© 2001 by The Society for Integrative and Comparative Biology
The Role of the Escape Swim Motor Network in the Organization of Behavioral Hierarchy and Arousal in Pleurobranchaea1
1 Department of Molecular and Integrative Physiology, 524 Burrill Hall, 407 S. Goodwin Ave., University of Illinois, Urbana, Illinois 61801
 |
SYNOPSIS |
|---|
TOP
 SYNOPSIS INTRODUCTIONTHE ESCAPE SWIM CPG...MECHANISMS OF PATTERN GENERATION...SINGLENESS OF ACTION DURING...ROLES IN BEHAVIORAL AROUSALBEHAVIORAL ROLES OUTSIDE OF...References |
|---|
The escape swimming pattern generator of the notaspid opisthobranch Pleurobranchaea drives a high threshold, override behavior. The pattern generator is integrated with neural networks of other behaviors so as to coordinate unitary behavioral expression and to promote general behavioral arousal. These functions are separately produced by different swim network elements. One set of swim premotor neurons, the A1/A10 ensemble, A3 and IVS, generate the swim pattern and, through corollary activity, suppress potentially conflicting feeding behavior by exerting broad inhibition at major feeding network interneurons. A second set of swim neurons, the serotonergic As1–4 neurons, provides intrinsic neuromodulatory excitation to the swim pattern generator that sustains the escape swim episode through multiple cycles. The As1–4 also provide neuromodulatory excitation to important modulatory, serotonergic cells in the feeding motor network and locomotor network, and may have a general regulatory role in the distributed serotonergic arousal network of the mollusk. The As1–4 appear to be also necessary to both avoidance and orienting turning, and are therefore likely to be critical, multi-functional components upon which much of the organization of the animal's behavior rests.
|
INTRODUCTION |
|---|
|
TOP
SYNOPSISINTRODUCTIONTHE ESCAPE SWIM CPG...MECHANISMS OF PATTERN GENERATION...SINGLENESS OF ACTION DURING...ROLES IN BEHAVIORAL AROUSALBEHAVIORAL ROLES OUTSIDE OF...References |
|---|
What general relevance to the study of behavior has the study of escape swimming in a mollusk? Indeed, one whose major attributes are marked simplicity of form and brain? It is that even with its limited equipment, the predatory sea-slug Pleurobranchaea californica manages to solve the complex problems of foraging and reproduction that challenge much more brainy creatures, and the lessons emerging from study of this and other simple experimental systems are changing our understanding of how behavior is organized in the nervous system. Comparative studies tell us that our complexities of body form and of brain and behavior simply serve a larger repertory of sub-routines aimed at solving the same general problems of survival and genetic continuity; thus the mollusk is a useful model for understanding more complex opportunistic foragers like ourselves.
Examination shows that Pleurobranchaea makes clear and adaptive decisions about when and where to forage, what to eat and when to stop eating. Defensive and avoidance behaviors emerge in appropriate contexts, and can replace appetitive behaviors (Gillette et al., 2000
). Indeed, Pleurobranchaea uses its limited intellect to perform very effective calculations of cost-benefit. It does so by deciding the alternative expressions of appetitive and avoidance behaviors on the basis of motivational state (Davis et al., 1974) and associative learning (Mpitsos and Collins, 1978). And it does so even though the apparent numbers of cells composing the neural networks for the various behaviors range from less than a score to barely a few hundred. Among them, the neurons that constitute the motor network for escape swimming are multi-functional elements with prominent roles in determining the structural organization of the animal's behavior.
While simple, Pleurobranchaea organizes its behavior hedonically, along an axis of pleasure and pain, much like higher vertebrates (Gillette et al., 2000). When quite hungry, the animal attacks vigorously in response to very low concentrations of food stimuli. Indeed, the hungrier animals even attack mildly painful stimuli, such as acidic solutions that are aversive to most invertebrate sea-life. Such behavior in a generalist predator suggests that starving animals might thereby exert more effort to subdue prey unwilling to be eaten. On the other side of the coin is the satiated animal, which not just ignores food stimuli, but tends to actively avoid it, responding to food with avoidance turns. We surmise that this behavior serves in part to protect it from other predators that might be drawn to the same food stimulus, most notably other cannibal Pleurobranchaea. The costs and benefits of foraging decisions are thereby made by integrating hunger, taste and pain, and adding in the useful lessons of experience. The general nature of the neural network interactions that we postulate provides the basis for cost-benefit calculations is shown in the diagram of Figure 1.
