Download Swim Initiation Neurons in Tritonia diomedea1

AMER. ZOOL., 41:952–961 (2001)
Swim Initiation Neurons in Tritonia diomedea1
W. N. FROST,2,* T. A. HOPPE,† J. WANG,*
AND
L.-M. TIAN†
*Department of Cell Biology and Anatomy, Finch University of Health Sciences/
The Chicago Medical School, 3333 Green Bay Road, North Chicago, Illinois 60064
†Department of Neurobiology and Anatomy, The University of Texas Medical School at Houston,
P.O. Box 20708 Houston, Texas 77225
INTRODUCTION
The marine mollusc Tritonia diomedea
initiates a rhythmic escape swim upon contact with a sufficiently aversive stimulus,
such as the seastar Pycnopodia helianthoides (Fig. 1a). The neural program underlying this behavior can be elicited by briefly
stimulating any one of a number of peripheral nerves in the isolated brain preparation,
indicating that the motor program is centrally generated, with little involvement of
sensory feedback ((Dorsett et al., 1969;
Frost, 1999) and Fig. 5).
Previous work has described much of the
circuitry mediating the Tritonia escape
swim response, including the afferent neurons (S-cells) (Getting, 1976; Slawsky,
1979), the central pattern generator (CPG)
neurons (Getting, 1983), and the swim flexion neurons (Willows et al., 1973; Hume et
al., 1982) (Fig. 1b). While these findings
made it possible to study pattern generation,
From the Symposium Swimming in Opisthobranch
Mollusks: Contributions to Control of Motor Behavior
presented at the Annual Meeting of the Society for
Integrative and Comparative Biology, 4–8 January
2000, at Atlanta, Georgia.
2 E-mail: [email protected]
1
motor program initiation could not readily
be addressed due to a gap in our knowledge
of the circuit elements between the afferent
neurons and the swim CPG. Here we fill-in
this gap, by describing two recently discovered pre-CPG interneurons, Tr1 (Triggertype 1) and DRI (Dorsal Ramp Interneuron), that convey the output of the afferent
neurons to the CPG. An initial description
of DRI has been published previously
(Frost and Katz, 1996); Tr1 is described
here for the first time.
METHODS
Animals
Tritonia diomedea were collected from
the waters of Puget Sound, Washington,
and were maintained in natural running seawater (10–128C) at the University of Washington’s Friday Harbor Laboratories and in
artificial seawater aquaria (Instant Ocean,
10–128C) in Houston and Chicago.
Recording preparations
For experiments where skin stimulation
was used to elicit the swim motor program,
animals were first anesthetized by injecting
60 ml of a solution composed of half 350
mM MgCl2 and half artificial seawater (In-
952
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SYNOPSIS. Two groups of interneurons, Tr1 and DRI, have been identified in the
escape swim circuit of the marine mollusc Tritonia diomedea that have important
roles in behavioral initiation. DRI functions as a command neuron, receiving direct
excitatory input from the afferent neurons, and in turn directly exciting the DSI
neurons of the central pattern generator. DRI fires throughout the swim motor
program, and activity in DRI is both necessary and sufficient for sensory input to
elicit the swim motor program. Tr1 is an excitatory interneuron that fires briefly
in response to sensory input and then remains silent during the motor program.
Tr1 excites DRI with an excitatory connection that has fast and slow components
and thus appears to have a role in converting brief afferent neuron activity to
long-lasting firing in downstream circuit elements. These neurons complete the
description of a continuous synaptic pathway from afferent to flexion neurons in
the Tritonia swim circuit. Their identification should facilitate studies of motor
program initiation, as well as of how various forms of experience, including simple
forms of learning, act to influence neuronal decision-making processes.
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stant Ocean, Aquarium Systems). The ventral foot was then cut along the midline
from the tail to the buccal mass. After removing the internal organs, an opening was
cut in the dorsal skin, above the brain. The
animal was then positioned dorsal side up
in the recording chamber, with the brain
(cerebral, pleural and pedal ganglia) pinned
out on the Sylgard surface of a 1-cm-diameter post rising from the chamber floor.
