Biological Bulletin Virtual Symposium: Marine Invertebrate Models of Learning and Memory
http://www.100md.com
《生物学报告》
1 McLean Hospital/Harvard University, 115 Mill Street, Belmont, Massachusetts 02478
2 Institute of Neurobiology and Department of Anatomy, University of Puerto Rico, 201 Blvd del Valle, San Juan, Puerto Rico 00901
Plato’s Symposium emphasized a two-tiered view of reality—the world of Being and the world of Becoming. While the world of Being is absolute and transcendent, the world of Becoming is always in movement, always changing. As reviewed in this Virtual Symposium, our present understanding of the neurobiological bases of learning and memory in marine invertebrate models reflects such a dichotomy. While common principles have emerged from the collective study of the models represented here, and many more that could not be included due to space limitations, the field retains a vital level of flux.
An appreciation for the extraordinary learning capabilities of invertebrates has a long history (Romanes, 1895; Jennings, 1906; Young, 1961; see Corning et al., 1973). About 40 years ago, neurobiologists began to exploit the advantageous properties of the nervous systems of certain higher invertebrates toward disclosing cellular mechanisms of behavioral plasticity (Kandel, 1970; Alkon, 1974; Davis and Gillette, 1978). These investigations established that several forms of learning could be explained in terms of neuronal, and specifically synaptic, plasticity. Thus, they paved the way for the intense study of synaptic mechanisms of learning and memory in the mammalian central nervous system that followed. Despite the extraordinary advances that have emerged from the study of long-term synaptic plasticity in the mammalian CNS, the invertebrate systems, with their relatively simple circuits and large identifiable neurons, still present superior opportunities to relate physiological mechanisms to the behavioral phenomena of learning (Krasne and Glanzman, 1995; Kandel, 2001).
We are pleased to have 14 contributions to this Virtual Symposium covering a variety of topics in learning and memory and encompassing a range of marine model systems. The articles reflect the latitude of the guidelines that were provided to participants. Contributors were asked to imagine a real symposium at a conference, organized with the purpose of encapsulating the current state of the field and stimulating further investigation. Such a symposium would consist of several keynote addresses reviewing entire research programs, as well as shorter presentations describing specific studies or even single experiments that could add to the overall objective. Throughout the symposium, individuals would have the opportunity to provide observations and commentary. Finally, participants were encouraged to consider their contributions in the overall historical context of the field and to suggest future directions.
The symposium begins with a comprehensive review of the temporal phases of memory in Aplysia by Hawkins, Kandel, and Bailey. This article highlights the complex signaling pathways that support these memory stages. It is followed by six primary reports that cover topics ranging from behavioral and electrophysiological substrates to molecular studies of signaling systems that produce learning-specific modifications. Adamo et al. examine a form of context-dependent learning in cuttlefish that occurs during an ecologically relevant task. They detail how the modification of body pattern by control of the chromatophore organs may be useful for studying cephalopod cognitive abilities. Kuzirian et al. contribute a paper on the enhancement of memory in Hermissenda by the protein kinase C (PKC) agonist bryostatin. Bryostatin is found to influence consolidation of memory in a dose-dependent manner, further supporting the importance of PKC in the Hermissenda learning model. A study of activity-dependent synaptic plasticity and metaplasticity in the Aplysia feeding central pattern generator is presented by Díaz-Ríos and Miller. The role of gamma-aminobutyric acid as a cotransmitter in this system is also examined. Another molluscan representative, Tritonia diomedea, is shown by Frost et al. to exhibit long-term habituation. This novel characterization adds to the repertoire of conditioning paradigms that can be studied in the Tritonia model system.
The final two primary reports focus on molecular substrates of learning and memory. The central importance of protein synthesis and axonal transport during Aplysia long-term synaptic facilitation is examined by Guan and Clark. In this paper, synapse-specific long-term facilitation in an in vitro conditioning paradigm is shown to require both central and peripheral protein synthesis as well as axonal transport. This article also considers how these observations impact our understanding of synaptic tagging. In the final primary paper of the symposium, Ha, Moroz, and colleagues detail the cloning, distribution, and phylogenetic analysis of an N-methyl-D-aspartate (NMDA) receptor in Aplysia. Because these receptors have a pivotal role in learning and memory in both vertebrates and invertebrates, the availability of a cloned NMDA receptor in this molluscan model should open many exciting new avenues for exploration.
