Identification of magnetically responsive neurons in the marine mollusc Tritonia diomedea
Department of Biology, University of North Carolina, Chapel Hill, NC, 27599-3280, USA
* Author for correspondence (e-mail: johnwang{at}email.unc.edu)
Accepted 14 October 2002
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Summary |
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Anatomical analyses revealed that prominent neurites from the Pd6 cells are located within two ipsilateral nerves, pedal nerves 1 and 2. These nerves extend to the periphery of the animal and innervate tissues of the anterior ipsilateral foot and body wall. Electrophysiological recordings demonstrated that action potentials generated by the Pd6 cells propagate from the central ganglia toward the periphery. These results imply that the Pd6 cells play an efferent role in the magnetic orientation circuitry. Given that these cells contain cilio-excitatory peptides and that Tritonia crawls using ciliary locomotion, the Pd6 neurons may control or modulate cilia used in crawling, turning, or both.
Key words: orientation, navigation, magnetoreception, magnetic, neuroethology, mollusc, Tritonia diomedea, TPep, neuropeptide, cilia
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Introduction |
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A promising model system that can be used to investigate the neural
circuitry underlying magnetic orientation is the marine mollusc Tritonia
diomedea. This species has been used extensively in neuroethological
studies because it possesses individually identifiable neurons that are easily
accessible while the animal performs a wide repertoire of behaviors
(Willows, 1967;
Willows et al., 1973
).
Laboratory experiments have demonstrated that Tritonia can use the
Earth's magnetic field as an orientation cue
(Lohmann and Willows, 1987
)
while field studies have suggested that this sensory ability may help guide
the animal between offshore and inshore areas
(Willows, 1999
). In addition,
electrophysiological experiments have demonstrated that a pair of neurons,
left pedal 5 (LPd5) and right pedal 5 (RPd5)
(Fig. 1), respond to changes in
earth-strength magnetic fields with increased spiking
(Lohmann et al., 1991
;
Popescu and Willows, 1999
;
Cain, 2001
). Studies have also
indicated that the Pd5 neurons influence ciliary locomotion by modulating the
beating rates of cilia on the foot of the animal
(Popescu and Willows, 1999
;
Cain, 2001
).
|
While the Pd5 cells are some of the most thoroughly characterized
magnetically sensitive neurons, other cells involved in the neural circuitry
underlying magnetic orientation behavior in Tritonia have yet to be
identified. One pair of bilaterally symmetrical neurons, the pedal 6 (Pd6)
neurons, shares many characteristics with Pd5. Among these are similarities in
coloration and location, the production of neuropeptides known as TPeps
(Lloyd et al., 1996;
Willows et al., 1997
), and
common synaptic inputs (Snow,
1982
). In this study, we present evidence that the Pd6 neurons
also respond to magnetic field changes with increased electrical activity and,
like the Pd5 neurons, play efferent roles in the neural circuitry underlying
magnetic orientation.
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Materials and methods |
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Semi-intact animal preparations
Intracellular recordings from neurons were carried out in semi-intact
preparations (Willows et al.,
1973). A small incision was made directly above the brain on the
animal's dorsal surface. Non-magnetic tungsten hooks were used to retract the
body wall, support the animal in the seawater bath, and expose the central
nervous system (CNS). A wax-covered platform was placed beneath the brain and
tungsten pins were used to immobilize the central ganglia. This preparation
allowed access to specific individual neurons while giving the animal freedom
to perform many of its behaviors (e.g. escape swimming). Animals were allowed
to recover for at least 1 h after the brain had been immobilized. Neurons were
then identified by their size, coloration and location within the CNS.
Targeted cells were impaled with glass microelectrodes filled with 3 mol
l-1 KCl (15-30 M
). Electrical signals were amplified,
monitored on an oscilloscope, digitized using a CED 1401 A-D board, and
analyzed using CED Spike 2 software (Cambridge Electronics Design, Cambridge,
UK).