A thin cylindrical sleeve, containing slits to
allow the nerves passage, was raised around
the brain, the slits were closed with Vaseline, and the brain and body chambers were
perfused separately with normal saline. All
other experiments utilized an isolated brain
preparation. For both preparations, the brain
was perfused at 28C while pinning the brain
out and dissecting away the thin sheath enclosing the dorsal, cerebral and pleural ganglia. Suction electrodes were then placed on
left and right pedal nerve 3, and the preparation was warmed to 10–118C for the duration of the experiment.
Electrophysiology
Neurons were impaled with glass microelectrodes (20–40 MV) filled with 3 M Kacetate and inserted into chucks containing
3 M KCl. Swim neurons were identified
based on their location, size, color, synaptic
connections with other identified neurons,
and their activity during the swim motor
program (Getting, 1976; Getting et al.,
1980; Frost and Katz, 1996). Normal saline
composition for both preparations was (in
mM): 420 NaCl, 10 KCl, 10 CaCl2, 50
MgCl2, 11 D-glucose and 10 HEPES, pH
7.6. High divalent cation saline composition
was (in mM): 285 NaCl, 10 KCl, 25 CaCl2,
125 MgCl2, 11 D-glucose, and 10 HEPES,
pH 7.6. Data were initially stored on videotape using a Vetter 3000A PCM recording adapter, and were then digitized and analyzed offline using a Biopac MP100 data
acquisition system. Tr1 was iontophoretically injected with 5, 6-carboxyfluorescein
and photographed in the live preparation
using an Optronics DEI-750D CCD camera
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FIG. 1. The Tritonia escape swim and its underlying circuit. A. Upon contact with a suitably aversive stimulus,
such as the tube feet of the seastar Pycnopodia helianthoides, Tritonia respond with an escape swim consisting
of a series of alternating ventral and dorsal whole-body flexions. The photograph shows an animal at a moment
of maximum dorsal flexion. B. The known swim circuit. Solid lines represent direct, monosynaptic connections,
broken lines represent indirect connections, or connections not yet confirmed to be monosynaptic. Synaptic
symbols: lines 5 excitatory, black circles 5 inhibitory, lines and circles 5 multiple component monosynaptic
connections. ‘‘VSI’’ represents both VSI-A and VSI-B; the exact connectivity shown is for VSI-B only. The
known number of neurons of each type on each side of the brain are: S-cells, ;80; Tr1, 1; DRI, 1; DSI, 3; C2,
1; VSI, 2; FNs, ;55 (Getting, 1983; Frost and Katz, 1996).
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ET AL.
and a Kramer Scientific fluorescence illumination module attached to a Zeiss SV6
stereomicroscope.
RESULTS
DRI
FIG. 2. The swim motor program elicited via DRI
stimulation. DRI and three CPG interneurons (C2 and
two DSIs) were impaled with intracellular electrodes.
DRI was stimulated to fire at 10 Hz for 50 sec, resulting in a 6 cycle swim motor program. Calibration
bars: All 20 mV, 8 sec.
S-cells produced EPSPs onto DRI in high
divalent cation saline.
As reported previously (Frost and Katz,
1996), directly activating DRI using intracellular stimulation elicits the swim motor
program (Fig. 2), while hyperpolarizing a
single DRI prevents the nerve shock-elicited motor program. These findings satisfy
the most stringent criteria for inclusion of
DRI as a command neuron (see Discussion). In our prior work we only tested the
ability of DRI hyperpolarization to block
motor programs elicited by stimulation of
Pedal Nerve 3. Here we report that hyperpolarizing DRI also blocks the initiation of
motor programs elicited by salt stimuli applied to the skin (Fig. 3, n 5 3 preparations)—the stimulus used in many of our
behavioral studies (Frost et al., 1996; Mongeluzi and Frost, 2000).