|
What is the role of the swim pattern generator in these computations? Our present evidence suggests that its constituent neurons play important roles in four ways: 1) they generate the escape swim, a very expensive avoidance behavior; 2) they ensure singleness of action during the swim, through corollary inhibition of other motor networks that would express conflicting behaviors; 3) they may have central roles in coordinating the arousal state of the animal; and 4) they act outside of swim behavior to coordinate the expression of other behaviors. Below, we will briefly discuss these four functions, and indicate how they are parts of the moment-to-moment solution of the cost-benefit algorithm on which the organism bases its behavioral decisions.
|
THE ESCAPE SWIM CPG OF PLEUROBRANCHAEA |
|---|
|
TOP
SYNOPSISINTRODUCTIONTHE ESCAPE SWIM CPG...MECHANISMS OF PATTERN GENERATION...SINGLENESS OF ACTION DURING...ROLES IN BEHAVIORAL AROUSALBEHAVIORAL ROLES OUTSIDE OF...References |
|---|
Escape swimming in the notaspid opisthobranch Pleurobranchaea is an override behavior in the animal's repertory. It is driven by a central pattern generator (CPG) in the cerebropleural ganglion, and consists of a series of alternating dorsal and ventral body flexions (Davis and Mpitsos, 1971
). Both the escape swim and its underlying CPG closely resemble those of the nudibranch Tritonia (Getting, 1989; Jing and Gillette, 1995, 1999). The close similarities in behavior and neural network support previous inference from anatomy that the nudibranchs evolved from the side-gilled slugs (Schmekel, 1985), and more specifically argue that the common ancestor was probably more like Pleurobranchaea than other extant genera (Jing and Gillette, 1999). We have pointed out that the similarities can be construed to suggest that the swimming tritoniids conserve the escape swim and its CPG as primitive characteristics (Jing and Gillette, 1999). The alternative hypothesis is also reasonable: the animals might have evolved similar CPGs from pre-existing, homologous neurons. That is, perhaps selective pressure favored parallel inventions of a similar escape behavior using homologous neurons most conveniently adaptable. The resolution of this slow-burning question may depend on future comparative analyses. |
MECHANISMS OF PATTERN GENERATION OF ESCAPE SWIMMING |
|---|
|
TOP
SYNOPSISINTRODUCTIONTHE ESCAPE SWIM CPG...MECHANISMS OF PATTERN GENERATION...SINGLENESS OF ACTION DURING...ROLES IN BEHAVIORAL AROUSALBEHAVIORAL ROLES OUTSIDE OF...References |
|---|
The structure of the swim CPG, as we presently understand it (Jing and Gillette, 1999
), is shown in Figure 2. Seven neurons, about a third of the A cluster of the cerebropleural ganglion, take part in escape swimming pattern generation. At least one other element, IVS, remains to be located. The CPG interneurons mediate either the dorsal flexion phase of the swim (A1/A10, and As1–4), or ventral flexion (A3 and IVS). Each fires cyclically in phase with the swim rhythm. The synaptic mechanisms that support patterned oscillation in the CPG, reciprocal inhibition, recurrent excitation, and recurrent inhibition, are common to most other characterized CPGs (Getting, 1988; Friesen, 1994).
|
Figure 3 shows CPG neuron activity during the swim. The network mechanisms have been discussed in greater detail (Jing and Gillette, 1999
). Briefly, initiation and maintenance of the swim is dependent on activity in the A10 neuron, whose tonic activity begins with the triggering stimulus. Subsequently, the As1–4 ensemble is recruited into the first burst of dorsal flexion, succeeded by A1. The activation of the As1–4 group brings recurrent excitation in slow compound EPSPs within the group, which reinforces their own activity and contributes to the prolonged depolarization of A1/A10 enduring throughout and following the swim episode. Recurrent excitation within the As1–4 ensemble, and between it and the A1/A10 ensemble, sustains multiple cycles of the swim episode. The maintained activity of A10 evokes the swim pattern as an emergent property of the CPG connectivity.
|
The ventral flexion phase of the swim is initiated by the biphasic excitatory/inhibitory connection from A1 to As1–4, and by recurrent inhibition in negative feedback to A1/A10 from the A3/IVS cells. A3 inhibitory effects on A1/A10 mark the transition between dorsal and ventral flexion. IVS, which mediates the ventral flexion phase, is potently excited by A1 and disinhibited by cessation of As1–4 activity. The re-onset of As1–4 activity, riding on their own slow EPSPs, and decline of activity of IVS because of waning excitatory input from A1 and inhibition from As1–4, then marks the beginning of the next cycle. The bilateral CPG halves are coordinated during the swim by electrical connections between the contralateral pairs of A1 and A10, As4, and As1–3, and the premotor activity descends to drive motorneurons of the pedal ganglia.