Six review articles also cover topics ranging from neural circuits to intracellular signaling pathways. The contribution by Glanzman addresses the current state of the field of Aplysia learning. This article emphasizes the importance of postsynaptic contributions to learning-dependent modifications of synaptic strength. Romano and colleagues examine the signal transduction pathways activated by long-term memory consolidation during a context-signal associative-learning paradigm in the crab Chasmagnathus. This contribution includes a consideration of the role of amyloid precursor protein (APP) in memory storage in the crab and discusses the potential relevance of this model to understanding APP’s role in human neuropathological conditions.
Crow and Tian present a review of the circuits involved in Pavlovian conditioning in Hermissenda by examining the neural circuit of ciliary locomotion. This neural circuit is crucial because it is the site of convergence of the conditioned and unconditioned stimuli in this system. Manabu Sakakibara compares conditioning in Hermissenda and Lymnaea. Although the two systems exhibit some similarities, this paper reports several fundamental organizational differences between the marine and freshwater species. Hochner et al. give a fascinating overview of learning and memory in the octopus model system and detail a new in vitro slice preparation of the ventral lobe of the octopus brain. This preparation promises to permit in-depth studies of the neurophysiological correlates of learning in this classic model. The series of review articles concludes with a paper by Grant, Pant, and colleagues describing compartment-specific dynamic protein modification by phosphorylation and dephosphorylation. This paper uses the squid giant fiber to examine the differences in phosphorylation of key cytoskeletal proteins depending on their location in the neuron. A provocative discussion of the potential relevance of this model to neurodegenerative diseases is also presented. Finally, Elaine Bearer summarizes the DART symposium on learning and memory held at the Marine Biological Laboratory in August of 2006.
We once again enthusiastically thank all of the participants for their insightful and thought-provoking contributions to the first Biological Bulletin Virtual Symposium. Each article adds to a broad panorama that portrays the present status of the field of invertebrate learning and memory. We hope that this forum conveys the enduring value and relevance of these models and stimulates readers toward further exploration of their extraordinary promise.
Literature Cited
TOP
Literature Cited
Adamo, S. A., K. Ehgoetz, C. Sangster, and I. Whitehorne. 2006. Signaling to the enemy? Body pattern expression and its response to external cues during hunting in the cuttlefish Sepia officinalis (Cephalopoda). Biol. Bull.210:192–200.
Alkon, D. L. 1974. Associative training of Hermissenda. J. Gen. Physiol.64:70–84.
Bearer, E. L. 2006. Dart Symposium on Learning and Memory. Biol. Bull.210:334.
Corning, W. C., J. A. Dyal, and A. O. D. Willows, eds. 1973. Invertebrate Learning. Vols. 1–3. Plenum, New York.
Crow, T., and L.-M. Tian. 2006. Pavlovian conditioning in Hermissenda: a circuit analysis. Biol. Bull.210:289–297.
Davis, W. J., and R. Gillette. 1978. Neural correlate of behavioral plasticity in command neurons of Pleurobranchaea. Science199:801–804.
Díaz-Ríos, M., and M. W. Miller. 2006. Target-specific regulation of synaptic efficacy in the feeding central pattern generator of Aplysia: potential substrates for behavioral plasticity? Biol. Bull.210:215–229.
Frost, W. N., C. L. Brandon, and C. Van Zyl. 2006. Long-term habituation in the marine mollusc Tritonia diomedea. Biol. Bull.210:230–237.
Glanzman, D. L. 2006. The cellular mechanisms of learning in Aplysia: of blind men and elephants. Biol. Bull.210:271–279.
Grant, P., Y. Zheng, and H. C. Pant. 2006. Squid (Loligo pealei) giant fiber system: a model for studying neurodegeneration and dementia? Biol. Bull.210:318–333.
Guan, X., and G. A. Clark. 2006. Essential role of somatic and synaptic protein synthesis and axonal transport in long-term synapse-specific facilitation at distal sensorimotor connections in Aplysia. Biol. Bull.210:238–254.