Although DRI satisfies the formal criteria
for assignment as a command neuron, the
fact that it receives feedback from the CPG
and its firing oscillates with the motor program raised the issue of whether it might
actually function as a CPG member. Previous work had shown that injecting sufficient hyperpolarizing current to suppress
firing in one of the two DRIs completely
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For many years, a key missing element
in the Tritonia swim network was the interneuronal population responsible for producing the long-lasting, declining ‘‘ramp’’
of depolarization in the dorsal swim interneurons (DSIs) of the CPG in response to
a swim-eliciting stimulus (Lennard et al.,
1980). Prior work (Getting and Dekin,
1985) concluded that this depolarization has
an important role in initiating the swim motor program. Using a dye filled electrode,
we searched for the missing ramp interneurons among the axons in the central commissure. This procedure led to the discovery of DRI, an interneuron that receives direct excitatory synaptic input from the afferent neurons (see below), and in turn
makes strong, direct excitatory connections
onto the DSIs of the CPG (Frost and Katz,
1996). The available data are consistent
with there being just one DRI on each side
of the brain (Frost and Katz, 1996). The
discovery of DRI completed the description
of a continuous synaptic pathway from the
afferent to the efferent neurons of the swim
circuit (Fig. 1b).
An early report (Getting, 1977) suggested that the S-cells made a monosynaptic
connection to CPG neuron Cerebral Cell 2
(C2). (3 of 8 cells were reported to do so.)
In the present experiments we observed
several indirect, but no direct connections
between 58 S-cell–C2 pairs tested in 11
preparations using either saline or a high
divalent cation saline solution effective at
blocking polysynaptic pathways in Tritonia; (Katz and Frost, 1995b). We therefore
suggest that the connections between the Scells and C2 are indirect.
In contrast to their connections to C2, we
found that the majority of S-cells made direct excitatory connections to DRI (Hoppe,
1998). In 10 preparations, 44 of 62 S-cells
made 1-for-1, constant latency EPSPs onto
DRI. In one of these preparations, 9 of 11
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blocks the ability of a nerve stimulus to
elicit the motor program (Frost and Katz,
1996). We reasoned that if DRI functions
as a CPG member, suppressing its firing via
hyperpolarization should also block oscillation initiated from within the CPG, such
as can be elicited via intracellular stimulation of one or more DSI neurons (Fickbohm
and Katz, 2000). On the other hand, if DRI
functions more as a gating-command neuron that drives the CPG and also receives
feedback from it, then suppressing DRI firing should not prevent DSI-driven CPG activity. We found that hyperpolarizing DRI
failed to prevent the DSI-driven motor program (Fig. 4, n 5 5 preparations). This result supports our categorization of DRI as
a pre-CPG command neuron that functions
more to initiate and sustain the motor program than as part of the mechanism generating the cycle-by-cycle mechanics of the
oscillation itself.
Tr1
Although the discovery of DRI established a continuous afferent-to-flexion neuron synaptic pathway, the firing patterns of
the cells suggested the existence of an asyet unidentified circuit element. Brief sen-
sory stimulation elicits a correspondingly
brief S-cell firing response, yet all previously identified downstream neurons in the
swim circuit typically fire for tens of seconds (Figs. 3, 5). Since the S-cells excite
DRI with fast EPSPs, something else
seemed needed to mediate this brief-to-long
firing transformation.
We describe here a new neuron that appears to contribute to this process. The Tr1
neuron (n 5 20 preparations, Figs. 1B, 5)
is located below the surface in the dorsal
pleural ganglion, near DRI and the statocyst
(Fig. 6A). Its defining features are: 1) the
location of its cell body and its characteristic axonal morphology (Fig. 6A), 2) it receives direct EPSPs from the S-cells (28 of
28 cells tested in 10 preparations, Fig. 6B),
3) it fires briefly, like the S-cells, at the onset of the swim motor program (Fig. 5), 4)
it makes an indirect excitatory connection
to DSI (Fig. 6C), and 5) direct intracellular
stimulation of a single Tr1 neuron is often
sufficient to activate the motor program
(Fig. 6D). Such Tr1-elicted motor programs
typically continue 1 to 3 cycles beyond the
end of intracellular stimulation (Avg. 1.5 6
0.3 extra cycles, n 5 8 preparations). This
latter property suggests that Tr1 may con-
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FIG. 3. DRI firing is necessary for the salt-elicited swim motor program. DSI and DRI were impaled with
intracellular electrodes in the semi-intact preparation. Three consecutive salt stimuli (0.1 ml, 4 M NaCl) were
applied to the tail 3–5 min apart (arrows). The first (left) and third (right) trials elicited swim motor programs.