Once triggered, the swim episode may be maintained in part by 5-HT released from the As1–4 ensemble that may underlie the slow EPSP among As1–4. These neurons do not have a critical role in pattern generation, as the coordinated CPG output can be driven by A10 activity without their significant spike activity; however, they appear to have a significant modulatory role, similar to the action of the homologous DSI neurons in the swim CPG of Tritonia (Lennard et al., 1980). 5-HT depolarizes and activates bursting mechanisms in a variety of molluskan cells. In other serotonergic neurons of Pleurobranchaea 5-HT activates (Sudlow and Gillette, 1995) or variously potentiates (Huang et al., 1998) a cAMP-gated Na+ current, also present in the As1–4 neurons (Jing et al., 1997) that could underlie their prolonged recurrent excitation and bursting.
The clear homologies between the CPG elements of Pleurobranchaea and Tritonia are between the cells A1 and C2, and for the serotonergic As1–3 cells and the three DSIs of the respective motor networks (Jing and Gillette, 1995, 1999). The neuron A3 may also be a homolog of the Tritonia VSI-A. The differences between the species' swim CPGs, such as an A10 analog and a fourth serotonergic DSI unreported from Tritonia, and a Dorsal Ramp Interneuron not found in Pleurobranchaea, may represent incomplete description of both species' CPGs.
|
SINGLENESS OF ACTION DURING THE ESCAPE SWIM |
|---|
|
TOP
SYNOPSISINTRODUCTIONTHE ESCAPE SWIM CPG...MECHANISMS OF PATTERN GENERATION...SINGLENESS OF ACTION DURING...ROLES IN BEHAVIORAL AROUSALBEHAVIORAL ROLES OUTSIDE OF...References |
|---|
Escape swimming is the dominant behavior in the animal's behavioral hierarchy, suppressing every other when stimulated (Davis and Mpitsos, 1971
). The dominance of escape swimming in the animal's behavioral repertory arises in part from inhibition of the feeding motor network by corollary outputs of the swim CPG (Jing and Gillette, 1995, 2000). Inhibition of feeding is specifically exerted by the pattern-generating subset of swim interneurons, A1, A10, and A3, acting polysynaptically through the output neuron A-ci1 and other unidentified cells, to inhibit feeding command neurons. The fuller picture of the degree and scope of suppression of feeding by the swim is summarized in Figure 4. Our observations add further confirmation to earlier speculation that in many instances behavioral choice is mediated by inhibitory interactions between competing motor systems, at the level of higher order interneurons (Kovac and Davis, 1977, 1980).
|
Suppression of feeding by the swim resembles in part learned and satiation-induced suppression of feeding behavior in being also based on synaptic inhibition of the feeding command neurons, the paracerebral neurons (PCNs) by the I1 population (cf. Davis and Gillette, 1978
; London and Gillette, 1984, 1986). However, feeding inhibition by the swim differs significantly from that caused by food-avoidance training and satiation. In learned and satiation-induced suppression of feeding the I1s are monosynaptically driven by tonic activity in the I2 population, themselves hyper-excited by food stimuli. In contrast, during the swim the I2s are inhibited and the I1s must receive their excitation from a different source, apparently A-ci1 (Jing and Gillette, 2000).
The differences in neural mechanisms of feeding inhibition between swimming and learning/satiation are reflected in behavioral function: in escape swimming a broader suppression of feeding is appropriate to the context. The I2s are major interneurons that during feeding fire cyclically in the radular retraction phase of the protraction/retraction cycle and drive many other retraction neurons (London and Gillette, 1984). In learning- or satiation-induced inhibition of feeding, the I2s fire tonically to virtually lock feeding network activity in the retraction phase of the feeding cycle (London and Gillette, 1986). It is notable that in this mechanism for feeding suppression a great deal of excitation is still present in the oscillator, and patterned feeding activity can still be released suddenly if feeding stimuli are increased to high levels (Davis and Gillette, 1978). In contrast, during swimming inhibition of the elements of the feeding oscillator appears to be much broader than that occurring due to learning or satiation, since during the swim both major retraction I2 interneurons and the major protraction paracerebral interneurons are effectively removed in a broad shutdown of the feeding motor network (Jing and Gillette, 2000). The inhibition of the I2 neurons during the swim must arise partly from monosynaptic inhibitory inputs from the I1s (London and Gillette, 1984), whose significance is only now appreciated.