Magnetic field measurements and magnetic field manipulations
The dissection chamber was located in the center of a computer-controlled
magnetic coil system consisting of three orthogonally arranged
AlldredScollar coils (Alldred and
Scollar, 1967). The two outer wraps of each AlldredScollar
coil measured 2.1 m on a side and the two inner wraps measured 2.2 m on a
side. The coil system was used to replicate the magnetic field in which the
animals were kept and to rotate the magnetic field 60° clockwise during
experiments. This field rotation occurred in one step and took less than 1 s.
During the rotated field condition, alterations to the total magnetic
intensity and inclination angles were minimal (the total intensity of the
magnetic field was only altered by +0.6% and the inclination angle was altered
by +0.8°).
Magnetic experiments with left pedal 6
Because the Pd6 neurons share many characteristics with the magnetically
sensitive Pd5 neurons, we investigated whether the Pd6 neurons also respond to
rotations of the magnetic field. We focused our experiments on left pedal 6
(LPd6). LPd6 could be easily distinguished from other large neighboring cells
based on location and size (Willows et
al., 1973; Murray et al.,
1992
).
Animals were placed in the magnetic coil system so that they initially
faced magnetic 240°. We used a magnetic test protocol similar to that of
Lohmann et al. (1991). This
test protocol consisted of a 20 min baseline followed by a 26 min magnetic
stimulus period. At the beginning of each baseline period, hyperpolarizing or
depolarizing current was injected into LPd6 to ensure that the cell produced
at least one action potential and no more than ten action potentials during
the ensuing 20 min period. If the activity of the cell was not in this range,
the current injected into the cell was adjusted and a completely new 20 min
baseline period was recorded.
Once the baseline was obtained, the computerized coil system produced a 26
min magnetic stimulus period in which the magnetic field was rotated 60°
every minute. The magnetic field was first rotated 60° clockwise. After 1
min, the magnetic field was rotated 60° counterclockwise back to its
original position. This alternating exposure of a clockwise 60° and
counterclockwise 60° magnetic field rotation was repeated for the 26 min
magnetic stimulus period (Lohmann et al.,
1991).
After each trial, the animal was allowed to recover for 1 h before another was conducted. Trials were continued as long as stable recordings of LPd6 could be maintained. For each trial, the number of spikes occurring during the 20 min baseline period and the final 20 min of the magnetic stimulus were counted. The LPd6 neurons of 11 different animals were tested using these procedures. When possible, recordings from RPd6 and other neurons were made simultaneously with those of LPd6.
To confirm that the increased spiking observed in LPd6 (see Results) was
due to the magnetic stimulus, we performed a second series of trials that
controlled for potential spontaneous increases. In these experiments, each
trial began with a 20 min baseline period. Once the baseline was recorded, the
animal was exposed to either the 26 min magnetic stimulus period or to a 26
min control period in which the magnetic field remained unaltered
(Lohmann et al., 1991). After
a 1 h recovery period, another 20 min baseline was recorded and the
alternative treatment was applied. The animal was exposed to these alternating
magnetic and control treatments as long as electrophysiological recordings
remained stable. The LPd6 of 10 animals were tested using this procedure.
Single rotation experiments
We also tested the response of LPd6 to single rotations of the magnetic
field. Such rotations may simulate approximately what the animal experiences
as it turns. These experiments were performed at Friday Harbor, Washington,
USA. Animals were trawled at Bellingham Bay from depths of 20-30 m and were
maintained in flow-through seawater tanks at the University of Washington
Friday Harbor Laboratories for 1-3 weeks before use.
During experiments, a semi-intact preparation was placed into a dissection
chamber with the anterior end directed toward a magnetic heading of 300°.
The dissection chamber was placed in the center of a 1 m x 1 m
single-axis Merritt 4-coil system (Merritt
et al., 1983) and attached to a flow-through water system. At this
location, the magnetic field had an inclination angle of 76.9° and an
intensity of 53.0 µT. A BK Precision 1760 Triple output d.c. power supply
was used to power the Merritt 4-coil system causing the magnetic field to
rotate 60° clockwise from the Earth's field. The intensity and inclination
of the field remained nearly constant (intensity changed by +0.2% and
inclination by +0.4°).
An initial 15 min baseline was recorded from LPd6 and other pedal neurons
without adjusting their resting potentials, using a procedure adapted from
Popescu and Willows (1999) and
Cain (2001
). The magnetic field
was then rotated 60° clockwise once. After a 6 min adjustment period, the
number of spikes was counted for 15 min and compared to the number of spikes
during the baseline period.