On the second (middle) trial, DRI was hyperpolarized to block its firing response to the salt. This prevented the
swim motor program. The dotted line indicates the DRI resting potential before the hyperpolarization. Calibration
bars: All 20 mV, 10 sec.
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W. N. FROST
tribute to the mechanism by which brief Scell discharges trigger long-lasting circuit
excitation.
To date, only one Tr1 neuron has been
encountered on each side of the brain.
However, hyperpolarizing Tr1 does not
block the ability of nerve stimulation to
elicit the swim motor program (n 5 2 preparations), nor does Tr1 stimulation elicit
motor program activity as long lasting as
that elicited by nerve stimulation, suggesting that there may be additional Tr1 neurons, or an additional class of Tr-like neurons on each side of the brain.
We next tested whether Tr1’s indirect excitation of DSI (Fig. 6C) occurred via recruitment of DRI, the only known excitatory input to DSI originating from outside the
CPG. This was a difficult experiment because Tr1 and DRI are both located out of
FIG. 5. The S-cells and Tr1 fire briefly at the onset
of the swim motor program. A brief stimulus (10 Hz,
1 sec) applied via suction electrode to Pedal Nerve 3
(arrow) elicited a brief firing train in the S-cell and
Tr1 cell, followed by a three cycle swim motor program in CPG neurons DSI and C2. Calibration bars:
All 20 mV, 10 sec.
sight, below the surface of the pleural ganglion. We were successful in penetrating
both DRI and Tr1 in two preparations, and
found that Tr1 produced 1-for-1, constant
latency EPSPs onto DRI (Fig. 7A). Significantly, brief Tr1 trains produced long-lasting firing in DRI (Fig. 7B). Hyperpolarizing
DRI in normal saline revealed that the connection had both fast and slow components
(Fig. 7A, C). These preliminary observations suggest that a key location for the
brief-to-long firing transformation in the
swim circuit may be a dual component fast/
slow excitatory synaptic connection between Tr1 and DRI. However further work
is needed to test this hypothesis. Such dual
component fast/slow synaptic connections
mediate brief-to-long lasting firing transitions in other circuits as well (Brodfuehrer
and Friesen, 1986b; Cleary and Byrne,
1993; Lieb and Frost, 1997).
DISCUSSION
While significant progress has been made
in elucidating the neural basis of rhythmic
pattern generation (Marder and Calabrese,
1996), less is known about the mechanisms
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FIG. 4. DRI does not appear to function as a CPG
element. DRI, C2 and 2 DSIs were impaled with intracellular electrodes. The two DSIs were stimulated
to fire at 20 Hz for 20 sec (hatched bar) while DRI
was hyperpolarized to prevent its spiking. This procedure failed to prevent the swim motor program, consistent with the view that DRI is not part of the cycle
generating mechanism, but instead functions as a preCPG command neuron. During the swim motor program, C2, DSI and DRI received inhibition during the
ventral phase, which was sufficient to phasically block
firing in one of the two DSIs (DSI-1), leaving just the
stimulus artifacts between the bursts. Calibration bars:
All 20 mV, 10 sec.
ET AL.
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of motor program initiation—the decisionmaking process that determines whether or
not a particular behavioral act will occur.
The Tritonia escape swim response is an
attractive model system for investigating
the neural mechanisms of behavioral initiation. The swim is an all-or-none response—the animal either swims or it
doesn’t in response to an appropriate stimulus—so the nature of its decision is unambiguous. Also, the animal takes a variable amount of time (up to 20 sec) when
deciding whether or not to swim, consistent
with decision-making processes in higher
animals.
Progress toward understanding the swiminitiation process in Tritonia has come with
the identification of the circuitry conveying
sensory input to the swim CPG. A key
question concerns how brief S-cell firing
brings about a sustained activation of the
CPG. Before the pre-CPG interneurons
were identified, this was addressed by comparing the duration of depolarization in the
DSI neurons when the nerve-elicited CPG
oscillation was either allowed or prevented
by hyperpolarizing C2 (Getting and Dekin,
1985). It was concluded that sensory input
initiates a slowly declining ramp of depolarization in the DSIs that sustains the ini-
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FIG. 6. Identifying characteristics of Tr1. A. Tr1 neuron injected with Carboxyfluorescein in the live preparation.