The adaptive significance of the two mechanisms of feeding suppression may be that more complete inhibition of feeding should be desirable during the escape swim, but the feeding inhibition due to learning or partial satiation should be more subject to cost-benefit decisions based on feeding stimulus quality and incentive. Thus, the decision to swim instead of feed is virtually irreversible. In contrast, feeding suppression by learning or satiation can be rapidly released once an elevated stimulus threshold is exceeded.
|
ROLES IN BEHAVIORAL AROUSAL |
|---|
|
TOP
SYNOPSISINTRODUCTIONTHE ESCAPE SWIM CPG...MECHANISMS OF PATTERN GENERATION...SINGLENESS OF ACTION DURING...ROLES IN BEHAVIORAL AROUSALBEHAVIORAL ROLES OUTSIDE OF...References |
|---|
5-HT acts like a general arousal factor in mollusks (Kupfermann and Weiss, 1981
; Sakharov, 1990). In Pleurobranchaea, exogenous 5-HT generally increases spontaneous activity and reactivity to sensory stimuli, notably lowers feeding thresholds in intact animals, and stimulates fictive feeding activity in the isolated CNS (Gillette et al., 1997). The arousal actions of 5-HT in the mollusk partly resemble those in the mammalian CNS, where descending serotonergic fibers from the raphe nuclei stimulate the excitability of motor networks in motor nuclei and spinal cord. However, the mollusks appreciably contrast with mammals in that their serotonergic elements are embedded in the various motor networks as intrinsic elements (Gillette and Davis, 1977; Weiss et al., 1982; McPherson and Blankenship, 1991; Katz and Frost, 1996), such that neuromodulatory motor arousal could be effected through activity in the various sub-systems serving feeding, locomotor and defensive behaviors (Jing and Gillette, 2000). These findings appear to partly define and elucidate the organization of a CNS-wide serotonergic arousal system in which the As1–4 may play a central role.
The observations suggest that the serotonergic arousal system comprises distributed but coupled arousal sub-systems for defensive reactions and feeding, and show how they are linked together (Fig. 4). Highlighted in particular are dual roles for As1–4 as 1) intrinsic neuromodulatory components of the swim pattern generator, and as 2) hierarchic central organizers of general arousal. As1–4, acting largely as excitatory neuromodulators, participate in neural networks for multiple defense-related behaviors, including escape swimming, locomotion, avoidance turning (Jing and Gillette, 1996; Jing, 1998), and perhaps reflexive withdrawal as do the homologous neurons of Tritonia (Getting and Dekin, 1985). As well, As1–4 provide direct excitation to serotonergic elements of the feeding arousal system, the metacerebral giants (MCGs) and the adjacent Anterior Cerebral (AC) cluster (Jing and Gillette, 2000). The MCGs are embedded in the feeding motor network where they act as intrinsic neuromodulators; the adjacent, coupled AC cluster may have a similar role, as these cells are likewise activated during feeding motor program (Gillette and Davis, 1977).
As1–4 also drive the serotonergic locomotor G neurons of the pedal ganglion (Jing and Gillette, 2000). The G neurons correspond to serotonergic locomotor neurons in pedal ganglia of other species: excitors of ciliary locomotion in Tritonia (Audesirk et al., 1979) and Lymnaea (Syed and Winlow, 1989), of both parapodal swimming and pedal muscular wave locomotion in Aplysia (McPherson and Blankenship, 1991, 1992), and of parapodal locomotion in the pteropod Clione (Satterlie, 1995). The combined phasic and tonic excitation of the serotonergic locomotor cells by As1–4 resembles the premotor neuromodulatory excitation of the locomotor cells in Clione noted by Satterlie and Norekian (1996), and may represent evolutionary conservation of neural circuit and function in the face of changing structure and function in the periphery, as was lucidly suggested for evolution of leech feeding mechanisms (Lent et al., 1989). The premotor role of the As1–4 in locomotion may be manifest in their prolonged activity following a swim, a period during which Pleurobranchaea displays rapid creeping locomotion (Gillette et al., 1991).
