© 2001 by The Society for Integrative and Comparative Biology
Mechanisms of Locomotory Speed Change: The Pteropod Solution1
1 Department of Biology, Arizona State University, Tempe, Arizona, 85287-1501
 |
SYNOPSIS |
|---|
TOP
 SYNOPSIS INTRODUCTIONSPEED CHANGES IN THE...IS THERE A GENERAL...References |
|---|
Three primary factors contribute to locomotory speed changes in the pteropod mollusk Clione limacina. (1) An increase in cycle frequency of locomotory appendages is associated with a baseline depolarization and enhancement of postinhibitory rebound in central pattern generator (CPG) interneurons, and a reorganization of the CPG through recruitment of additional interneurons. (2) An increase in the force of appendage movements is generated through enhancement of activity of active motoneurons, recruitment of additional motoneurons and peripheral modulation of swim musculature. (3) Changes in biomechanical aspects of appendage movements are presumably achieved, at least in part, through changes in the activity of motoneurons and swim muscle. All changes associated with non-startle swim acceleration are produced by a serotonergic arousal system that acts at all three levels of the swimming system: CPG interneurons, motoneurons and swim musculature.
|
INTRODUCTION |
|---|
|
TOP
SYNOPSISINTRODUCTIONSPEED CHANGES IN THE...IS THERE A GENERAL...References |
|---|
Three types of variability in locomotor behavioral output have been described neurophysiologically in vertebrate spinal cord preparations (reviewed by Sillar et al., 1997
). These include (1) changes in the frequency of the locomotor pattern, (2) changes in the duration and intensity of motoneuron activity, which translate into changes in the force of muscle contraction, and (3) changes in the phase relationships between motoneuron pools, which result in alterations in muscle coordination and gait (biomechanical changes). To examine the relative contributions of these three speed changing variables in a locomotory system (vertebrate or invertebrate), it is necessary to first construct a theoretical framework identifying likely modulatory targets for each type of change. For example, cycle frequency changes in the locomotory system should be largely limited to alterations within the central pattern generator (CPG), and can include modifications that shorten the cycle period in conjunction with an overall increase in tonic excitation of CPG neurons. Shortening of the cycle period can result from intrinsic changes, such as alteration of endogenous properties of CPG neurons, or from reorganization of the CPG circuitry.
A general increase in CPG excitability can lead directly to an increase in activity of motoneurons, in turn producing an increase in the force of appendage movements. However, large increases in appendage force should involve recruitment of additional or different motoneuron pools. In addition, targets for direct modulation can include motoneurons, in which case increases in the intensity of motoneuron firing can occur over and above excitation increases passed on from the CPG. Furthermore, direct peripheral modulation of muscle cell activity can increase force output independent of CPG and motoneuron activity.
Neuromuscular modifications that result in increased force of locomotory movements can also increase locomotory efficiency by altering biomechanical properties of the movements. In animals with projecting locomotory appendages, and in particular those with wing-like appendages, biomechanical modifications can include a change in the angle of attack, a change in the range of appendage excursion, and a change in appendage stiffness. Finally, in animals with a variety of appendage types, differential activation of muscle groups can produce a dramatic shift in biomechanical output resulting in a gait change.
|
SPEED CHANGES IN THE CLIONE LOCOMOTORY SYSTEM |
|---|
|
TOP
SYNOPSISINTRODUCTIONSPEED CHANGES IN THE...IS THERE A GENERAL...References |
|---|
The locomotory system of the pteropod mollusk Clione limacina exhibits swim accelerations that utilize all three forms of change: increase in CPG cycle frequency, increase in muscle force and change in biomechanical aspects of appendage movements (Satterlie, 1991
; Satterlie and Norekian, 1996). Furthermore, with appropriate forms of mechanical stimulation of the body, swim acceleration can involve a dramatic change in forward propulsion that appears to be equivalent to a gait change in higher animals. Thus, the Clione locomotory system is a useful model for investigation of mechanisms of both subtle and dramatic locomotory speed changes in which analyses can be accomplished at the level of individual neurons and muscle cells. Here, we discuss how the Clione locomotory system produces swim accelerations with specific reference to the three primary mechanisms of speed change listed above.