The cell body is below the surface, and the axon can be seen travelling beneath the surface, out of focus,
crossing the central commissure and entering the right side of the brain. S: statocyst; Pd: pedal ganglion; Ce:
cerebral ganglion; Pl: pleural ganglion. B. S-cell excitatory synaptic connection to Tr1 in normal saline. C. Tr1
makes an indirect excitatory connection to DSI. A Tr1 train caused the tonically active DSI (DSI-1) to increase
its firing rate. Holding a second DSI (DSI-2) hyperpolarized during the train revealed that the DSI excitation
resulted from a flurry of EPSPs that did not follow the Tr1 action potentials one-for-one. D. A Tr1 train elicited
by intracellular current injection (10 sec, mean 5 15.2 Hz) elicited a swim motor program that outlasted the
train by 2 full cycles. Calibration bars: B. Tr1, 1 mV; S-cell, 20 mV; 500 msec. C. All 20 mV, 2 sec. D. All 20
mV, 10 sec.
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tial 10–15 sec of oscillation. After that, excitatory interactions among the CPG neurons were suggested to sustain the remaining duration of the motor program.
DRI was recently identified as the major
source of the excitatory synaptic input to
the DSIs (Frost and Katz, 1996). When
CPG oscillation is suppressed by hyperpolarizing both C2 neurons, a brief nerve
stimulus elicits a gradually slowing train of
action potentials in DRI, and a corresponding declining ramp of depolarization in the
DSIs (Frost and Katz, 1996). The excitatory
ramp in the DSIs was found to be reduced
or eliminated when DRI was hyperpolarized to prevent its firing. DRI was furthermore found to be individually necessary
and sufficient for afferent input to activate
the swim motor program (Figs. 3, 4 and
(Frost and Katz, 1996)).
These features satisfy the most stringent
criteria for command neuron status—a cell
that fires in response to sensory input and
whose activity is both necessary and sufficient for the activation of a motor program
by that input (Kupfermann and Weiss,
1978). A number of individual neurons
have now been identified that satisfy these
criteria (Rock et al., 1981; Fredman and Jahan-Parwar, 1983; Nolen and Hoy, 1984;
Frost and Katz, 1996; Xin et al., 1996; Edwards et al., 1999; Jing and Gillette, 1999;
Hedwig, 2000). In practice, however, the
term ‘‘command neuron’’ has frequently
been applied to neurons whose activity is
simply sufficient to elicit a motor program,
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FIG. 7. Tr1 to DRI connection. A. Tr1 connects to DRI with 1-for-1 constant latency EPSPs. B. A Tr1 train
(2.5 sec, mean 5 22.6 Hz) produced several seconds of firing in DRI. C. Hyperpolarizing DRI during a Tr1
train revealed a dual component fast/slow EPSP in DRI. Calibration bars: A. DRI, 5 mV; Tr1, 20 mV; 1 sec.
B. DRI, 10 mV; Tr1, 20 mV; 10 sec. C. DRI, 4 mV; Tr1, 20 mV; 1 sec. All records in normal saline.
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feedback connection from the CPG to its
own command neuron may have an important role in initiating and sustaining the
swim rhythm (Katz et al., 1994; Katz and
Frost, 1997).
The overall organization of the swim initiation circuitry in Tritonia appears to be
similar to that described for swimming in
the leech (Brodfuehrer et al., 1995). Both
species direct sensory input to trigger-type
neurons that in turn excite gating command
neurons that activate and sustain CPG activity. In both cases, as in others (Gillette
et al., 1978; Fredman and Jahan-Parwar,
1983; McCrohan, 1984; Nolen and Hoy,
1984; Delaney and Gelperin, 1990; Jing
and Gillette, 1999) the gating neurons also
receive synaptic feedback from the pattern
generator during the rhythm. These similarities across species reinforce the idea that
this circuit structure for the control of motor
program initiation may be commonly employed for the control of many stimuluselicited, rhythmic motor programs, such as
those mediating escape responses.
ACKNOWLEDGMENTS
We wish to thank Richard Satterlie for
organizing the symposium, and Lise Eliot
and Ion Popescu for comments on the manuscript. This work was supported by
NS36500. The symposium was supported
by National Science Foundation grant BN
9905990.
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