The lack of contribution by As1–4 to feeding inhibition during the swim distinguishes them from the other swim premotor neurons. Rather, their effects on the feeding network are stimulatory in the sense of prolonged network excitation (Jing and Gillette, 2000). The As1–4 provide potent phasic and tonic excitation to modulatory serotonergic cells of the feeding network: the MCGs and their adjacent coupled cells of the anterior cerebral clusters. The MCGs, known mediators of feeding arousal in diverse gastropods (Gillette and Davis, 1977; Granzow and Fraser-Rowell, 1981; Weiss et al., 1982; Rosen et al., 1989; Yeoman et al., 1996), innervate Pleurobranchaea's buccal ganglion, buccal musculature and lip area, and stimulate the feeding oscillator network of the buccal ganglion (Gillette and Davis, 1977), while the anterior cerebral cluster may provide the serotonergic innervation of the oral veil musculature and chemosensory epithelium (Moroz et al., 1997), both involved in motor and sensory aspects of feeding behavior. Thus, the arousal role of the As1–4 extends across defensive and locomotor behaviors to feeding.
Also consistent with neuromodulatory stimulation of the feeding network was the finding that As1–4 caused slow excitation of the major I2 retractor interneurons of the feeding network (Jing and Gillette, 2000). Cyclic activity in the I2s is necessary to the feeding motor pattern, and tonic activity underlies the suppression of feeding in food-avoidance trained and satiated animals (see last section). The I2s also directly phasically excite the MCGs (London and Gillette, 1984), thus adding another feed-forward path in the serotonergic arousal system.
|
BEHAVIORAL ROLES OUTSIDE OF THE ESCAPE SWIM |
|---|
|
TOP
SYNOPSISINTRODUCTIONTHE ESCAPE SWIM CPG...MECHANISMS OF PATTERN GENERATION...SINGLENESS OF ACTION DURING...ROLES IN BEHAVIORAL AROUSALBEHAVIORAL ROLES OUTSIDE OF...References |
|---|
Directional turning, both avoidance and orienting, is supported by the As1–4 cells. One of us has reported in his Ph.D. dissertation (Jing, 1998
; paper in preparation) neurons in the A cluster, the bilaterally paired A4 cells, that are necessary and sufficient to the avoidance turn. Only a single unilateral A4 is activated during avoidance turning. When an ipsilateral A4 is hyperpolarized, the avoidance turn response to an electric shock to the oral veil is prevented, and when driven, it causes neural activity with characters similar to the stereotypic avoidance turn. The As1–4 are electrically and chemically coupled with A4. Activity in the As1–4s accompanies the A4 and must be present to support the tonic firing of the unilateral A4 during avoidance turn. Other evidence (Hatcher et al., 1998) suggests that the As1–4s by themselves may cause orienting turns.
In the greater context of Pleurobranchaea's repertory of behavior, the escape swim is an expensive one in terms of energy spent, and danger of being swept away by currents from a home patch of available mates and food sources (See also Willows, 2001). It is consequently a high-threshold behavior only reliably triggered by recognition of a highly vulnerable situation, specifically the presence of a larger, cannibal conspecific (Hatcher et al., 1994). Thus, where evading the maximum cost (death) is overwhelmingly justified, the cost of swimming can be a bargain. Evidence that the swim CPG evolved from neurons already present in the opisthobranch CNS and used for other purposes rests on the likely homologies of the serotonergic As1–4 and to the prominence of likely A1 homologs in other, non-swimming, mollusks (Jing and Gillette, 1999). The multifunctional roles of the CPG elements outside of swimming behavior reinforce this view. Figure 4 summarizes our present knowledge of how the neurons of the CPG function to integrate the animals' behavior.
Two major themes are embedded in the network interactions of Figure 4: 1) singleness of behavioral action, and 2) the outlines of regional differentiation and spatial integration within a widespread serotonergic arousal network. Singleness of action, or unitary expression of behavior, is ensured by inhibitory connections from one network to another, so that activation of one network inhibits antagonistic behavioral output (reviewed in Jing and Gillette, 1999). Similarly, the model shows where feeding behavior can be inhibited by the escape swim (by direct activation of the I1 neurons) or conditions of satiation and prior food-avoidance training (by activation of the I2s; Davis and Mpitsos, 1971; Davis and Gillette, 1978; Davis et al., 1983; London and Gillette, 1986). Satiation and food avoidance learning act through inhibition exerted at specific command neurons necessary and sufficient to active feeding, but in this case inhibition can be often overcome by raising the feeding network excitation; for instance, by increasing the strength of the food stimulus. The escape swim causes a more global inhibition including other major interneurons of the feeding network (Jing and Gillette, 2000), appropriately for an escape response. The swim may also effectively suppress the orienting and avoidance turns by commandeering the As1–4s, critical for the turns, for its own pattern generation; other yet unidentified mechanisms may act as well.