Three features make the Clione preparation particularly attractive for this type of investigation. First, the pattern generator for normal (slow) swimming is extremely simple (Arshavsky, 1985c; Satterlie, 1985). Two groups of antagonistic interneurons interact via reciprocal inhibitory connections creating a two-phase CPG that is essentially a real-life example of the "Half-Center CPG" originally proposed by Brown (1914; Fig. 1). Second, all aspects of swim acceleration can be induced by bathing the preparation in serotonin-containing saline (Arshavsky et al., 1985a, b, c, d; Satterlie and Spencer, 1985). Two specific groups of cerebral serotonin-immunoreactive neurons (Cr-SA and Cr-SP neurons) have been identified that can produce all aspects of swim acceleration in swimming animals, and can initiate swimming in quiescent animals (Satterlie and Norekian, 1995, 1996). Third, all cell types involved in the locomotory system, including CPG interneurons, motoneurons, muscle cells, sensory neurons and modulatory neurons are accessible for intracellular recording.
|
The following review will "walk through" a description of specific properties of the Clione locomotory system that are involved in speed changes. In most cases, these properties contribute to increases in CPG cycle frequency and/or the force of wing movements, however, at least one permissive change is necessary to explain the observed speed increases. The properties will be sequentially introduced as a series of problems and solutions. While the problems and solutions will be specific to the Clione locomotory system, distinct parallels exist with locomotory systems of higher animals, particularly in relation to speed changes. While Arshavsky et al. (1985b)
report that swim interneurons from the "White Sea" population of Clione have regular, spontaneous spike activity, we have been unable to repeat these observations in intact preparations or with physically isolated interneurons in our work on the "Friday Harbor" Clione population. Problem. The first proposed mechanism for producing swim acceleration is an increase in cycle frequency. How is this achieved in Clione?
Solution. The change from slow to fast swimming in Clione involves a distinct increase in cycle frequency that is associated with a tonic baseline depolarization of CPG interneurons (Satterlie and Norekian, 1995; Satterlie et al., 2000; Fig. 2). The baseline depolarization, which can be produced with application of exogenous serotonin, or with stimulation of Cr-SA or Cr-SP neurons (Satterlie and Norkeian, 1995, 1996), is one of two changes in the activity of individual CPG interneurons that together contribute to the increase in cycle frequency. The second change is a serotonin-induced enhancement of postinhibitory rebound (PIR; Satterlie et al., 2000). Together, the baseline depolarization, which brings the membrane potential of the interneurons closer to threshold, and the increased amplitude of PIR depolarizations, can decrease the time between mid-cycle inhibition and subsequent spike production. Thus, these imposed changes in CPG interneuron activity, by themselves, can produce an increase in cycle frequency.
|
Problem. Cycle frequency increases resulting from the combination of baseline depolarization and PIR enhancement might not be sufficient to explain the full range of frequency changes seen during normal swim accelerations. Wing movements during slow swimming typically range from 1–2 Hz, while fast swimming occurs with cycle frequencies of up to 5 Hz (normally in the 3–4 Hz range). It is questionable that baseline depolarization and PIR enhancement can produce changes of this magnitude. Thus, additional mechanisms of cycle shortening must exist.
