Aplysia Siphon Withdrawal Research Articles

The contributions and mechanisms of changes in excitability during simple forms of learning in Aplysia.

Learning and memory have long been thought to involve changes in synaptic connections between neurons. However, in many cases learning-related plasticity also involves changes in the excitability of neurons. These findings have raised questions about the relative importance of these two types of mechanisms to behavioral learning, and also about the extent to which they involve shared or unique molecular mechanisms. We have taken a reductionist approach to these questions by addressing them in a simple model organism, Aplysia californica. Studies of a semi-intact Aplysia siphon withdrawal preparation suggest that classical conditioning involves an increase in the evoked firing of sensory neurons (SNs) as well as facilitation of the monosynaptic PSP to motor neurons (MNs). Furthermore, these two mechanisms may act cooperatively at the cellular level: increased SN firing produces more PSPs, each of which is facilitated, leading to a multiplicative increase in depolarization of the MN and siphon withdrawal. The changes in SN firing and the monosynaptic PSP also share several mechanisms at the molecular level, suggesting that they may both be due in part to a decrease in K+ current that causes an increase in SN excitability as well as an increase in SN spike width and thus increased transmitter release. However, changes in the monosynaptic PSP also involve additional mechanisms that are not shared and may affect different aspects of synaptic transmission as well. Studies of operant conditioning of feeding suggest that it involves similar mechanisms as classical conditioning of siphon withdrawal. In particular, for both types of associative learning adenylyl cyclase appears to serve as a molecular coincidence detector that leads to increased activation of PKA and changes in excitability of key neurons in the neural circuit. Furthermore, in both cases those changes in excitability make an important contribution to the behavioral learning.

Intermediate-term memory in Aplysia involves neurotrophin signaling, transcription, and DNA methylation

Long-term but not short-term memory and synaptic plasticity in many brain areas require neurotrophin signaling, transcription, and epigenetic mechanisms including DNA methylation. However, it has been difficult to relate these cellular mechanisms directly to behavior because of the immense complexity of the mammalian brain. To address that problem, we and others have examined numerically simpler systems such as the hermaphroditic marine mollusk Aplysia californica. As a further simplification, we have used a semi-intact preparation of the Aplysia siphon withdrawal reflex in which it is possible to relate cellular plasticity directly to behavioral learning. We find that inhibitors of neurotrophin signaling, transcription, and DNA methylation block sensitization and classical conditioning beginning ∼1 h after the start of training, which is in the time range of an intermediate-term stage of plasticity that combines elements of short- and long-term plasticity and may form a bridge between them. Injection of decitabine (an inhibitor of DNA methylation that may have other actions in these experiments) into an LE sensory neuron blocks the neural correlates of conditioning in the same time range. In addition, we found that both DNA and RNA methylation in the abdominal ganglion are correlated with learning in the same preparations. These results begin to suggest the functions and integration of these different molecular mechanisms during behavioral learning.

Network processes involved in the mediation of short-term habituation in Aplysia: contribution of intrinsic regulation of excitability and synaptic augmentation

Short-term habituation (STH) is the decrease in behavioral responding observed during repeated stimulation at regular intervals. For siphon-elicited siphon withdrawal in Aplysia (S-SWR), we previously showed that the amplitude of responses measured in LFS-type siphon motor neurons (LFS MNs) during training is dependent on the stimulus interval used and is training-site specific. The major source of excitation from siphon stimulation onto the LFS MNs comes from the L29 interneurons. Here we examined the role of the L29s in STH by addressing two questions:(1) What are the relative contributions of intrinsic regulation of excitability and network inhibition on L29 activity during STH training?By activating L29s with intracellular current injection, we found that intrinsic changes in excitability occur, but only at short training intervals (1 s). We also demonstrated that network inhibition is not required for regulating L29 responses during training, indicating that any expression of inhibition is redundant to the excitability changes. (2) How does L29 synaptic plasticity contribute to the maintenance of training site-specificity exhibited in LFS MNs?When training stimuli are delivered 1 s apart [1 s, interstimulus interval (ISI)], L29 responses decrease in both stimulated (trained) and un-stimulated (untrained) pathways, yet site-specificity of training is maintained in the LFS MNs. Our results suggest that activity-dependent synaptic facilitation (augmentation; AUG) expressed by the L29s acts to compensate for the decreased activity in the untrained pathway. First, we demonstrated that the L29-LFS synapse exhibits significant AUG with L29 activation at a 1 s ISI. Second, we showed that the induction of AUG prevents the reduction in siphon-evoked LFS responses that is otherwise observed with decreased L29 activity. Collectively, our results support a role for the L29s in regulating network dynamics during STH training, but only at rapid (1 s ISI) training intervals.