Neuroanatomy of the Pd6 neurons
To visualize the morphology of the Pd6 neurons, 500 mmoll-1
CoCl2 was pressure-injected into their somata (for LPd6,
N=5; for RPd6, N=4) using a PV820 Picopump (World Precision
Instruments). After the CoCl2 was allowed to diffuse throughout the
neuron for 12-24 h the CNS was removed from the animal. The brain was
incubated in 11°C ASW with several drops of concentrated ammonium sulfide
(Croll, 1986). After 15 min,
the CNS was washed with fresh ASW, fixed with 10% formalin in ASW for 24 h,
dehydrated with an ascending ethanol series, cleared with methyl salicylate,
and mounted onto a glass slide. The Pd6 somata and neurites were visualized
using light microscopy.
The CoCl2 fills indicated that Pd6 neurons had neurites located in two ipsilateral pedal nerves, pedal nerves 1 and 2 (see Results), which innervated the foot. These two nerves were dissected to determine their gross areas of innervation. Semi-intact preparations (N=5) were incubated in 1% Methylene Blue for 1 h at 4°C. Each preparation was washed with ASW and the pedal nerves were carefully followed from the CNS. At the point where the nerves entered the foot and body wall, they were dissected from the musculature. To facilitate dissecting the pedal nerves from the foot musculature, the buccal mass and viscera were removed and additional 1% Methylene Blue incubations were used as needed. Pedal nerve 1 (PdN1) and pedal nerve 2 (PdN2) were traced to determine branching patterns and innervation areas. This procedure continued until the nerves and subsequent branching neurites became too small to visualize.
Determining the direction of LPd6 action potentials
The direction of action potential propagation in LPd6 was determined by
recording intracellularly from this cell while simultaneously recording
extracellularly from the pedal nerves, LPdN1 and LPdN2. Extracellular signals
were recorded using en passant suction electrodes in differential
recording mode and amplified with an A-M Systems Differential AC Amplifier
(Carlsborg, Washington, USA). Single units corresponding to LPd6 were
identified in LPdN1 and LPdN2 by evoking action potentials in the soma of LPd6
(with current injection through the intracellular electrode). LPd6 units in
the nerves were located during stimulation of LPd6 by determining which spikes
corresponded one-to-one with the evoked potentials in the soma. Spontaneous
LPd6 spikes were then used to determine the direction of action potential
propagation within LPdN1 and LPdN2.
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Results |
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Although the statistical analysis demonstrated that increased spiking occurred during the imposed field periods, responses in individual trials were variable. Increases in spike frequency occurred in 10 of the 16 individual trials (62.5%). When increases occurred, they ranged in magnitude from 1 to 44 spikes. Responses of the LPd6 were characterized by a gradual increase in spike frequency occurring with a latency of approximately 4-12 min after the first field change (Fig. 2A).
Experiments with constant-field controls
A second experiment was conducted to confirm that the increased spiking
observed in LPd6 during magnetic stimuli was attributable to the change in
magnetic field and not to spontaneous changes in electrical activity. For each
LPd6 tested, we compared its electrical activity during magnetic stimuli
periods with control periods of equal length (N=10,
Fig. 3).
|
For each animal, the mean change in action potentials between the imposed magnetic field period and preceding baseline period was compared to the mean change between the control period and preceding baseline period (Fig. 4). As a group, significantly more action potentials were produced in the imposed magnetic field periods than in the control periods (Wilcoxon ranked-signs test, P<0.01, N=10).
|
Magnetic experiments with other neurons
The electrical activity of RPd6 (the bilateral mate of LPd6) was monitored
in six animals while the magnetic field around the animal was changed
(Fig. 5). The mean change in
number of spikes during the baseline period from the magnetic stimulus period
was 16.3±7.8 action potentials (N=6, mean ± S.E.M.). In
4 of the 6 trials, RPd6 increased spiking during the magnetic stimulus period,
with increases ranging from 9 to 46 spikes.
