (9 min in total) and
the depolarizing postsynaptic potentials of the interneurone began to increase
in amplitude (Fig. 5C). After
approximately 20 min washing, the interneurone was still depolarized but
sensory stimulation evoked depolarizing postsynaptic potentials of over 10 mV
in amplitude (Fig. 5D).
|
|
The remaining 10 nonspiking interneurones received hyperpolarizing postsynaptic potentials during sensory stimulation (Fig. 6). The amplitude of the hyperpolarizing postsynaptic potentials in the nonspiking interneurones that showed either serotonin-mediated hyperpolarization (N=5) or depolarization (N=5) was enhanced and prolonged after serotonin perfusion. Before serotonin application, sensory stimulation elicited hyperpolarizing postsynaptic potentials of approximately 6 mV in amplitude in one of these interneurones (Fig. 6Ai). After serotonin application (3 min), the membrane potential of the interneurone began to shift negatively (Fig. 6Aii). After 3 min of washing (in total, 6 min after serotonin application), the interneurone was hyperpolarized by 15 mV and the hyperpolarizing postsynaptic potentials of the nonspiking interneurone mediated by sensory stimulation were reduced in size to approximately 50% of their initial amplitude (Fig. 6Aiii). This change in amplitude of the hyperpolarizing postsynaptic potentials is also characteristic of typical chemical synaptic transmission. The hyperpolarizing response of the interneurone during sensory stimulation was, however, gradually enhanced after approximately 10 min of serotonin perfusion. The amplitude of the hyperpolarizing postsynaptic potentials in the interneurone increased to approximately 75% of the initial postsynaptic potentials, although the level of hyperpolarization of the interneurone was similar to that at 6 min (cf. Fig. 6Aiii and iv). The membrane potential of the interneurone was still hyperpolarized after approximately 30 min of serotonin perfusion while the amplitude of the hyperpolarizing postsynaptic potentials of the interneurone during sensory stimulation was considerably larger than that of the initial postsynaptic potentials (Fig. 6Av). The hyperpolarizing postsynaptic potentials of another interneurone that showed serotonin-mediated depolarization were also enhanced by bath application of serotonin. Before serotonin application, hyperpolarizing postsynaptic potentials of approximately 5 mV in amplitude were observed in the interneurone during electrical stimulation of sensory afferents (Fig. 6Bi). Bath application of 100 µmol l-1 serotonin for 3 min caused a membrane depolarization of the interneurone that was restored to the initial level after approximately 20 min of washing. Subsequent sensory stimulation evoked hyperpolarizing postsynaptic potentials of approximately 10 mV in amplitude (Fig. 6Bii).
|
Effect of serotonin on spiking interneurones
The responses of eight ascending interneurones, including three VE-1, two
NE-1, RO-1, RO-4 and RO-5, as well as two spiking local interneurones of a
medial group were examined during bath application of serotonin. Most showed
no significant change in membrane potential after bath application of either
100 µmol l-1 or 1 mmol l-1 serotonin but some
interneurones showed a small membrane hyperpolarization of 2-5 mV in
amplitude. For example, identified ascending interneurone, VE-1
(Nagayama et al., 1993a) was
only slightly hyperpolarized by bath application of 1 mmol l-1
serotonin, although the tonically occurring spikes of the reductor motor
neurone were completely suppressed for more than 10 min
(Fig. 7A). No spiking
interneurones were depolarized or produced spikes following bath application
of serotonin.
|
Electrical stimulation of the second nerve root sensory bundle at 20 Hz elicited excitatory responses in the ascending interneurone VE-1 (Fig. 7B). The stimulus intensity was set so that about half of the electric pulses elicited spikes in the interneurone (Fig. 7Bi). When 1 mmol l-1 serotonin was applied for 3 min, the excitability of VE-1 to sensory stimulation gradually increased (Fig. 7Bii). With the same intensity of stimulation. VE-1 responded with spikes to every electrical pulse with no significant depolarization of the resting potential (Fig. 7Biii). The excitability of the interneurone then gradually decreased and returned to the initial level after approximately 20 min of washing with normal saline (Fig. 7Biv-vi).
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Discussion |
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More than 30 neurones in the crayfish and approximately 100 neurones in the
lobster ventral nerve cord display serotonin-like immunoreactivity
(Beltz and Kravitz, 1983;
Real and Czternasty, 1990
). In
the terminal ganglion of the crayfish, at least one neurone with a cell body
in a central medial region shows serotonin-like immunoreactivity
(Real and Czternasty, 1990
).