The Role of Rapid, Local, Postsynaptic Protein Synthesis in Learning-Related Synaptic Facilitation in Aplysia

The discovery that dendrites of neurons in the mammalian brain possess the capacity for protein synthesis stimulated interest in the potential role of local, postsynaptic protein synthesis in learning-related synaptic plasticity. But it remains unclear how local, postsynaptic protein synthesis actually mediates learning and memory in mammals. Accordingly, we examined whether learning in an invertebrate, the marine snail Aplysia, involves local, postsynaptic protein synthesis. Previously, we showed that the dishabituation and sensitization of the defensive withdrawal reflex in Aplysia require elevated postsynaptic Ca(2+), postsynaptic exocytosis, and functional upregulation of postsynaptic alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA)-type glutamate receptors. Here, we tested whether the synaptic facilitation that underlies dishabituation and sensitization in Aplysia requires local, postsynaptic protein synthesis. We found that the facilitatory transmitter, serotonin (5-HT), enhanced the response of the motor neuron to glutamate, the sensory neuron transmitter, and this enhancement depended on rapid protein synthesis. By using individual motor neurites surgically isolated from their cell bodies, we showed that the 5-HT-dependent protein synthesis occurred locally. Finally, by blocking postsynaptic protein synthesis, we disrupted the facilitation of the sensorimotor synapse. By demonstrating its critical role in a synaptic change that underlies learning and memory in a major model invertebrate system, our study suggests that local, postsynaptic protein synthesis is of fundamental importance to the cell biology of learning.

Dynamic regulation of the siphon withdrawal reflex of Aplysia californica in response to changes in the ambient tactile environment.

The state of an animal's environment can be viewed as a source of information that can be used to regulate both ongoing and future behavior. The present work examined how the ambient environment can regulate the Aplysia siphon withdrawal reflex (SWR) by changing the environment between calm and turbulent. Results indicate that the SWR is dynamically regulated on the basis of variations in external conditions, so that responsiveness (measured as both reflex duration and threshold) is matched to the state of the environment. Prior exposure to a noxious stimulus (tailshock) has selective effects on this regulation, suggesting the existence of multiple regulatory mechanisms. Further, neurophysiological correlates to behavioral observations were measured in sensory and motor neurons. This will allow for a detailed cellular analysis of environmental information-processing in this system.

Structure of the network mediating siphon-elicited siphon withdrawal in Aplysia

1. The network mediating siphon-elicited siphon withdrawal in Aplysia is a useful model system for cellular studies of simple forms of learning and memory. Here we describe three new cells in this circuit, L33, L34, and L35, and several new connections among the following network neurons: LE, L16, L29, L30, L32, L33, L34, and L35. On the basis of these findings we present an updated diagram of the network. Altogether, 100 neurons have now been identified in the abdominal ganglion that can participate in both siphon-elicited and spontaneous respiratory pumping siphon withdrawals. 2. Two features of the interneuronal population may have important behavioral functions. First, the L29 interneurons make fast and slow excitatory connections onto the LFS cells, which may be important for transforming brief sensory neuron discharges into the long-lasting motor neuron firing that underlies withdrawal duration. Second, inhibitory interneurons are prominent in the network. The specific connectivity of certain of these interneurons is appropriate to block potentially interfering inhibitory inputs from other networks during execution of the behavior. 3. Deliberate searches have so far revealed very few excitatory interneuronal inputs to the network interneurons and motor neurons within the abdominal ganglion. These results, together with intracellular studies by others, are more consistent at present with a relatively dedicated rather than a highly distributed organizational scheme for the siphon-elicited siphon withdrawal circuitry.