There are points not yet understood. How does feeding suppress avoidance, but not orienting, turns? How does feeding suppress locomotion? Kovac and Davis (1977, 1980) showed that feeding-induced suppression of withdrawal caused by a mechanical stimulus was due to corollary discharge (CD) of certain feeding interneurons that reduced sensory excitation of withdrawal motorneurons. We postulate a similar mechanism acting to suppress locomotion during feeding (cf. Jing, 1998).
A role for the serotonergic neurons of the CNS as a distributed arousal network, somewhat analogous to the reticular activating network of mammals, is gaining currency among molluskan neuroethologists, based on evidence from all the different preparations being studied. In Pleurobranchaea, the serotonergic cells form an interconnected network of neurons that provide intrinsic excitatory neuromodulation to the different networks within which they reside. The As1–4 cells appear to exert a potentially dominant position in the serotonergic network, as their activity can stimulate all the other serotonergic cells known. Table 1 summarizes the known and suspected functions of the various identified serotonergic neurons of Pleurobranchaea.
|
We hope that the syntheses, speculations and hypotheses we have put forward in this review will serve to stimulate future research.
|
ACKNOWLEDGMENTS |
|---|
The symposium was supported by National Science Foundation grant BN 9905990.
|
FOOTNOTES |
|---|
1 From the Symposium Swimming in Opisthobranch Mollusks: Contributions to Control of Motor Behaviour presented at the Annual Meeting of the Society for Integrative and Comparative Biology, 4–8 January 2000, at Atlanta, Georgia.
2 E-mail: rhanor{at}life.uiuc.edu
3 Present address: Department of Physiology & Biophysics, Box 1218, Mt. Sinai School of Medicine, One Gustave L. Levy Place, New York, New York 10029-6574
|
References |
|---|
|
TOP
SYNOPSISINTRODUCTIONTHE ESCAPE SWIM CPG...MECHANISMS OF PATTERN GENERATION...SINGLENESS OF ACTION DURING...ROLES IN BEHAVIORAL AROUSALBEHAVIORAL ROLES OUTSIDE OF...References |
|---|
Audesirk, G. J., R. E. McCaman, and A. O. Willows. 1979. The role of serotonin in the control of pedal ciliary activity by identified neurons in Tritonia diomedea. Comp. Biochem. Physiol. [C], 62C:87-91.[CrossRef]
Davis, W. J., and R. Gillette. 1978. Neural correlates of behavioral plasticity in command neurons in Pleurobranchaea. Science, 199:801-804.
Davis, W. J., R. Gillette, M. P. Kovac, R. P. Croll, and E. M. Matera. 1983. Organization of synaptic inputs to paracerebral feeding command interneurons of Pleurobranchaea californica. III. Modifications induced by experience. . J. Neurophysiol, 49:1557-1572.
Davis, W. J., and G. J. Mpitsos. 1971. Behavioral choice and habituation in the marine mollusk Pleurobranchaea californica. Z. Vergl. Physiol, 75:207-232.
Davis, W. J., G. J. Mpitsos, and J. M. Pinneo. 1974. The behavioral hierarchy of the Pleurobranchaea. I. The dominant position of the feeding behavior. J. Comp. Physiol, 90:207-224.[CrossRef]
Friesen, W. O. 1994. Reciprocal inhibition: A mechanism underlying oscillatory animal movements. Neurosci. Biobehav. Rev, 18:547-553.[CrossRef][ISI][Medline]
Getting, P. A. 1988. Comparative analysis of invertebrate central pattern generators. In A. H. Cohen, S. Rossignol, and S. Grillner (eds.), Neural control of rhythmic movements in vertebrates, pp. 101–127. John Wiley & Sons, New York.
Getting, P. A. 1989. A network oscillator underlying swimming in Tritonia. In J. W. Jacklet (ed.), Neuronal and cellular oscillators, pp. 215–236. Marcel Dekker, Inc., New York.