|
During the course of our experiments, intracellular recordings were also
made from 13 other cells during rotations of the magnetic field. With the
exception of the Pd5 neurons, which have previously been shown to respond to
magnetic stimuli (Lohmann et al.,
1991; Popescu and Willows,
1999
; Cain, 2001
),
no other cells showed evidence of magnetic sensitivity
(Fig. 6).
|
Electrophysiological responses to single field rotations
Although the majority of our tests relied on a magnetic stimulus involving
multiple field rotations (Lohmann et al.,
1991; Popescu and Willows,
1999
; Cain, 2001
),
the response of the LPd6 cell to a single 60° clockwise rotation of the
field was also monitored in four animals. In 3 of 4 trials, spiking in the
LPd6 increased after the field had been rotated, with increases ranging from 4
to 76 action potentials. Simultaneous recordings of LPd6, LPd5, RPd6 and RPd5
indicated that all four cells responded to a single rotation of the magnetic
field (Fig. 7). In addition,
the postsynaptic potentials of all four of these neurons were often
synchronous (Fig. 8), implying
that they have one or more presynaptic cells in common.
|
|
Neuroanatomy of LPd6
The somata of the Pd6 neurons are located in the dorsal, posterior region
of the pedal ganglia and often measure approximately 350 µm in diameter
(Fig. 9A,B). Cobalt fills
revealed that each Pd6 cell possesses a large, primary neurite, which emerges
from the soma and bifurcates within the pedal ganglion
(Fig. 9A,B). One process enters
ipsilateral pedal nerve 1 and the other enters ipsilateral pedal nerve 2.
|
Gross dissection and Methylene Blue staining (N=5) indicated that LPdN1 and LPdN2 project to distinct, non-overlapping regions of the anterior ipsilateral foot and body wall (Fig. 9C). These nerves emerge from the ganglion laterally, pass around the buccal mass (which lies just ventral to the fused CNS) and then extend toward the ipsilateral body wall before innervating the foot. PdN1 innervates the anterior portion of the foot, while PdN2 innervates a region of the foot immediately posterior to that of PdN1. The innervation areas of these two nerves did not appear to overlap. Innervation patterns of the bilaterally symmetric RPdN1 and 2 appeared to be similar (data not shown).
Direction of LPd6 action potential propagation
Simultaneous extracellular and intracellular recordings of LPd6 were
performed to determine the direction of action potential propagation. In all
preparations (N=5), spontaneous action potentials were observed in
the LPd6 soma before the corresponding extracellular units were recorded in
LPdN1 or LPdN2 (Fig. 10A,B).
This demonstrated that action potentials in LPd6 neurons propagate from the
central ganglia to the periphery.
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Discussion |
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Behavioral experiments demonstrated that Tritonia can orient using
the Earth's magnetic field and that rotating, reversing or eliminating the
horizontal component of the ambient field alters the orientation and turning
responses of these animals (Lohmann and
Willows, 1987). We therefore hypothesize that the Pd6 and Pd5
neurons are components of the neural circuitry that underlies magnetic
orientation behavior. This circuitry presumably enables the animal to detect
the Earth's magnetic field, orient its body relative to this cue, and locomote
along a specific magnetic heading.
Anatomical and electrophysiological characterization of the Pd6
neurons
In principle, the Pd6 neurons might function in any part of the magnetic
orientation circuitry, including: (i) a sensory role; (ii) an integrative or
processing role; (iii) a motor role in controlling or modulating effector
cells such as muscles or cilia. However, the anatomical and
electrophysiological evidence strongly suggest a motor role for the Pd6
neurons. First, these neurons appear to innervate the foot. Each Pd6 neuron
possesses one neurite, which then divides and enters each of the ipsilateral
Pd nerves 1 and 2 (Fig. 9A,B).
These pedal nerves in turn project to non-overlapping regions of the foot.
Second, action potentials in the LPd6 propagate from the central ganglia
through LPdN1 and LPdN2 to the anterior foot
(Fig. 10A,B). Such a pattern,
from CNS to periphery, is typical of motor neurons
(Bullock and Horridge, 1965).