Postsynaptic modifications in long-term facilitation in Aplysia: upregulation of excitatory amino acid receptors

Long-term sensitization of the gill and siphon withdrawal in Aplysia is accompanied by facilitation of sensorimotor synaptic connections that depends on new protein synthesis. This phenomenon has been previously shown to involve presynaptic growth. At the postsynaptic level, a reorganization should occur to parallel the formation of new synaptic contacts. We show here that 24 hr following an application of 5-HT, which produces long-term synaptic facilitation (LTF), the response of the motoneuron to an excitatory amino acid agonist of the synaptic receptors is increased. General inhibition of protein synthesis with anisomycin blocks this enhancement. Inhibiton of protein synthesis limited to the postsynaptic neuron by intracellular injection of gelonin, a ribosome-inactivating toxin, also blocks the increase in the response to the agonist but fails to block 24 hr LTF. These results are compatible with a model of LTF that involves coordinate pre- and postsynaptic changes. The latter may include an upregulation of functional postsynaptic receptors. These may not be initially required for LTF measured at a 24 hr time point, but could become necessary for later stages of LTF. An increase in the number of functional postsynaptic receptors in a reserve pool may also prime the postsynaptic neuron for subsequent learning-associated plasticity.

Effects of interstimulus interval and contingency on classical conditioning of the Aplysia siphon withdrawal reflex

The siphon withdrawal reflex of Aplysia undergoes differential classical conditioning with cutaneous stimulation of the siphon or mantle shelf as the discriminative conditioned stimuli (CS+ and CS-) and shock to the tail as the unconditioned stimulus (US). The reflex has proved to be useful for analyzing the neural mechanisms of conditioning. To test the generality of this experimental system, we have begun to compare the properties of conditioning in Aplysia with those of conditioning in vertebrates. We first examined the effect of the interstimulus interval (ISI) by varying the time between presentation of the CS+ and the US in different groups of animals. Significant differential conditioning was obtained when the onset of the CS+ preceded the onset of the US by 0.5 sec, and marginal conditioning was obtained when the ISI was 1.0 sec. By contrast, no significant conditioning occurred when the CS+ preceded the US by 2, 5, or 10 sec, when the onsets of the stimuli were simultaneous, or when US onset preceded the CS+ by 0.5, 1.0, or 1.5 sec (backward conditioning). We next examined the effect of contingency by giving one group of animals normal differential conditioning, and a second group the same training but with additional USs inserted between the paired trials. Presentation of these additional USs reduced the degree to which the US was contingent on the CS+, but did not change the number of pairings. Animals receiving normal training again showed significant conditioning, whereas animals receiving additional USs showed no conditioning.(ABSTRACT TRUNCATED AT 250 WORDS)

Is there a cell-biological alphabet for simple forms of learning?

Recent studies indicate that the cellular mechanism underlying classical conditioning of the Aplysia siphon withdrawal reflex is an extension of the mechanism underlying sensitization. This finding suggests that the mechanisms of yet higher forms of learning may similarly be based on the mechanisms of these simple forms of learning. We illustrate this hypothesis by showing how several higher order features of classical conditioning, including generalization, extinction, second-order conditioning, blocking, and the effect of contingency, can be accounted for by combinations of the cellular processes that underlie habituation, sensitization, and classical conditioning in Aplysia.

Mechanisms of pattern generation underlying swimming in Tritonia. II. Network reconstruction.

