Neural control of locomotion in Aplysia: Role of the Central Ganglia

doi:10.1016/S0163-1047(79)92744-4

Behavioral and Neural Biology

Volume 27, Issue 1, September 1979, Pages 39-58

https://doi.org/10.1016/S0163-1047(79)92744-4 Get rights and content

In this study the effects of connective lesions on the control of pedal locomotion in Aplysia californica were examined. Normal goal directed locomotion consists of a behavioral sequence. The foot is detached, extended, and the anterior edge reattached. A series of waves are generated in the resulting arch which pull the animal forward. Escape locomotion is similar except that the foot extension is exaggerated; the entire body contracts off the substrate and the tail is released following anterior foot attachment. When the cerebropedal and cerebropleural connectives were bilaterally sectioned, locomotion was abolished. Bilateral sectioning of the cerebropedal connectives alone also eliminated the first phases of normal locomotion, although limited pedal waves were still generated. Bilateral sectioning of the cerebropleural connectives only eliminated escape locomotion. Cutting the pleuropedal connectives greatly reduced the rate of normal locomotion and also abolished escape locomotion. Unilateral section of the cerebropedal and cerebropleural connectives resulted in reduced motor activity on the lesioned side, with diagonally running pedal waves (lesioned side trailing) in the foot. Sectioning the pedal commissure caused the motor activity of each hemifoot to become desynchronized. When the pedal ganglia were isolated by cutting both the cerebropedal and pleuropedal connectives limited pedal waves were still generated, although the initial phases of the locomotor sequence were absent. These results suggest that the different parts of the locomotor control system are localized in separate ganglia. The motor pattern generators reside in each pedal ganglion with coordination maintained by the pedal commissure. The results are consistent with the hypothesis that the commands for initiating locomotion originate in the cerebral ganglion and descend to the pedal ganglia via the cerebropedal connectives. The pleural ganglia apparently serve both to modulate the rate of locomotion and as a relay for input to the cerebral ganglion.

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Cited by (37)