Ha, T. J., A. B. Kohn, Y. V. Bobkova, and L. L. Moroz. 2006. Molecular characterization of NMDA-like receptors in Aplysia and Lymnaea: relevance to memory mechanisms. Biol. Bull.210:255–270.
Hawkins, R. D., E. R. Kandel, and C. H. Bailey. 2006. Molecular mechanisms of memory storage in Aplysia. Biol. Bull.210:174–191.
Hochner, B., T. Shomrat, and G. Fiorito. 2006. The octopus: a model for a comparative analysis of the evolution of learning and memory mechanisms. Biol. Bull.210:308–317.
Jennings, H. S. 1906. Behavior of the Lower Organisms. Columbia University Press, New York. 366 pp.
Kandel, E. R. 1970. Nerve cells and behavior. Sci. Amer.223:57–67.
Kandel, E. R. 2001. The molecular biology of memory storage: a dialogue between genes and synapses. Science294:1030–1038.
Krasne, F. B., and D. L. Glanzman. 1995. What we can learn from invertebrate learning. Annu. Rev. Psychol.46:585–624.
Kuzirian, A. M., H. T. Epstein, C. J. Gagliardi, T. J. Nelson, M. Sakakibara, C. Taylor, A. B. Scioletti, and D. L. Alkon. 2006. Bryostatin enhancement of memory in Hermissenda. Biol. Bull.210:201–214.
Romanes, G. J. 1895. Mental Evolution in Animals. Appleton, New York. 411 pp.
Romano, A., F. Locatelli, R. Freudenthal, E. Merlo, M. Feld, P. Ariel, D. Lemos, N. Federman, and M. Sol Fusti?ana. 2006. Lessons from a crab: molecular mechanisms in different memory phases of Chasmagnathus. Biol. Bull.210:280–288.
Sakakibara, M. 2006. Comparative study of visuo-vestibular conditioning in Lymnaea stagnalis. Biol. Bull.210:298–307.
Young, J. Z. 1961. Learning and discrimination in the octopus. Biol. Rev. Camb. Philos. Soc.36:32–96.(Donna L. McPhie1 and Mark)
2 Institute of Neurobiology and Department of Anatomy, University of Puerto Rico, 201 Blvd del Valle, San Juan, Puerto Rico 00901
Plato’s Symposium emphasized a two-tiered view of reality—the world of Being and the world of Becoming. While the world of Being is absolute and transcendent, the world of Becoming is always in movement, always changing. As reviewed in this Virtual Symposium, our present understanding of the neurobiological bases of learning and memory in marine invertebrate models reflects such a dichotomy. While common principles have emerged from the collective study of the models represented here, and many more that could not be included due to space limitations, the field retains a vital level of flux.
An appreciation for the extraordinary learning capabilities of invertebrates has a long history (Romanes, 1895; Jennings, 1906; Young, 1961; see Corning et al., 1973). About 40 years ago, neurobiologists began to exploit the advantageous properties of the nervous systems of certain higher invertebrates toward disclosing cellular mechanisms of behavioral plasticity (Kandel, 1970; Alkon, 1974; Davis and Gillette, 1978). These investigations established that several forms of learning could be explained in terms of neuronal, and specifically synaptic, plasticity. Thus, they paved the way for the intense study of synaptic mechanisms of learning and memory in the mammalian central nervous system that followed. Despite the extraordinary advances that have emerged from the study of long-term synaptic plasticity in the mammalian CNS, the invertebrate systems, with their relatively simple circuits and large identifiable neurons, still present superior opportunities to relate physiological mechanisms to the behavioral phenomena of learning (Krasne and Glanzman, 1995; Kandel, 2001).
We are pleased to have 14 contributions to this Virtual Symposium covering a variety of topics in learning and memory and encompassing a range of marine model systems. The articles reflect the latitude of the guidelines that were provided to participants. Contributors were asked to imagine a real symposium at a conference, organized with the purpose of encapsulating the current state of the field and stimulating further investigation. Such a symposium would consist of several keynote addresses reviewing entire research programs, as well as shorter presentations describing specific studies or even single experiments that could add to the overall objective. Throughout the symposium, individuals would have the opportunity to provide observations and commentary. Finally, participants were encouraged to consider their contributions in the overall historical context of the field and to suggest future directions.