Solution. The change from slow to fast swimming in Clione involves reconfiguration of the CPG through recruitment of additional interneurons. The most important newcomer is the Type 12 interneuron (Arshavsky et al., 1985d, 1989). Type 12 interneurons receive inhibitory synaptic inputs during slow swimming, and produce phasic plateau potentials when recruited during fast swimming. Cr-SA or Cr-SP neuron input is capable of inducing plateau activity in Type 12 interneurons (Satterlie and Norekian, 1995), which produces significant shortening of the cycle period by providing "early" excitation to D-phase (dorsal phase) CPG interneurons and "early" inhibition to V-phase (ventral phase) CPG interneurons and motoneurons (Arshavsky et al., 1995d; Fig. 3A). The combination of baseline depolarization, PIR enhancement and CPG reconfiguration appears to be sufficient to produce the range of observed swim frequencies of Clione.
|
Problem. The interneurons that make up the slow swimming CPG of Clione produce a single, broad action potential per appropriate half cycle, and receive an equally broad IPSP (from antagonistic interneurons) in the opposite half cycle. Action potential and IPSP durations each can be over 100 msec (Arshavsky et al., 1985b, c
; Satterlie and Spencer, 1985; Satterlie et al., 2000). The total duration of the action potential plus IPSP thus becomes critical in terms of total cycle period when swimming increases to 4 Hz and above. In particular, the total duration takes up a higher percentage of total cycle period as swim frequency increases (Satterlie et al., 2000). In the absence of any change in spike and IPSP durations, the two would occupy around 50% of the total cycle period at 1 Hz swimming, nearly 80% at 3 Hz, 104% at 4 Hz and 130% at 5 Hz swimming!
Solution. During the change from slow to fast swimming, CPG interneurons (excluding Type 12 cells) show a significant decrease in spike duration, with an average reduction of 20%, and a maximal reduction of 50% (Satterlie et al., 2000). This spike narrowing was reflected in a similar narrowing of incoming IPSPs from antagonistic interneurons. Spike narrowing reduces the impact of cycle frequency increases so that the total duration of the action potential plus IPSP never exceeds 70% of the total cycle period (Satterlie et al., 2000). Spike narrowing could be experimentally induced with exogenous application of serotonin, or with activation of Cr-SA or Cr-SP neurons.
Problem. Synaptic outputs of CPG interneurons are critical to the proper function of the pattern generator. These include not only reciprocal inhibitory connections between the interneuron groups, but also monosynaptic inputs to swim motoneurons (Arshavsky et al., 1985b, c; Satterlie, 1985; Satterlie and Spencer, 1985). Any decrease in interneuron spike duration could negatively influence synaptic efficacy, and thus have deleterious effects on operation of the locomotory system at a time when the activity level in the system is being up-modulated. Spike narrowing, in conjunction with an increase in locomotory speed, is thus counterintuitive. In particular, any decrease in synaptic efficacy in the excitatory connections from swim interneurons to synergistic motoneurons would work against a desired increase in motoneuron activity that would help realize a significant increase in the force of appendage movements during the acceleration. Specifically, the general excitor motoneurons must be recruited into activity during fast swimming (Satterlie, 1993), and this recruitment presumably results from an increase in synaptic and/or modulatory drive to the motoneurons.
Solution. Cr-SA and Cr-SP neurons not only provide modulatory input to CPG interneurons, but also provide direct excitatory input to both types of motoneurons (Satterlie and Norekian, 1995). This includes tonic depolarization, which increases the firing frequency of small motoneurons and contributes to the recruitment of general excitor motoneurons. This excitatory modulation, which is extrinsic to the CPG, reduces the potentially negative influence of interneuron spike duration, and helps produce an excited state in motoneurons. Thus, spike narrowing is strictly permissive, allowing significant increases in cycle frequency during the change from slow to fast swimming, and compensatory modulatory inputs to motoneurons ensure that the overall level of motoneuron activity is increased (Satterlie et al., 2000).
Problem. Any tonic excitatory modulation of motoneurons raises the possibility of inappropriate firing in the wrong half of the swim cycle. This would be particularly critical during fast swimming, when an increase in the force of wing movements is desired, and antiphasic firing activity of antagonistic motoneuron groups is essential.