Sensitized by a sea slug: Site-specific short-term and general long-term sensitization in Aplysia following Navanax attack
2022, Neurobiology of Learning and Memory
Citation Excerpt :
thereby reducing the probability of the lobster relocating them after it has recovered from the ink/opaline. This post-attack escape behavior by Aplysia reasonably requires full participation of the head and tail to realize maximal speed (Jahan-Parwar & Fredman, 1979; Leonard & Lukowiak, 1984,1986); protracted withdrawal of either is likely to slow the escape. After sufficient distance has been attained by the galloping sea hare, sensitization is adaptively activated to a wide range of stimuli to help protect the once-attacked sea hare from further attacks (Walters, 1991).
Neurobiological studies of the model species, Aplysia californica (Mollusca, Gastropoda, Euopisthobranchia), have helped advance our knowledge of the neural bases of different forms of learning, including sensitization, a non-associative increase in withdrawal behaviors in response to mild innocuous stimuli. However, our understanding of the natural context for this learning has lagged behind the mechanistic studies. Previous studies, which exclusively used artificial stimuli, such as electric shock, to produce sensitization, left open the question of which stimuli might cause sensitization in nature. Our laboratory first addressed this question by testing for short and long-term sensitization after predatory attack by a natural predator, the spiny lobster. In the present study, we tested for sensitization after attack by a very different predator, the predacious sea-slug, Navanax inermis (Mollusca, Gastropoda, Euopisthobranchia).
Unlike the biting and prodding action of lobster attack, Navanax uses a rapid strike that sucks and squeezes its prey in an attempt to swallow it whole. We found that Navanax attack to the head of Aplysia caused strong immediate sensitization of head withdrawal, and weaker, delayed, sensitization of tail-mantle withdrawal. By contrast, attack to the tail of Aplysia resulted in no sensitization of either reflex. We also developed an artificial attack stimulus that allowed us to mimick a more consistently strong attack. This artificial attack produced stronger but qualitatively similar sensitization: Strong immediate sensitization of head withdrawal and weaker sensitization of tail-mantle withdrawal after head attack, immediate sensitization in tail-mantle withdrawal, but no sensitization of head withdrawal after tail attack. We conclude that Navanax attack causes robust site-specific sensitization (enhanced sensitization near the site of attack), and weaker general sensitization (sensitization of responses to stimuli distal to the attack site).
We also tested for long-term sensitization (lasting longer than 24 h) after temporally-spaced delivery of four natural Navanax attacks to the head of subject Aplysia. Surprisingly, these head attacks, any one of which strongly sensitizes head withdrawal in the short term, failed to sensitize head-withdrawal in the long term. Paradoxically, these repeated head attacks produced long-term sensitization in tail-mantle withdrawal.
These experiments and observations confirm that Navanax attack causes short, and long-term sensitization of withdrawal reflexes of Aplysia. They add site-specific sensitization as well as paradoxical long-term sensitization of tail-mantle withdrawal to a short list of naturally induced learning phenotypes in this model species. Together with previous observations of sensitization after lobster attack, these data strongly support the premise that sensitization in Aplysia is an adaptive response to sub-lethal predator attack.
A comparison of hatchery-rearing in exercise to wild animal physiology and reflex behavior in Aplysia californica
2018, Comparative Biochemistry and Physiology -Part A : Molecular and Integrative Physiology
Citation Excerpt :
Finally, there may be little similarity between the energetics of vertebrate skeletal muscle and the network of longitudinal and transverse muscle fibers that form the foot muscle of Aplysia. Aplysia TWR recruits foot and tail adherence muscles used in escape locomotion (Jahan-Parwar and Fredman, 1979; Flinn et al., 2001). The same muscles are likely recruited in adherence to the substrate, such as in flume tests.
Aplysia californica was hatchery-reared in two turbulence protocols intended to imitate the intermittent turbulence of the native habitat and to promote development of the foot muscle from the exercise of adhering to the substrate. Hatchery-reared animals in turbulence regimes were compared to siblings reared in quiet water, and to wild animals, using noninvasive assessments of the development of the foot muscle. The objective was to learn if the turbulence-reared phenotype mimicked laboratory-targeted aspects of the wild phenotype, that is, reflex behavior, swim tunnel performance, and resting oxygen consumption (MO₂). No group exhibited different MO₂. MO₂ values for all of the compared groups of animals followed the power law, with an exponent of 0.69, consistent with this relationship throughout the animal kingdom. Turbulence-induced exercise did not affect the righting reflex or the tail withdrawal reflex, standard behavioral tests that involve the foot muscle, compared to quiet water-reared siblings. Wild individuals had significantly shorter time-to-right than all hatchery reared animals, however, wild animals did not perform better in flume tests. That turbulence-reared hatchery- or wild animals lacked superior flume performance suggests that this species may shelter from intertidal wave energy to remain near its optimal feeding areas.
Modular deconstruction reveals the dynamical and physical building blocks of a locomotion motor program
2015, Neuron
Citation Excerpt :
To address these issues, we imaged populations of neurons in the pedal ganglion of the sea-slug Aplysia while reliably eliciting its motor program for locomotion. The pedal ganglion contains approximately 1,600 neurons (Cash and Carew, 1989) and wholly contains the rhythmic pattern generator (Jahan-Parwar and Fredman, 1979, 1980), motorneurons (Hening et al., 1979; Fredman and Jahan-Parwar, 1980), and associated neuromodulatory neurons (Hall and Lloyd, 1990; McPherson and Blankenship, 1992) for locomotion, thus making it a tractable target for mapping a motor program to the dynamics and structure of its underlying distributed network. This mixture of systems means that population imaging of the Aplysia pedal ganglion is representative of the analytical challenges that will become increasingly common for large-scale recordings of complex neural systems (Cunningham and Yu, 2014), as we know that the recorded populations will have captured multiple dynamical systems within them.