Getting, P. A., and M. S. Dekin. 1985. Mechanisms of pattern generation underlying swimming in Tritonia. IV. Gating of central pattern generator. J. Neurophysiol, 53:466-480.
Gillette, R., and W. J. Davis. 1977. The role of the metacerebral giant neurone in the feeding behaviour of Pleurobranchaea. J. Comp. Physiol, 116:129-159.[CrossRef]
Gillette, R., R.-C. Huang, N. Hatcher, and L. L. Moroz. 2000. Cost-benefit analysis potential in feeding behavior of a predatory snail by integration of hunger, taste and pain. Proc. Natl. Acad. Sci. U.S.A, 97:3585-3590.
Gillette, R., L. L. Moroz, R. Fuller, and J. V. Sweedler. 1997. 5-HT and NO co-localized in neurons of feeding and locomotor networks may interact to regulate hunger state in Pleurobranchaea. Soc. Neurosci, 23:978(Abstr.).
Gillette, R., M. Saeki, and R.-C. Huang. 1991. Defense mechanisms in notaspidean snails: Acid humor and evasiveness. J. Exp. Biol, 156:335-347.
Granzow, B., and C. H. Fraser-Rowell. 1981. Further observations on the serotonergic cerebral neurons of Helisoma (Mollusca, Gastropoda): The case for homology with the metacerebral giant cells. J. Exp. Biol, 90:283-306.
Hatcher, N., J. Jing, and R. Gillette. 1998. Avoidance and orienting turning in the predatory sea slug Pleurobranchaea californica. Soc. Neurosci, 24:1700(Abstr.).
Hatcher, N., M. Mickiewicz, M. U. Gillette, and R. Gillette. 1994. Cataloguing aversive behavior and stimuli in the predatory seaslug Pleurobranchaea. Soc. Neurosci, 20:580(Abstr.).
Huang, K., L. L. Moroz, L. C. Sudlow, and R. Gillette. 1998. NO and 5-HT may regulate feeding network arousal state in Pleurobranchaea californica. Soc. Neurosci, 24:1840(Abstr.).
Jing, J. 1998. Interacting premotor networks mediating behavioral selection in the predatory marine snail Pleurobranchaea californica. Ph.D. Diss., University of Illinois, Urbana, Illinois.
Jing, J., and R. Gillette. 1995. Neuronal elements that mediate escape swimming and suppress feeding behavior in the predatory sea slug Pleurobranchaea. J. Neurophysiol, 74:1900-1910.
Jing, J., and R. Gillette. 1996. Turning behavior in the predatory sea slug Pleurobranchaea: Functional anatomy and neural mechanisms. Soc. Neurosci, 22:1404(Abstr.).
Jing, J., and R. Gillette. 1999. Central pattern generator for escape swimming in the notaspid sea slug Pleurobranchaea californica. J. Neurophysiol, 81:654-667.
Jing, J., and R. Gillette. 2000. Escape swim network interneurons have diverse roles in behavioral switching and putative arousal in Pleurobranchaea. J. Neurophysiol, 83:1346-1355.
Jing, J., L. C. Sudlow, and R. Gillette. 1997. Mechanisms of pattern generation of escape swimming and potential role of cAMP-gated cation current in the sea slug Pleurobranchaea. Soc. Neurosci, 23:1047(Abstr.).
Katz, P. S., and W. N. Frost. 1996. Intrinsic neuromodulation: Altering neuronal circuits from within. Trends Neurosci, 19:54-61.[CrossRef][ISI][Medline]
Katz, P. S., and W. N. Frost. 1997. Removal of spike frequency adaptation via neuromodulation intrinsic to the Tritonia escape swim central pattern generator. J. Neurosci, 17:7703-7713.
Katz, P. S., P. A. Getting, and W. N. Frost. 1994. Dynamic neuromodulation of synaptic strength intrinsic to a central pattern generator circuit. Nature, 367:729-731.[CrossRef][Medline]
Kovac, M. P., and W. J. Davis. 1977. Behavioral choice: Neurophysiological mechanism in Pleurobranchaea. Science, 198:632-634.
Kovac, M. P., and W. J. Davis. 1980. Neural mechanism underlying behavioral choice in Pleurobranchaea. J. Neurophysiol, 43:469-487.