Solution. CPG interneuron-to-motoneuron outputs not only include excitatory connections with synergistic motoneurons, but also inhibitory connections with antagonistic motoneurons (Arshavsky et al., 1985c; Satterlie and Spencer, 1985). This modification of the half-center model (Fig. 3B) ensures that mid-cycle inhibition occurs in both interneurons and motoneurons. In the latter case, mid-cycle inhibition would decrease the probability of inappropriate firing on the part of motoneurons. This inhibition may also contribute to recruitment of general excitor motoneurons since they exhibit significant PIR activity (unpublished). It is not known if motoneuron PIR is enhanced during fast swimming.
Problem. With the connectivity indicated by Figure 3B, neurotransmitter phenotype of CPG interneurons becomes important. For example, if both groups of cells utilize the same transmitter, postsynaptic motoneurons would have at least two populations of receptors to a single transmitter that would produce opposite electrical effects. Alternately, the two populations of CPG interneurons could have different transmitter phenotypes.
Solution. Evidence for two separate transmitter phenotypes in d-phase and v-phase CPG interneurons has been found, suggesting that the former are glutaminergic and the latter cholinergic. Panchin et al. (1995) and Panchin and Sadreyev (1997) have shown that muscarinic antagonists block synaptic connections from v-phase interneurons to their targets. Furthermore, similar pharmacological evidence implicates glutamate as a d-phase interneuron transmitter (Panchin et al., 1995). Our work supports this latter conclusion as kainic acid is a potent excitor of CPG activity, and d-phase interneuron outputs are blocked by the glutaminergic antagonist CNQX (unpublished).
Thus far, a case can be made for serotonin-induced shortening of cycle period during swim acceleration, and serotonergic excitation of motoneurons, to include recruitment of general excitor motoneurons (Satterlie and Norekian, 1995, 1996). The latter results in recruitment of fast-twitch, fatigable muscle fibers and a significant increase the force of wing contractility (Satterlie, 1993). Presumably, biomechanical changes also result from fast-twitch fiber recruitment. This raises the question, "Does serotonin also have a direct modulatory effect on the swim musculature?" If so, it is highly unlikely that such modulation would directly involve Cr-SA or Cr-SP neurons since their processes are restricted to the central ganglia (Satterlie et al., 1995; Satterlie and Norekian, 1995).
A cluster of large serotonin-immunoreactive neurons has been identified in each pedal ganglion (Pd-SW neurons; Satterlie et al., 1995). Of the five to seven cells in each cluster at least three send processes to the ipsilateral wing through the wing nerve, and have wide innervation fields that cover the entire wing (either dorsal or ventral musculature). Physiologically, Pd-SW neurons do not produce a motor effect in quiescent preparations, but with ongoing swimming, Pd-SW neuron activity results in enhancement of the force of wing contractions that outlasts the period of spike activity by up to 10 sec (Satterlie, 1995). These cells have no effect on CPG or swim motoneuron activities—their effects appear to be strictly peripheral.
Problem. Examination of the peripheral targets of Pd-SW neurons using serotonin-immunohistochemistry and Neurobiotin fills, produced a somewhat surprising result. Pd-SW cells selectively innervate the slow-twitch, fatigue resistant muscle fibers (Satterlie, 1995). If the goal is to produce a peripheral enhancement of muscle contractility, why not modulate fast-twitch fibers, or both slow and fast-twitch fibers?
Solution. One answer would suggest that selective recruitment of fast-twitch musculature would produce a significant increase in force in the initial stages of wing movements (muscle force rise time is around 15 msec), while slow twitch activity would occur later in the wing movement (muscle force rise time is around 80 msec; Satterlie et al., 1990). Enhancement of slow-twitch activity would better match up the overall force output of the two fiber types. Furthermore, the fast-twitch fibers show significant fatigability (Satterlie et al., 1990). It might not be that useful to enhance contractility in muscle fibers which show such rapid fatigue.