ArticlesMechanisms of pattern generation underlying swimming in Tritonia. II. Network reconstructionP. A. GettingP. A. GettingPublished Online:01 Apr 1983https://doi.org/10.1152/jn.1983.49.4.1017MoreSectionsPDF (3 MB)Download PDF ToolsExport citationAdd to favoritesGet permissionsTrack citations ShareShare onFacebookTwitterLinkedInWeChat Previous Back to Top Next Download PDF FiguresReferencesRelatedInformation Cited ByEmergence of in vitro preparations and their contribution to understanding the neural control of behavior in vertebratesJoyce Keifer24 August 2022 | Journal of Neurophysiology, Vol. 128, No. 3Modeling relationships between rhythmic processes and neuronal spike timingPamela D. Rivière, Gabriel Schamberg, Todd P. Coleman, and Lara M. Rangel26 August 2022 | Journal of Neurophysiology, Vol. 128, No. 3Hidden synaptic differences in a neural circuit underlie differential behavioral susceptibility to a neural injury11 June 2014 | eLife, Vol. 3Parameter Space Analysis Suggests Multi-Site Plasticity Contributes to Motor Pattern Initiation in TritoniaRobert J. Calin-Jageman, Mark J. Tunstall✠, Brett D. Mensh, Paul S. Katz, and William N. Frost1 October 2007 | Journal of Neurophysiology, Vol. 98, No. 4Cycle Period of a Network Oscillator Is Independent of Membrane Potential and Spiking Activity in Individual Central Pattern Generator NeuronsPaul S. Katz, Akira Sakurai, Stefan Clemens, and Deron Davis1 September 2004 | Journal of Neurophysiology, Vol. 92, No. 3G Protein Signaling in a Neuronal Network is Necessary for Rhythmic Motor Pattern ProductionStefan Clemens, and Paul S. Katz1 February 2003 | Journal of Neurophysiology, Vol. 89, No. 2Physiology and pathophysiology of cortico-basal ganglia–thalamocortical loops: Theoretical and practical aspectsProgress in Neuro-Psychopharmacology and Biological Psychiatry, Vol. 26, No. 4Hormonal Regulation of Neural and Behavioral Plasticity in InsectsRealistic Simulation of the Aplysia Siphon-Withdrawal Reflex Circuit: Roles of Circuit Elements in Producing Motor OutputJ. R. Lieb, and W. N. Frost1 March 1997 | Journal of Neurophysiology, Vol. 77, No. 3Sound localisation in cricketsJournal of Comparative Physiology A, Vol. 175, No. 4Computer simulation of the segmental neural network generating locomotion in lamprey by using populations of network interneuronsBiological Cybernetics, Vol. 68, No. 1Principles of organization of neural systems controlling automatic movements in animalsProgress in Neurobiology, Vol. 39, No. 1Recombination of motor pattern generatorsCurrent Biology, Vol. 1, No. 4Cerebral interneurons controlling fictive feeding in Limax maximusJournal of Comparative Physiology A, Vol. 166, No. 3Locomotion in the pulmonate snail Melampus—II. Recovery after pedal ganglion excisionComparative Biochemistry and Physiology Part A: Physiology, Vol. 96, No. 3Special cellular and synaptic mechanisms in motor pattern generationComparative Biochemistry and Physiology Part C: Comparative Pharmacology, Vol. 91, No. 1Structure predicts synaptic function of two classes of interneurons in the thoracic ganglia of Locusta migratoriaCell and Tissue Research, Vol. 250, No. 1Neuronal circuits controlling flight in the locust: central generation of the rhythmTrends in Neurosciences, Vol. 9Activation of NMDA receptors elecits fictive locomotion and bistable membrane properties in the lamprey spinal cordBrain Research, Vol. 336, No. 2 More from this issue > Volume 49Issue 4April 1983Pages 1017-1035 Copyright & PermissionsCopyright © 1983 the American Physiological Societyhttps://doi.org/10.1152/jn.1983.49.4.1017PubMed6854355History Published online 1 April 1983 Published in print 1 April 1983 Metrics

Interneurons involved in mediation and modulation of gill-withdrawal reflex in Aplysia. I. Identification and characterization.

