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AMER. ZOOL., 41:939–942 (2001)
Swimming in Opisthobranch Mollusks: Contributions to Control of Motor
Behavior: Introduction to the Symposium1
RICHARD A. SATTERLIE2
Department of Biology, Arizona State University, Tempe, Arizona 85287-1502
Beginning with the pioneering work of
Dennis Willows (Willows and Hoyle, 1969;
Willows et al., 1973), studies utilizing opisthobranch mollusks have been particularly
useful in the description of rhythmic motor
behaviors and their mechanisms of central
pattern generation. General mechanisms
that contribute to central pattern generator
function in other animal groups, such as reciprocal inhibition, postinhibitory rebound,
multi-component synaptic potentials, delayed excitation, and extrinsic modulation
(to name a few), have been found to contribute to the generation of rhythmic motor
behavior in opisthobranchs. In addition,
some novel concepts that have since been
substantiated in other animal groups were
developed through work on opisthobranch
locomotory systems: some CPG neurons
are multifunctional and may participate in
different motor behaviors (Getting, 1989);
networks can be intrinsically modulated by
components within the CPG networks (Katz
et al., 1994; Katz and Frost, 1995).
The Opisthobranch Swimming symposium was organized with a primary goal of
providing details of motor control from four
specific Opisthobranch orders that have
swimming members. This comparative approach is particularly interesting since behavioral observations of swimming activity
in the four orders reveal three distinct types
of swimming. In the Anaspids (Aplysia) and
Gymnosomes (Clione), swimming is accomplished by flapping of parapodia. In the
latter group, parapodia are highly modified
into wings. In the Notaspids (Pleurobranchaea) and dorso-ventrally flattened Nudibranchs (Tritonia), swimming consists of
1 From the Symposium on 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]
alternate dorsal and ventral flexions of the
body. Finally, in the laterally flattened Nudibranchs (Melibe), swimming occurs with
alternating lateral flexions of the body. In
all but one case (Clione), the central neural
circuits and effectors for swimming also
participate in other behaviors. For example,
the parapodia of Aplysia undergo local protective contractions in response to directed
stimulation and produce coordinated respiratory pumping contractions in addition to
their role in swimming (Kandel, 1979). In
the Notaspids and Nudibranchs, the effectors and at least some of the central circuitry underlying effector activity are involved in local retraction movements and
local bending responses in addition to
swimming contractions. A comparative
look at the polymorphic nature of the neuromuscular systems of these animals is thus
of interest. Clione is unusual in that the central circuitry and peripheral musculature
used in swimming appears to be dedicated
to that behavior. Despite this, many features
of the Clione swim control system appear
to be similar to that of Aplysia. Using this
as one example, a secondary goal of the
symposium was to allow some speculation
on inter-order relationships based on common and unique properties of the neural
machinery that generates these different
forms of swimming.
An additional objective of the symposium was to honor Dr. A. O. Dennis Willows for his groundbreaking work on the
Tritonia swimming system (Willows and
Hoyle, 1969; Willows et al., 1973). The
symposium participants are either Dennis’s
academic children, grandchildren, or
‘‘adopted brothers/nephews,’’ and all have
benefited from his help and encouragement
through his roles of colleague and collaborator, and as Director of the Friday Harbor
Laboratories of the University of Washington. The following symposium papers bear
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RICHARD A. SATTERLIE
a direct stamp of Dennis’s work on, and interest in, Opisthobranch swimming.
The list of participants of this symposium
is short two important contributors whose
research careers were tragically cut short.
This symposium acknowledges the important contributions of Drs. Peter Getting and
Harold Pinsker, whose seminal investigations have molded our current work, not
only with respect to swimming in Tritonia
(Getting) and Aplysia (Pinsker), but also
well beyond work on swimming Mollusks.
One common theme that emerged from
the symposium that deserves discussion
here is the role of serotonin in modulating
swimming activity in all five opisthobranchs (Aplysia, Clione, Melibe, Pleurobranchaea and Tritonia). Serotonergic
modulation of locomotion is a well-known
feature of a wide variety of animals, including vertebrate spinal locomotory circuits, in which serotonin has been shown
not only to enhance muscle tone to produce
an increase in locomotor activity (e.g., Barbeau and Rossignol, 1991), but also to initiate locomotor activity (Crowley and
Schmidt, 1994; Sillar and Simmers, 1994;
Gerin et al., 1995). In mammals, serotonin
has been shown to initiate locomotion in
decerebrated, curarized rabbits (Viala and
Buser, 1969), and in neonatal rats (Cazalets
et al., 1992; Cazalets, 1995).
In more than one symposium presentation, modulatory cells were considered to
comprise a general serotonergic arousal
system that was capable of up-modulating
swimming, as well as other non-swimming
activities. This highlights a need for a brief
discussion of putative properties of such
general arousal systems. The following is
meant to be a starting point for further
thought and discussion on the concept of
‘‘arousal,’’ particularly when the following
papers from this symposium are read. Many
of the following points were adapted and
modified from Kandel (1979), Teyke et al.