A much more speculative answer to this question requires a look at speed changes other than the slow-to-fast "gait" change. Clione is able to produce subtle swim accelerations during slow swimming that do not involve an increase in CPG cycle frequency or recruitment of general excitor motoneurons (Satterlie and Norekian, 1996). One way to accomplish such acceleration is through purely peripheral modulation of muscle contractility. Since this occurs in the slow swimming mode, the logical target for modulation is the slow-twitch musculature. Thus, selective serotonergic innervation of the slow-twitch fibers may be a compromise between the need for enhanced contractility during slow-to-fast swim accelerations, and the need to produce purely peripheral contractility increases, and thus speed changes within the slow swimming mode.
|
IS THERE A GENERAL AROUSAL SYSTEM THAT UNDERLIES SWIM ACCELERATION IN CLIONE? |
|---|
|
TOP
SYNOPSISINTRODUCTIONSPEED CHANGES IN THE...IS THERE A GENERAL...References |
|---|
All of the major features of swim acceleration in Clione can be achieved by bath application of physiologically reasonable concentrations of serotonin (Arshavsky et al., 1985a, b, c, d
; Satterlie, 1991; Satterlie and Norekian, 1996). Furthermore, identical changes follow stimulation of single cells from the anterior (Cr-SA) or posterior (Cr-SP) clusters of cerebral serotonergic neurons (Satterlie and Norekian, 1995, 1996). Modulatory targets of these neurons include CPG interneurons, Type-12 interneurons, both types of motoneurons, Pd-SW neurons that modulate muscle contractility, and a serotonergic heart excitor neuron, which increases heart rate. Furthermore, an additional pair of cerebral serotonin-immunoreactive neurons provide weak excitation to the swim system but also inhibit the whole-body withdrawal system, whose activity is incompatible with swimming (Norekian and Satterlie, 1996; Satterlie et al., 2000). Pd-SW neurons and the heart excitor can function independently, in the absence of the slow-to-fast swim acceleration, but are recruited into activity by Cr-SA and Cr-SP neurons when the slow-to-fast swim change is induced. The combined activity of all of these serotonergic neurons may represent a general arousal system (see Satterlie, 2001) since it displays the following features. (1) Activity in more than one behavioral module is altered, and includes excitatory, permissive and inhibitory influences on the modules to favor a specific behavioral output. Effects on the swim system are both excitatory and permissive, the effect on the heart is purely excitatory, and the effect on whole-body withdrawal is inhibitory. (2) The behavioral state persists for a brief time following cessation of the initiating stimuli. Both the period of elevation of spike activity in the serotonergic cells and the modulatory influences on the target cells last for many seconds after the delivery of the initiating stimulus (Satterlie, 1995; Satterlie and Norekian, 1995, 1996). (3) The modulatory influence of the system is widespread, and can be produced as part of more than one behavioral act. For example, in Clione, fast swimming is used as an aversive (escape) mechanism, during food acquisition behavior, and during egg-laying behavior.
A common feature of swimming opisthobranchs appears to be involvement of a group of serotonergic neurons that produce an arousal state related to the initiation and maintenance of swimming activity. This view is particularly well documented by Katz et al. (2001) in this volume. The role of the serotonergic system in the Clione locomotory system deserves additional discussion, however, considering the increased role of swimming in the overall behavioral repertoire of Clione. While Cr-SA and Cr-SP neuron activity initiates locomotion in quiescent preparations, the primary role of these cerebral neurons, which are extrinsic to the swim CPG, is to accelerate ongoing swimming activity. Their activity ensures an increase in swim cycle frequency through inputs to the swim CPG, through increased firing activity and recruitment in motoneurons, and activation of additional serotonergic neurons that enhance contractility of swim musculature and increase heart activity. An additional pair of cerebral serotonergic neurons strongly inhibits whole-body withdrawal (Cr-SV neurons; Norekian and Satterlie, 1996). This slightly different role of the serotonergic arousal system in Clione allows interesting speculation concerning the species-specific uses of this general locomotory arousal system. In Clione, swimming is a nearly continuous background activity, at least during major parts of the diurnal cycle. Swimming thus occupies a different hierarchical position in the Clione behavioral repertoire, in comparison to that of some of the other swimming opisthobranchs, in which swimming primarily represents an escape response. In Clione, the serotonergic arousal system still functions in elevating the swimming behavioral response, but this appears as an acceleration system, rather than an initiation/maintenance system. Also, since slow swimming occupies such a low position in the overall behavioral hierarchy of Clione, swim acceleration is used for several behaviors in addition to escape. In particular, fast swimming is an important part of prey capture and consumption (Conover and Lalli, 1972; Litvinova and Orlovsky, 1985; Hermans and Satterlie, 1992), and it is used to break away from the egg mass during egg-laying behavior (unpublished). Since it is apparent that serotonergic arousal of locomotion occurs in a wide range of animals, both invertebrate and vertebrate, comparative investigation of species-specific uses of such arousal systems is providing useful information for the elucidation of mechanisms of locomotory plasticity, as well as for rational speculation concerning the evolution of general locomotory and arousal systems within and between animal groups. For this, swimming opisthobranchs provide an excellent example.