Furthermore, several serotonin-like immunoreactive neurones in more anterior
ganglia send descending axons into the terminal ganglion that give rise to
extensive branching. Since nonspiking interneurones have numerous fine
branches extending within both the ventral and dorsal neuropil
(Nagayama et al., 1994
), it is
possible that serotonin-like immunoreactive neurones make synapses directly
with the nonspiking interneurones. The identification of the
serotonin-containing neurones and simultaneous intracellular recordings
between them and the nonspiking interneurones are needed to further clarify
this point.
Modulatory effects of serotonin on the sensory responses of
nonspiking interneurones
The excitability of ascending interneurones during sensory stimulation was
reversibly increased after bath application of serotonin without any
significant change in membrane potential. A similar serotonergic modulation
has been described in both invertebrates and vertebrates (e.g.
Peck et al., 2001). The number
of spikes in afferents of leech mechanoreceptors
(Gascoigne and McVean, 1991
)
and a crayfish leg chordotonal organ (El
Manira et al., 1991
) are increased by serotonin, while the sensory
responses of a lobster oval organ proprioceptor are depressed
(Pasztor and Bush, 1989
). In
Aplysia californica, serotonin facilitates the connection between
siphon sensory neurones and gill and siphon motor neurones by increasing
transmitter released from presynaptic sensory neurones
(Kandel and Schwartz, 1982
;
Glanzman et al., 1989
).
Although the amplitude of depolarizing or hyperpolarizing potentials in
nonspiking interneurones elicited by sensory stimulation was also increased
without any direct correlation with the serotonin-mediated potential change,
the responses in nonspiking interneurones to sensory stimulation were enhanced
and prolonged after washing. A similar post-serotonin enhancement has been
reported in Tritonia swim interneurones
(Katz and Frost, 1995
). The
slow excitatory postsynaptic potentials (EPSPs) of the dorsal flexion neurone
mediated by the dorsal swim interneurone increased in amplitude for more than
10 h. Since spiking interneurones showed no post-serotonin enhancement, and
hyperpolarizing responses of the nonspiking interneurones also continued to
increase despite sensory afferents not making inhibitory synapses directly
with the nonspiking interneurones
(Nagayama and Sato, 1993
;
Nagayama, 1997
;
Ushizawa et al., 1996
), the
post-serotonin enhancement could not be due to the presynaptic effect of the
release of transmitter from the sensory afferents. Certain postsynaptic
mechanisms on the membrane of the nonspiking interneurones, such as an
upregulation of the receptors, could perhaps occur during serotonergic
modulation.
Behavioural significance of serotonergic modulation
The effect of serotonin on the synaptic responses of the lateral giant (LG)
interneurones in the crayfish is known to be dependent on the social status of
the animal (Yeh et al., 1996).
In socially isolated or dominant crayfish, serotonin increases the response of
LG to the sensory stimulation of tailfan afferents. By contrast, in socially
subordinate crayfish, serotonin inhibits the response of LG
(Yeh et al., 1997
).
Furthermore, the behavioural performance of the crayfish to mechanical
stimulation of the abdomen was also different depending on the social status
of the crayfish (Drummond et al.,
2002
). In this study, six nonspiking interneurones showed
depolarization and nine interneurones showed hyperpolarization, although their
sensory responses were commonly enhanced by bath application of serotonin.
There is, however, no close relationship in this study between
serotonin-mediated membrane potential changes and sensory inputs or motor
outputs of the nonspiking interneurones. For example, five out of nine
nonspiking interneurones that made inverting connections with the reductor
motor neurone showed serotonin-mediated membrane depolarization, while the
remaining four interneurones showed hyperpolarization. At the moment, the
relationship between the mode of serotonergic effect on the nonspiking
interneurones and the social status of the crayfish is unclear. Since the
nonspiking interneurones receive both peripheral and central inputs and
continuously control the excitability of the uropod motor neurones
(Nagayama and Hisada, 1987
;
Namba et al., 1994
,
1997
), the post-serotonin
enhancement of the nonspiking interneurones in response to sensory stimulation
and probably inter- and intra-segmental interactions affects the background
excitability of the motor neurones. Thus, the effects of nonspiking
interneurones can be gated or biased depending on the behaviour at a given
state of the crayfish.
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Acknowledgments |
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