The neural substrates of motor programs are only well understood for small, dedicated circuits. Here we investigate how a motor program is constructed within a large network. We imaged populations of neurons in the Aplysia pedal ganglion during execution of a locomotion motor program. We found that the program was built from a very small number of dynamical building blocks, including both neural ensembles and low-dimensional rotational dynamics. These map onto physically discrete regions of the ganglion, so that the motor program has a corresponding modular organization in both dynamical and physical space. Using this dynamic map, we identify the population potentially implementing the rhythmic pattern generator and find that its activity physically traces a looped trajectory, recapitulating its low-dimensional rotational dynamics. Our results suggest that, even in simple invertebrates, neural motor programs are implemented by large, distributed networks containing multiple dynamical systems.
Neuronal Transcriptome of Aplysia: Neuronal Compartments and Circuitry
2006, Cell
Citation Excerpt :
As with C. elegans, the identified nerve cells in Aplysia form precise connections with one another. Thus, the connections between identified cells of a neural circuit can be mapped on a cell-to-cell basis for a variety of behaviors ranging in complexity from simple withdrawal reflexes to complex fixed action patterns such as locomotion, feeding, and defense reactions (Hening et al., 1979; Jahan-Parwar and Fredman, 1979; Kupfermann, 1974; Kupfermann and Kandel, 1969). Moreover, these behaviors are modulated by various forms of nonassociative and associative forms of learning, as well as by arousal and motivational states (Cleary and Byrne, 1993; Kupfermann and Weiss, 1982; Rosen et al., 1989; Fitzgerald et al., 1997; Kandel, 2001).
Molecular analyses of Aplysia, a well-established model organism for cellular and systems neural science, have been seriously handicapped by a lack of adequate genomic information. By sequencing cDNA libraries from the central nervous system (CNS), we have identified over 175,000 expressed sequence tags (ESTs), of which 19,814 are unique neuronal gene products and represent 50%–70% of the total Aplysia neuronal transcriptome. We have characterized the transcriptome at three levels: (1) the central nervous system, (2) the elementary components of a simple behavior: the gill-withdrawal reflex—by analyzing sensory, motor, and serotonergic modulatory neurons, and (3) processes of individual neurons. In addition to increasing the amount of available gene sequences of Aplysia by two orders of magnitude, this collection represents the largest database available for any member of the Lophotrochozoa and therefore provides additional insights into evolutionary strategies used by this highly successful diversified lineage, one of the three proposed superclades of bilateral animals.
The effect of dopamine receptor blockade on motor behavior in Aplysia californica
2001, Pharmacology Biochemistry and Behavior
The mammalian D1- and D2-like receptor blockers SCH-23390 and raclopride were used to block receptors in Aplysia californica, and the effect on reflexes and escape behavior was examined. Four groups of 20 young adults were each injected with SCH-23390, raclopride, SCH-23390+raclopride, or seawater. The drug (0.0125 mg/g of body weight) was injected 2 mm anterior to the parapodia. After the injection of either SCH-23390 or SCH-23390+raclopride, there was a significant increase in parapodia opening (P<.001), siphon withdrawal (P<.05), and galloping following tail pinch (P<.01) compared to raclopride-injected or control animals. The data showed that blockade of receptors by SCH-23390, but not raclopride, produced significant changes in motor behavior in A. californica.
Neural regeneration in gastropod molluscs
1995, Progress in Neurobiology
Snails recover function following a variety of neural injuries. They grow new tentacles with associated tentacle ganglia, selectively reinnervate peripheral targets, repair central connections and may even replace lost neurons and ganglia. The plasticity revealed in their responses to neural injury is an extreme expression of the adaptability observed in studies of learning and age-related changes in the nervous system. Recent information on neurogenesis in gastropods is providing a basis for comparing developmental events with neural regeneration. Studies of neural regeneration in gastropods have capitalized on our ability to identify many gastropod neurons individually and characterize the cellular properties and network properties that generate output patterns that underlie behaviors. The robustness of the model systems formed by cultured gastropod neurons is apparent in the similarity of the activity patterns in circuits formed in vitro and in vivo. Cell membrane repair, activation of an altered pattern of protein synthesis, and observation of the searching action of the growth cones can be studied under defined conditions that promote or inhibit the processes. Basic properties of growth cones, the molecular binding and second messenger systems underlying adhesion, sprouting and pathfinding, and events in synaptogenesis are accessible to analysis. Rules that govern selection of synaptic partners are being evaluated on the basis of cellular characteristics such as transmitter and receptor expression and ganglion of origin. The conservation of the molecular language that governs growth and communication between cells suggests that information gained in such studies may some day be applied to promote neural regeneration in mammals.

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¹: This work was supported by PHS Grant NS 12483 to B.J.-P. Part of this study was conducted at the Marine Biological Laboratory at Woods Hole, Mass., and supported by a grant from the Grass Foundation.

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Behavioral and Neural Biology

References (28)

Intra- and Interganglionic Synaptic Connections in the CNS of Aplysia

Brain Research Bulletin

Pedal locomotion in Aplysia californica. I. Sensory and motor fields of pedal nerves

Comparative Biochemistry and Physiology

Role of Interganglionic Synaptic Connections in the Control of Pedal and Parapodial Movements in Aplysia

Brain Research Bulletin

Dissociation of the appetitive and consummatory phases of feeding behavior in Aplysia: A lesion study

Behavioral Biology

Neuronal organization and ontogeny in the lobster swimmeret system

Distributed neuronal oscillators and efference copy in the feeding system of Pleurobranchaea

Journal of Neurophysiology

Über Bau and Funktion der Statocyste bei der Schnecke Aplysia limacina

Zeitschrift für Vergleichende Physiologie

Response of Aplysia statocyste receptor cells to physiologic stimulation

Journal of Physiology

Some aspects of the descending control of spinal circuits generating locomotor movements