The symposium begins with a comprehensive review of the temporal phases of memory in Aplysia by Hawkins, Kandel, and Bailey. This article highlights the complex signaling pathways that support these memory stages. It is followed by six primary reports that cover topics ranging from behavioral and electrophysiological substrates to molecular studies of signaling systems that produce learning-specific modifications. Adamo et al. examine a form of context-dependent learning in cuttlefish that occurs during an ecologically relevant task. They detail how the modification of body pattern by control of the chromatophore organs may be useful for studying cephalopod cognitive abilities. Kuzirian et al. contribute a paper on the enhancement of memory in Hermissenda by the protein kinase C (PKC) agonist bryostatin. Bryostatin is found to influence consolidation of memory in a dose-dependent manner, further supporting the importance of PKC in the Hermissenda learning model. A study of activity-dependent synaptic plasticity and metaplasticity in the Aplysia feeding central pattern generator is presented by Díaz-Ríos and Miller. The role of gamma-aminobutyric acid as a cotransmitter in this system is also examined. Another molluscan representative, Tritonia diomedea, is shown by Frost et al. to exhibit long-term habituation. This novel characterization adds to the repertoire of conditioning paradigms that can be studied in the Tritonia model system.
The final two primary reports focus on molecular substrates of learning and memory. The central importance of protein synthesis and axonal transport during Aplysia long-term synaptic facilitation is examined by Guan and Clark. In this paper, synapse-specific long-term facilitation in an in vitro conditioning paradigm is shown to require both central and peripheral protein synthesis as well as axonal transport. This article also considers how these observations impact our understanding of synaptic tagging. In the final primary paper of the symposium, Ha, Moroz, and colleagues detail the cloning, distribution, and phylogenetic analysis of an N-methyl-D-aspartate (NMDA) receptor in Aplysia. Because these receptors have a pivotal role in learning and memory in both vertebrates and invertebrates, the availability of a cloned NMDA receptor in this molluscan model should open many exciting new avenues for exploration.
Six review articles also cover topics ranging from neural circuits to intracellular signaling pathways. The contribution by Glanzman addresses the current state of the field of Aplysia learning. This article emphasizes the importance of postsynaptic contributions to learning-dependent modifications of synaptic strength. Romano and colleagues examine the signal transduction pathways activated by long-term memory consolidation during a context-signal associative-learning paradigm in the crab Chasmagnathus. This contribution includes a consideration of the role of amyloid precursor protein (APP) in memory storage in the crab and discusses the potential relevance of this model to understanding APP’s role in human neuropathological conditions.
Crow and Tian present a review of the circuits involved in Pavlovian conditioning in Hermissenda by examining the neural circuit of ciliary locomotion. This neural circuit is crucial because it is the site of convergence of the conditioned and unconditioned stimuli in this system. Manabu Sakakibara compares conditioning in Hermissenda and Lymnaea. Although the two systems exhibit some similarities, this paper reports several fundamental organizational differences between the marine and freshwater species. Hochner et al. give a fascinating overview of learning and memory in the octopus model system and detail a new in vitro slice preparation of the ventral lobe of the octopus brain. This preparation promises to permit in-depth studies of the neurophysiological correlates of learning in this classic model. The series of review articles concludes with a paper by Grant, Pant, and colleagues describing compartment-specific dynamic protein modification by phosphorylation and dephosphorylation. This paper uses the squid giant fiber to examine the differences in phosphorylation of key cytoskeletal proteins depending on their location in the neuron. A provocative discussion of the potential relevance of this model to neurodegenerative diseases is also presented. Finally, Elaine Bearer summarizes the DART symposium on learning and memory held at the Marine Biological Laboratory in August of 2006.
We once again enthusiastically thank all of the participants for their insightful and thought-provoking contributions to the first Biological Bulletin Virtual Symposium. Each article adds to a broad panorama that portrays the present status of the field of invertebrate learning and memory. We hope that this forum conveys the enduring value and relevance of these models and stimulates readers toward further exploration of their extraordinary promise.