Interneurons involved in mediation and modulation of gill-withdrawal reflex in Aplysia. I. Identification and characterization.R D Hawkins, V F Castellucci, and E R KandelR D Hawkins, V F Castellucci, and E R KandelPublished Online:01 Feb 1981https://doi.org/10.1152/jn.1981.45.2.304MoreSectionsPDF (2 MB)Download PDF ToolsExport citationAdd to favoritesGet permissionsTrack citations ShareShare onFacebookTwitterLinkedInWeChat Previous Back to Top Next Download PDF FiguresReferencesRelatedInformation Cited BySomatotopic organization and functional properties of mechanosensory neurons expressing sensorin-A mRNA in Aplysia californica20 February 2004 | Journal of Comparative Neurology, Vol. 471, No. 2Neural Circuit of Tail-Elicited Siphon Withdrawal in Aplysia. II. Role of Gated Inhibition in Differential Lateralization of Sensitization and DishabituationAdam S. Bristol, Stéphane Marinesco, and Thomas J. Carew1 February 2004 | Journal of Neurophysiology, Vol. 91, No. 2The use of elevated divalent cation solutions to isolate monosynaptic components of sensorimotor connections in AplysiaJournal of Neuroscience Methods, Vol. 120, No. 1Molecular Mechanisms Underlying a Unique Intermediate Phase of Memory in AplysiaNeuron, Vol. 31, No. 1Cognitive Neuroscience and the Study of MemoryNeuron, Vol. 20, No. 3Activity-Dependent Potentiation of Synaptic Transmission From L30 Inhibitory Interneurons of Aplysia Depends on Residual Presynaptic Ca2+ But Not on Postsynaptic Ca2+Thomas M. Fischer, Robert S. Zucker, and Thomas J. Carew1 October 1997 | Journal of Neurophysiology, Vol. 78, No. 4Realistic Simulation of the Aplysia Siphon-Withdrawal Reflex Circuit: Roles of Circuit Elements in Producing Motor OutputJ. R. Lieb, and W. N. Frost1 March 1997 | Journal of Neurophysiology, Vol. 77, No. 3Differential modulation of chemical and electrical components of mixed synapses in the lobster stomatogastric ganglionJournal of Comparative Physiology A, Vol. 175, No. 2New neural multiprocess memory model for adaptively regulating associative learningNeural Networks, Vol. 7, No. 9Inhibitory neuron produces heterosynaptic inhibition of the sensory-to-motor neuron synapse inAplysiaBrain Research, Vol. 577, No. 1Learning and memoryBrain Research Reviews, Vol. 16, No. 2Immunocytochemical study of the postnatal development of 5-HT-containing neurons and fibers in the cerebroid ganglia of Cryptomphalus aspersaInternational Journal of Developmental Neuroscience, Vol. 6, No. 4Development of plastic mechanisms related to learning at identified chemical synaptic connections in AplysiaNeuroscience, Vol. 17, No. 2Imunocytochemical localization and direct assays of serotonin-containing neurons in AplysiaNeuroscience, Vol. 11, No. 3Distribution of serotonin-immunoreactivity in juvenile AplysiaNeuroscience, Vol. 11, No. 2Heterosynaptic facilitation and behavioral sensitization are inhibited by lowering endogenous cAMP inAplysiaBrain Research, Vol. 288, No. 1-2Uptake of [3H]serotonin in the abdominal ganglion ofAplysia california. Further studies on the morphological and biochemical basis of presynaptic facilitationBrain Research, Vol. 272, No. 1Computational modelling of learning and behaviour in small neuronal systems More from this issue > Volume 45Issue 2February 1981Pages 304-14 https://doi.org/10.1152/jn.1981.45.2.304PubMed7463107History Published online 1 February 1981 Published in print 1 February 1981 Metrics

Neuronal correlates of siphon withdrawal in freely behaving Aplysia.