|
ACKNOWLEDGMENTS |
|---|
We thank Dr. A. O. Dennis Willows and the staff of Friday Harbor Laboratories for their assistance and support during our studies. The work was supported by NSF grants IBN-9319927 and IBN-9904424 to R.A.S., and NSF grant IBN-960805 and NINDS grant NS-34662 to T.P.N. We also thank NSF for support of the symposium through grant IBN-9905990.
|
FOOTNOTES |
|---|
1 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: rsatterlie{at}asu.edu
|
References |
|---|
|
TOP
SYNOPSISINTRODUCTIONSPEED CHANGES IN THE...IS THERE A GENERAL...References |
|---|
Arshavsky, Y. I., I. N. Beloozerova, G. N. Orlovsky, Y. V. Panchin, and G. A. Pavlova. 1985a. Control of locomotion in marine mollusc Clione limacina. I. Efferent activity during actual and fictitious swimming. Exp. Brain Res, 58:255-262.[ISI][Medline]
Arshavsky, Y. I., I. N. Beloozerova, G. N. Orlovsky, Y. V. Panchin, and G. A. Pavlova. 1985b. Control of locomotion in marine mollusc Clione limacina. II. Rhythmic neurons of pedal ganglia. Exp. Brain Res, 58:263-272.[ISI][Medline]
Arshavsky, Y. I., I. N. Beloozerova, G. N. Orlovsky, Y. V. Panchin, and G. A. Pavlova. 1985c. Control of locomotion in marine mollusc Clione limacina. III. On the origin of locomotory rhythm. Exp. Brain Res, 58:273-284.[ISI][Medline]
Arshavsky, Y. I., I. N. Beloozerova, G. N. Orlovsky, Y. V. Panchin, and G. A. Pavlova. 1985d. Control of locomotion in marine mollusc Clione limacina. IV. Role of type 12 interneurons. Exp. Brain Res, 58:285-293.[ISI][Medline]
Arshavsky, Y. I., T. G. Deliagina, G. N. Orlovsky, Y. V. Panchin, G. A. Pavlova, and L. B. Popova. 1986. Control of locomotion in marine mollusc Clione limacina. VI. Activity of isolated neurons of pedal ganglia. Exp. Brain Res, 63:106-112.[ISI][Medline]
Arshavsky, Y. I., G. N. Orlovsky, Y. V. Panchin, and G. A. Pavlova. 1989. Control of locomotion in marine mollusc Clione limacina. VII. Reexamination of type 12 interneurons. Exp. Brain Res, 78:398-406.[CrossRef][ISI][Medline]
Brown, T. G. 1914. On the nature of the fundamental activity of the nervous centers; together with an analysis of the conditioning of rhythmic activity in progression, and a theory of the evolution of function in the nervous system. J. Physiol. (London), 48:18-46.