We conclude, therefore, that LPd6 has the anatomical features, projection
patterns and pattern of action potential propagation that are characteristic
of many molluscan motor neurons (Willows
et al., 1973
; Dorsett,
1986
). Thus, the results suggest that the Pd6 neurons play an
efferent role in magnetic orientation by regulating the activity of unknown
effector cells in the anterior part of the foot.
An enigmatic yet consistent feature of the Pd6 neurons' response to
magnetic stimuli was a long latency (approximately 1-15 min) between the onset
of the stimulus and the onset of the response (Figs
2,
3,
5,
7). Similar latencies were also
observed in the responses of the Pd5 neurons
(Fig. 7) and have been reported
in all previous studies involving magnetic responses of the Pd5 neurons
(Lohmann et al., 1991;
Popescu, 1999
;
Cain, 2001
). In other animals,
reported latencies of physiological responses to magnetic stimuli range from
20 to 40 min in honeybee bristle cell sensilla
(Korall and Martin, 1987
) to
approximately 2 min in guinea pig pineal cells
(Semm et al., 1980
;
Semm, 1983
) to milliseconds in
birds and fish (Semm, 1983
;
Beason and Semm, 1987
;
Walker et al., 1997
). In
addition, behavioral responses to magnetic field changes can have lengthy
latencies: from 3 min in spiny lobsters during reversals of the horizontal
magnetic field (Lohmann et al.,
1995
) to latencies of up to 5 days in bobolinks after reversals of
the vertical magnetic field (Beason,
1989
). The reasons for the variability in latency between species,
and the cause of the unusually long delays observed in Tritonia and
in some other animals, remain to be determined. Among several interesting
possibilities are that the receptor mechanism or neural processing of the
magnetic information may require a significant period of averaging in some
animals, or that the nervous system may update magnetic field information only
periodically (Beason, 1989
;
Walcott, 1996
;
Wiltschko et al., 1998
).
Possible function of the Pd5 and Pd6 neurons in magnetic orientation
behavior
With the finding that the Pd6 neurons respond to changes in earth-strength
magnetic fields, four magnetically sensitive neurons in Tritonia have
now been identified (LPd6, RPd6, LPd5, RPd5). The Pd6 and Pd5 neurons share
several characteristics that suggest that these cells may have a similar
function. First, simultaneous recordings from these four neurons during the
presentation of magnetic field stimuli indicate that the responses in each are
qualitatively similar (Fig. 7).
Second, these neurons often have synchronous postsynaptic potentials
(Fig. 8), implying that they
receive common synaptic input from presynaptic cells; both also receive common
sensory input (Murray et al.,
1992). Third, both bilaterally symmetric pairs of neurons have
action potentials propagating to the periphery through nerves that appear to
innervate the foot (Fig. 9;
Cain, 2001
).
An additional similarity is that the Pd6 and Pd5 neurons both synthesize a
trio of 15-amino-acid neuropeptides known collectively as TPeps
(Lloyd et al., 1996).
Immunohistological studies localized TPep in ciliated structures such as the
foot epithelium and oviduct (Willows et
al., 1997
). Ultrastructural studies further localized TPep to
dense-cored vesicles within the cell bodies of the Pd6 and Pd5 neurons and to
neurites adjacent to the ciliated cells of the foot epithelium
(Cain, 2001
). TPeps have been
shown to increase the ciliary beating frequency of isolated foot epithelial
cells as well as the ciliary transport rates of foot patches
(Willows et al., 1997
). Given
that Tritonia locomotes using cilia on the ventral surface of its
foot, the Pd5 cells have been hypothesized to control or modulate cilia
involved in locomotion, turning, or both
(Willows et al., 1997
;
Popescu and Willows, 1999
).
Our results suggest that a similar function is possible for the Pd6 neurons,
although alternative functions (e.g. the control of muscles or the release of
mucus for facilitating ciliary locomotion) cannot be ruled out at present.
In summary, our results demonstrate for the first time that the Pd6 neurons respond with enhanced electrical activity when earth-strength magnetic fields around the animal are changed. They also suggest that these neurons play efferent (motor) roles in the magnetic orientation circuitry. Thus, these advances represent another step in the difficult task of identifying and unraveling the sensory, processing and motor elements that enable Tritonia and other animals to orient to the Earth's magnetic field.
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Acknowledgments |
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