1. Central neuronal mechanisms of siphon withdrawal in Aplysia were studied for the first time in intact, freely behaving animals by means of population recordings from implanted whole-nerve cuff electrodes. Intracellular follow-up studies were then conducted when the same animal was reduced to a semi-intact preparation. 2. Background spontaneous activity in the siphon nerve consisted of low-frequency firing of a population of efferent units containing identified siphon motoneurons. 3. Spontaneous patterned bursts of efferent activity occurred irregularly and were associated with all-or-nothing contractions of the parapodia, gill, and siphon. Spontaneous bursts were due to centrally generated activity in the interneuron II (INT II) network, an oscillatory network with endogenous pacemaker properties. 4. In intact animals, even weak tactile stimuli to the siphon typically triggered an INTII burst shortly after the stimulus-locked efferent activity. Thus, the stimulus can phase-advance the INT II oscillator. In semi-intact preparations, short-latency INT II bursts were triggered less less frequently and required more intense stimuli. 5. With weak to moderate-intensity stimuli in intact animals, the presence of short-latency triggered INT II bursts largely determined the duration of the siphon component and amplitude of the gill component of the withdrawal reflex. 6. When stimuli were repeated over a range of interstimulus intervals (from 60 to 1 min), the likelihood of triggering a short-latency INT II burst die not change systematically. Thus, the ability of the siphon stimulus to stably entrain the all-or-none INT II component over a wide range of intervals will interact behaviorally with the decrement of the monosynaptic component of the reflex with repetition.

Receptive fields and response properties of mechanoreceptor neurons innervating siphon skin and mantle shelf in Aplysia.