Conover, R. J., and C. M. Lalli. 1972. Feeding and growth in Clione limacina (Phipps), a pteropod mollusc. J. Mar. Biol. Ecol, 9:279-302.[CrossRef]
Hermans, C. O., and R. A. Satterlie. 1992. Fast-strike feeding behavior in a pteropod mollusc, Clione limacina Phipps. Biol. Bull, 182:1-7.[Abstract]
Katz, P., D. J. Fickbohm, and C. P. Lynn-Bullock. 2001. Evidence that the central pattern generator for swimming in Tritonia arose from a non-rhythmic neuromodulatory arousal system: Implications for the evolution of specialized behavior. Amer. Zool, 41:962-975.[CrossRef]
Litvinova, N. M., and G. N. Orlovsky. 1985. Feeding behaviour of pteropod mollusc Clione limacina. Bull. Soc. Natur. Moscow, Sect. Biol, 90:73-77.
Panchin, Y. V., and R. I. Sadreyev. 1997. Effects of acetylcholine and glutamate on isolated neurons of locomotory network of Clione. NeuroReport, 8:2897-2901.[ISI][Medline]
Panchin, Y. V., R. I. Sadreyev, and Y. I. Arshavsky. 1995. Control of locomotion in marine mollusk Clione limacina. X. Effects of acetylcholine antagonists. Exp. Brain Res, 106:135-144.[ISI][Medline]
Norekian, T. P., and R. A. Satterlie. 1996. Cerebral serotonergic neurons reciprocally modulate swim and withdrawal neural networks in the mollusc, Clione limacina. J. Neurophysiol, 75:538-546.
Satterlie, R. A. 1985. Reciprocal inhibition and postinhibitory rebound produce reverberation in a locomotor pattern generator. Science, 229:402-404.
Satterlie, R. A. 1991. Electrophysiology of swim musculature in the pteropod mollusc Clione limacina. J. Exp. Biol, 159:285-301.
Satterlie, R. A. 1993. Neuromuscular organization in the swimming system of the pteropod mollusc Clione limacina. J. Exp. Biol, 181:119-140.[Abstract]
Satterlie, R. A. 1995. Serotonin modulation of swimming speed in the pteropod mollusc Clione limacina. II. Peripheral modulation. J. Exp. Biol, 198:905-916.
Satterlie, R. A. 2001. Swimming in Opisthobranch mollusks: Introduction to the symposium. Amer. Zool, 41:939-942.[CrossRef]
Satterlie, R. A., G. E. Goslow, and A. Reyes. 1990. Two types of striated muscle suggest two-geared swimming in the pteropod mollusc Clione limacina. J. Exp. Zool, 255:131-140.[CrossRef][ISI]
Satterlie, R. A., and T. P. Norekian. 1995. Serotonin modulation of swimming speed in the pteropod mollusc Clione limacina. III. Cerebral neurons. J. Exp. Biol, 198:917-930.
Satterlie, R. A., and T. P. Norekian. 1996. Modulation of swimming speed in the pteropod mollusc, Clione limacina: Role of a compartmental serotonergic system. Invert. Neurosci, 2:157-165.[CrossRef][ISI][Medline]
Satterlie, R. A., T. P. Norekian, S. Jordan, and C. J. Kazilek. 1995. Serotonin modulation of swimming speed in the pteropod mollusc Clione limacina. I. Serotonin immunoreactivity in the central nervous system and wings. J. Exp. Biol, 198:895-904.
Satterlie, R. A., T. P. Norekian, and T. J. Pirtle. 2000. Serotonin-induced spike narrowing in a locomotor pattern generator permits increases in cycle frequency during accelerations. J. Neurophysiol, 83:2163-2170.
Satterlie, R. A., and A. N. Spencer. 1985. Swimming in the pteropod mollusc, Clione limacina. J. Exp. Biol, 116:205-222.
Sillar, K. T., O. Kiehn, and N. Kudo. 1997. Chemical modulation of vertebrate motor circuits. In P. S. G. Stein, S. Grillner, A. I. Selverston, and D. G. Stuart, (eds.), Neurons, networks and motor behavior, pp. 183–193. MIT Press, Cambridge.
CiteULike 
Connotea 
Del.icio.us What's this?
| ||||||||||||||||||||||||||||||||||||||||||||||||||