Literature Cited
TOP
Literature Cited
Adamo, S. A., K. Ehgoetz, C. Sangster, and I. Whitehorne. 2006. Signaling to the enemy? Body pattern expression and its response to external cues during hunting in the cuttlefish Sepia officinalis (Cephalopoda). Biol. Bull.210:192–200.
Alkon, D. L. 1974. Associative training of Hermissenda. J. Gen. Physiol.64:70–84.
Bearer, E. L. 2006. Dart Symposium on Learning and Memory. Biol. Bull.210:334.
Corning, W. C., J. A. Dyal, and A. O. D. Willows, eds. 1973. Invertebrate Learning. Vols. 1–3. Plenum, New York.
Crow, T., and L.-M. Tian. 2006. Pavlovian conditioning in Hermissenda: a circuit analysis. Biol. Bull.210:289–297.
Davis, W. J., and R. Gillette. 1978. Neural correlate of behavioral plasticity in command neurons of Pleurobranchaea. Science199:801–804.
Díaz-Ríos, M., and M. W. Miller. 2006. Target-specific regulation of synaptic efficacy in the feeding central pattern generator of Aplysia: potential substrates for behavioral plasticity? Biol. Bull.210:215–229.
Frost, W. N., C. L. Brandon, and C. Van Zyl. 2006. Long-term habituation in the marine mollusc Tritonia diomedea. Biol. Bull.210:230–237.
Glanzman, D. L. 2006. The cellular mechanisms of learning in Aplysia: of blind men and elephants. Biol. Bull.210:271–279.
Grant, P., Y. Zheng, and H. C. Pant. 2006. Squid (Loligo pealei) giant fiber system: a model for studying neurodegeneration and dementia? Biol. Bull.210:318–333.
Guan, X., and G. A. Clark. 2006. Essential role of somatic and synaptic protein synthesis and axonal transport in long-term synapse-specific facilitation at distal sensorimotor connections in Aplysia. Biol. Bull.210:238–254.
Ha, T. J., A. B. Kohn, Y. V. Bobkova, and L. L. Moroz. 2006. Molecular characterization of NMDA-like receptors in Aplysia and Lymnaea: relevance to memory mechanisms. Biol. Bull.210:255–270.
Hawkins, R. D., E. R. Kandel, and C. H. Bailey. 2006. Molecular mechanisms of memory storage in Aplysia. Biol. Bull.210:174–191.
Hochner, B., T. Shomrat, and G. Fiorito. 2006. The octopus: a model for a comparative analysis of the evolution of learning and memory mechanisms. Biol. Bull.210:308–317.
Jennings, H. S. 1906. Behavior of the Lower Organisms. Columbia University Press, New York. 366 pp.
Kandel, E. R. 1970. Nerve cells and behavior. Sci. Amer.223:57–67.
Kandel, E. R. 2001. The molecular biology of memory storage: a dialogue between genes and synapses. Science294:1030–1038.
Krasne, F. B., and D. L. Glanzman. 1995. What we can learn from invertebrate learning. Annu. Rev. Psychol.46:585–624.
Kuzirian, A. M., H. T. Epstein, C. J. Gagliardi, T. J. Nelson, M. Sakakibara, C. Taylor, A. B. Scioletti, and D. L. Alkon. 2006. Bryostatin enhancement of memory in Hermissenda. Biol. Bull.210:201–214.
Romanes, G. J. 1895. Mental Evolution in Animals. Appleton, New York. 411 pp.
Romano, A., F. Locatelli, R. Freudenthal, E. Merlo, M. Feld, P. Ariel, D. Lemos, N. Federman, and M. Sol Fusti?ana. 2006. Lessons from a crab: molecular mechanisms in different memory phases of Chasmagnathus. Biol. Bull.210:280–288.
Sakakibara, M. 2006. Comparative study of visuo-vestibular conditioning in Lymnaea stagnalis. Biol. Bull.210:298–307.
Young, J. Z. 1961. Learning and discrimination in the octopus. Biol. Rev. Camb. Philos. Soc.36:32–96.(Donna L. McPhie1 and Mark)