(1990), and Kupfermann et al. (1991).
First, the concept of arousal, as presented
here, is distinct from motivational variables
that produce specific goal-oriented behavior, such as those that serve to correct or
satisfy a well-defined physiological or homeostatic imbalance/need (e.g., feeding,
thirst). The latter would be better termed a
‘‘motivational state’’ (Kandel, 1979). The
distinction between a motivational state and
an arousal may involve different ‘‘levels’’
within a modulatory hierarchy since an
arousal system may be activated as part of
an overall motivational state. This leads to
a second property of arousal systems: they
may be activated, in whole or in part, during more than one type of behavior. Whereas a motivational state is directed towards
one primary goal, an arousal system may
function as a general gain setting system
that is utilized in a variety of different behaviors. As a specific example, swim acceleration in the pteropod mollusk Clione,
which is triggered by activity in a serotonergic ‘‘arousal’’ system, is used during
several different behaviors: avoidance behavior, startle-related escape, acquisition
and comsummatory phases of feeding behavior, and at the conclusion of egg laying
(to break the animal away from the egg
mass). While both motivational and arousal
states would alter activity in lower levels of
the motor system through excitatory, permissive, or inhibitory influences, arousal
systems would be multifunctional, while
motivational states would be dedicated to a
specific goal. In addition, the multifunctional nature of arousal systems should place
them at a lower hierarchical level than motivational states, which may include activation of an arousal system as part of the
overall response.
Motivational and arousal states produce
modulatory effects that typically persist for
some time after cessation of the initiating
stimulus. While motivational states can last
for fairly long periods (minutes/hours), the
arousal responses of opisthobranchs, reported in the following papers, typically are
of much shorter duration. This raises a pair
of interesting questions. Are specific cells
involved in the maintenance of long duration motivational states, and if so, are they
separate from cells involved in the initiation
of motivation? The likelihood of positive
answers to these questions is higher for motivational states than for arousal systems
provided the former are directed to correction/satisfaction of a physiological need.
The modulatory action of at least some of
OPISTHOBRANCH SWIMMING
the serotonergic arousal systems of opisthobranchs appears to operate via second messenger systems, and their time course is
limited by the activation/deactivation parameters of these cellular responses. Furthermore, as an example, the time course of
swim acceleration in Clione is limited by
the duration of activation in two clusters of
cerebral modulatory neurons, plus a 5–10
sec period following cessation of spike activity (Satterlie and Norekian, 1995).
The ability of modulatory states to organize a variety of neuronal circuits presents a potentially interesting difference,
when motivational and arousal states are
compared. The influence of motivational
states should be widespread, involving activity in several independent circuits. While
the suite of circuits can vary with the type
of stimulus, overall, there should be some
consistency imposed on such a system since
the motivational state is designed to address
a specific physiological need. On the other
hand, arousal systems presumably subserve
several different behaviors and should show
significant flexibility to mesh with the specific needs of each behavior. As an example, the serotonergic system of Clione appears to be compartmentally organized. Individual, or small groups, of serotonergic
cells modulate specific effectors, such as
the heart and swimming musculature.
While each ‘‘compartment’’ can operate independently, they are activated together to
produce a full suite of physiological responses during swim acceleration (Satterlie
and Norekian, 1995). Potentially, different
combinations of modulatory cells could
also be simultaneously activated during different behaviors, imposing a polymorphic
nature on the modulatory arousal system.
In this, and several of the following papers, reference is made to ‘‘serotonergic
arousal systems.’’ While the cells/circuits
that modulate swimming in these opisthobranchs utilize serotonin, this does not imply that these and other arousal systems are
transmitter specific. The possibility of release of multiple neuroactive substances
from single neurons presents a potential
source of variability in modulatory systems,
as does the potential participation of neurons with different transmitter phenotypes.
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In the following set of papers, an initial
attempt was made to group papers according to opisthobranch species, so the reader
would be familiar with the peculiarities of
each animal when reading multiple papers
describing work on a single species. This
was abandoned in favor of a more topical
organization, although an attempt was made
to group papers by species when possible.
It is hoped that the symposium papers will
stimulate further interest in the comparative
analysis of motor control, and highlight the
value of invertebrate preparations in this
enterprise.
ACKNOWLEDGMENTS
I would like to thank the symposium participants for their efforts in producing the
oral presentations and written works. The
symposium was generously supported by
the National Science Foundation (IBN
9905990)—special thanks to Dr. Elvira Doman, Program Officer of the Integrative Animal Biology Program. We are also grateful
to the Division of Neurobiology of the Society for Integrative and Comparative Biology for financial support, and Dr. Paul
Katz and Georgia State University for organizing a social gathering during the meeting.
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