Kupfermann, I., and K. R. Weiss. 1981. The role of serotonin in arousal of feeding behavior of Aplysia. In B. E. Jacobs and A. Gelperin (eds.), Serotonin neurotransmission and behavior, pp. 255–287. MIT Press, Cambridge.
Lennard, P. R., P. A. Getting, and R. I. Hume. 1980. Central pattern generator mediating swimming in Tritonia. II. Initiation, maintenance, and termination. . J. Neurophysiol, 44:165-173.
Lent, C. M., M. H. Dickinson, and C. G. Marshall. 1989. Serotonin and leech feeding behavior: Obligatory neuromodulation. Amer. Zool, 29:1241-1254.
London, J. A., and R. Gillette. 1984. Functional roles and circuitry in an inhibitory pathway to feeding command neurones in Pleurobranchaea. J. Exp. Biol, 113:423-446.
London, J. A., and R. Gillette. 1986. Mechanism for food avoidance learning in the central pattern generator of feeding behavior of Pleurobranchaea californica. Proc. Natl. Acad. Sci. U.S.A, 83:4058-4062.
McPherson, D. R., and J. E. Blankenship. 1991. Neural control of swimming in Aplysia brasiliana. III. Serotonergic modulatory neurons. . J. Neurophysiol, 66:1366-1379.
McPherson, D. R., and J. E. Blankenship. 1992. Neuronal modulation of foot and body-wall contractions in Aplysia californica. J. Neurophysiol, 67:23-28.
Moroz, L. L., L. C. Sudlow, J. Jing, and R. Gillette. 1997. Serotonin-immunoreactivity in peripheral tissues of the opistobranch molluscs Pleurobranchaea californica and Tritonia diomedea. J. Comp. Neurol, 382:176-188.[CrossRef][ISI][Medline]
Mpitsos, G. J. Collins., and S. D. 1978. Learning: Rapid aversive conditioning in the gastropod mollusk Pleurobranchaea. Science, 188:954-957.
Mpitsos, G. J., and W. J. Davis. 1973. Learning: Classical and avoidance conditioning in the mollusk Pleurobranchaea. Science, 180:317-320.
Rosen, S. C., K. R. Weiss, R. S. Goldstein, and I. Kupfermann. 1989. The role of a modulatory neuron in feeding and satiation in Aplysia: Effects of lesioning of the serotonergic metacerebral cells. J. Neurosci, 9:1562-1578.[Abstract]
Sakharov, D. A. 1990. Integrative functions of serotonin common to distant related invertebrate animals. In M. K. S. Gustafsson and M. Reuter (eds.), The early brain, pp. 73–88. Abo Akademy Press, Abo.
Satterlie, R. A. 1995. Serotonergic modulation of swimming speed in the pteropod mollusc Clione limacina. II. Peripheral modulatory neurons. . J. Exp. Biol, 198:905-916.
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]
Schmekel, L. 1985. Aspects of evolution within the opisthobranchs. In E. R. Trueman and M. R. Clarke (eds.), The Mollusca, Editor-in-Chief, K. M. Wilbur, Vol. 10, Evolution, pp. 221–267. Academic Press, Inc., New York.
Sudlow, L. C., and R. Gillette. 1995. Cyclic AMP-gated sodium current in neurons of the pedal ganglion of Pleurobranchaea californica is activated by serotonin. J. Neurophysiol, 73:2230-2236.
Syed, N. I., and W. Winlow. 1989. Morphology and electrophysiology of neurons innervating the ciliated locomotor epithelium in Lymnaea stagnalis (L.). . Comp. Biochem. Physiol, 93:633-644.[CrossRef]
Weiss, K. R., U. T. Koch, J. Koester, S. C. Rosen, and I. Kupfermann. 1982. The role of arousal in modulating feeding behavior of Aplysia: Neural and behavioral studies. In B. G. Hoebel and D. Novin (eds.), The neural basis of feeding and reward, pp. 25–57. Haer Institute, Brunswick, Maine.
Willows, A. O. D. 2001. Costs and benefits of Opisthobranch swimming and neurobehavioral mechanisms. Amer. Zool, 41:943-951.[CrossRef]
Yeoman, M. S., M. J. Brierley, and P. R. Benjamin. 1996. Central pattern generator interneurons are targets for the modulatory serotonergic cerebral giant cells in the feeding system of Lymnaea. J. Neurophysiol, 75:11-25.
CiteULike 
Connotea 
Del.icio.us What's this?
| ||||||||||||||||||||||||||||||||||||||||||||||||||