Receptive fields and response properties of mechanoreceptor neurons innervating siphon skin and mantle shelf in Aplysia.J Byrne, V Castellucci, and E R KandelJ Byrne, V Castellucci, and E R KandelPublished Online:01 Sep 1974https://doi.org/10.1152/jn.1974.37.5.1041MoreSectionsPDF (4 MB)Download PDF ToolsExport citationAdd to favoritesGet permissionsTrack citations ShareShare onFacebookTwitterLinkedInWeChat Previous Back to Top Next Download PDF FiguresReferencesRelatedInformationCited ByMolecular Mechanisms of Memory Storage in AplysiaThe Biological Bulletin, Vol. 210, No. 3Analysis of 5-HT–Induced Short-Term Facilitation at Aplysia Sensorimotor Synapse During Bursts: Increased Synaptic Gain That Does Not Require ERK ActivationGregg A. Phares, and John H. Byrne1 July 2005 | Journal of Neurophysiology, Vol. 94, No. 1Somatotopic organization and functional properties of mechanosensory neurons expressing sensorin-A mRNA in Aplysia californica20 February 2004 | Journal of Comparative Neurology, Vol. 471, No. 2Parallel processing in an identified neural circuit: the Aplysia californica gill-withdrawal response model systemBiological Reviews, Vol. 79, No. 1Distribution of sensorin immunoreactivity in the central nervous system ofHelix pomatia: Functional aspects1 January 2003 | Journal of Neuroscience Research, Vol. 75, No. 1Complexities of a simple system: new lessons, old challenges and peripheral questions for the gill withdrawal reflex of AplysiaBrain Research Reviews, Vol. 43, No. 3Activity-Dependent Presynaptic Facilitation and Hebbian LTP Are Both Required and Interact during Classical Conditioning in AplysiaNeuron, Vol. 37, No. 1Temporal and spatial aspects of an environmental stimulus influence the dynamics of behavioral regulation of the Aplysia siphon-withdrawal response.1 January 2003 | Behavioral Neuroscience, Vol. 117, No. 3The use of elevated divalent cation solutions to isolate monosynaptic components of sensorimotor connections in AplysiaJournal of Neuroscience Methods, Vol. 120, No. 1Identification of Mechanoafferent Neurons in Terrestrial Snail: Response Properties and Synaptic ConnectionsAleksey Y. Malyshev, and Pavel M. Balaban1 May 2002 | Journal of Neurophysiology, Vol. 87, No. 5Distributed Motor Pattern Underlying Whole-Body Shortening in the Medicinal LeechIvan Arisi, Davide Zoccolan, and Vincent Torre1 November 2001 | Journal of Neurophysiology, Vol. 86, No. 5Diverse Synaptic Connections Between Peptidergic Radula Mechanoafferent Neurons and Neurons in the Feeding System ofAplysiaSteven C. Rosen, Mark W. Miller, Colin G. Evans, Elizabeth C. Cropper, and Irving Kupfermann1 March 2000 | Journal of Neurophysiology, Vol. 83, No. 3Realistic Simulation of the Aplysia Siphon-Withdrawal Reflex Circuit: Roles of Circuit Elements in Producing Motor OutputJ. R. Lieb, and W. N. Frost1 March 1997 | Journal of Neurophysiology, Vol. 77, No. 3cAMP induces long-term morphological changes in sensory neurons ofAplysiaBrain Research, Vol. 539, No. 2Serotonin acts in the synaptic region of sensory neruons in Aplysia to enhance transmitter releaseNeuroscience Letters, Vol. 104, No. 1-2A quantitative analysis of 2-D gels identifies proteins in which labeling is increased following long-term sensitization in AplysiaNeuron, Vol. 1, No. 4Mechanoreceptors in the oral tube and buccal mass of Philine apertaComparative Biochemistry and Physiology Part A: Physiology, Vol. 87, No. 1Post-tetanic potentiation inAplysia sensory neuronsBrain Research, Vol. 293, No. 2Uptake of [3H]serotonin in the abdominal ganglion ofAplysia california. Further studies on the morphological and biochemical basis of presynaptic facilitationBrain Research, Vol. 272, No. 1Methionine enkephalin increases CNS suppressive control exerted over gill reflex behaviours and associated neural activity in Aplysia californiaRegulatory Peptides, Vol. 3, No. 3-4The neuronal organisation of the paired pedal ganglia of Lymnaea stagnalis (L.)Comparative Biochemistry and Physiology Part A: Physiology, Vol. 69, No. 4Processing of chemosensory and mechanosensory information in identifiable Aplysia neuronsComparative Biochemistry and Physiology Part A: Physiology, Vol. 66, No. 1Two different and compatible intraneuronal labels for ultrastructural study of synaptically related cellsBrain Research, Vol. 173, No. 2Respiratory pumping: Neuronal control of a centrally commanded behavior in aplysiaBrain Research, Vol. 143, No. 1Further identification of neurons in the abdominal ganglion ofAplysia using behavioral criteriaBrain Research, Vol. 121, No. 1Dynamic properties of mechanoreceptor neurons mediating the defensive gill-withdrawal reflex inAplysiaBrain Research, Vol. 114, No. 1Tritonia swimming: triggering of a fixed action patternBrain Research, Vol. 96, No. 1 More from this issue > Volume 37Issue 5September 1974Pages 1041-64 https://doi.org/10.1152/jn.1974.37.5.1041PubMed4370315History Published online 1 September 1974 Published in print 1 September 1974 Metrics

A cholinergic mechanism of inhibitory synaptic transmission in a molluscan nervous system.

A cholinergic mechanism of inhibitory synaptic transmission in a molluscan nervous system.

INFLUENCE OF DISCHARGE OF MOTONEURONS UPON EXCITATION OF NEIGHBORING MOTONEURONS

INFLUENCE OF DISCHARGE OF MOTONEURONS UPON EXCITATION OF NEIGHBORING MOTONEURONS

ANALYSIS OF THE ACTIVITY OF THE CHAINS OF INTERNUNCIAL NEURONS

ANALYSIS OF THE ACTIVITY OF THE CHAINS OF INTERNUNCIAL NEURONS