DOI: 10.1126/science.8211146. Long-Term Synaptic Facilitation in the Absence of Short-Term Facilitation in <i>Aplysia</i> Neurons

Long-Term Synaptic Facilitation in the Absence of Short-Term Facilitation in Aplysia Neurons

10.1126/science.8211146

Crossref journal-article

American Association for the Advancement of Science (AAAS)

Science (221)

Abstract

Serotonin (5-HT) induces both short-term and long-term facilitation of the identified synaptic connections between sensory and motor neurons of Aplysia . Three independent experimental approaches showed that long-term facilitation can normally be expressed in the absence of short-term facilitation: (i) The 5-HT antagonist cyproheptadine blocked the induction of short-term but not long-term facilitation; (ii) concentrations of 5-HT below threshold for the induction of short-term facilitation nonetheless induced long-term facilitation; and (iii) localized application of 5-HT to the sensory neuron cell body and proximal synapses induced long-term facilitation in distal synapses that were not exposed to 5-HT and had not expressed short-term facilitation. These results suggest that short-term and long-term synaptic facilitation are induced in parallel in the sensory neurons and that the short-term process, because it is induced and expressed at the synapse, can occur locally, but the long-term process, because of its dependence on a nuclear signal, is expressed throughout the neuron.

Bibliography

Emptage, N. J., & Carew, T. J. (1993). Long-Term Synaptic Facilitation in the Absence of Short-Term Facilitation in Aplysia Neurons. Science, 262(5131), 253â256.

Authors 2

Nigel J. Emptage (first)
Thomas J. Carew (additional)

References 40 Referenced 158

Atkinson, R. C., Psychology of Learning and Motivation: Advances in Research and Theory 2: 89 (1968). (10.1016/S0079-7421(08)60422-3) / Psychology of Learning and Motivation: Advances in Research and Theory (1968)
BADDELEY, A.D., AMNESIA AND DISTINCTION BETWEEN LONG-AND SHORT-TERM MEMORY, JOURNAL OF VERBAL LEARNING AND VERBAL BEHAVIOR 9: 176 (1970). (10.1016/S0022-5371(70)80048-2) / JOURNAL OF VERBAL LEARNING AND VERBAL BEHAVIOR (1970)
BAILEY, C.H., MORPHOLOGICAL ASPECTS OF SYNAPTIC PLASTICITY IN APLYSIA - AN ANATOMICAL SUBSTRATE FOR LONG-TERM-MEMORY, ANNALS OF THE NEW YORK ACADEMY OF SCIENCES 627: 181 (1991). (10.1111/j.1749-6632.1991.tb25924.x) / ANNALS OF THE NEW YORK ACADEMY OF SCIENCES (1991)
BAILEY, C.H., TIME COURSE OF STRUCTURAL-CHANGES AT IDENTIFIED SENSORY NEURON SYNAPSES DURING LONG-TERM SENSITIZATION IN APLYSIA, JOURNAL OF NEUROSCIENCE 9: 1774 (1989). (10.1523/JNEUROSCI.09-05-01774.1989) / JOURNAL OF NEUROSCIENCE (1989)
BAXTER, D.A., SEROTONERGIC MODULATION OF 2 POTASSIUM CURRENTS IN THE PLEURAL SENSORY NEURONS OF APLYSIA, JOURNAL OF NEUROPHYSIOLOGY 62: 665 (1989). (10.1152/jn.1989.62.3.665) / JOURNAL OF NEUROPHYSIOLOGY (1989)
BAXTER, D.A., DIFFERENTIAL-EFFECTS OF CAMP AND SEROTONIN ON MEMBRANE CURRENT, ACTION-POTENTIAL DURATION, AND EXCITABILITY IN SOMATA OF PLEURAL SENSORY NEURONS OF APLYSIA, JOURNAL OF NEUROPHYSIOLOGY 64: 978 (1990). (10.1152/jn.1990.64.3.978) / JOURNAL OF NEUROPHYSIOLOGY (1990)
BUONOMANO, D.V., LONG-TERM SYNAPTIC CHANGES PRODUCED BY A CELLULAR ANALOG OF CLASSICAL-CONDITIONING IN APLYSIA, SCIENCE 249: 420 (1990). (10.1126/science.2165631) / SCIENCE (1990)
BYRNE, J.H., ROLES OF 2ND MESSENGER PATHWAYS IN NEURONAL PLASTICITY AND IN LEARNING AND MEMORY - INSIGHTS GAINED FROM APLYSIA, ADVANCES IN SECOND MESSENGER AND PHOSPHOPROTEIN RESEARCH 27: 47 (1993). / ADVANCES IN SECOND MESSENGER AND PHOSPHOPROTEIN RESEARCH (1993)
Carew, T. J., Annu. Rev. Neurosci. 9: 435 (1986). (10.1146/annurev.ne.09.030186.002251) / Annu. Rev. Neurosci. (1986)
Clark, G. A., Proceedings of the National Academy of Sciences of the United States of America 81: 2577 (1984). / Proceedings of the National Academy of Sciences of the United States of America (1984)
CLARK, G.A., SOC NEUR ABSTR 13: 390 (1987). / SOC NEUR ABSTR (1987)
CLEARY, L, SOC NEUR ABSTR 11: 692 (1985). / SOC NEUR ABSTR (1985)
CROW, T, DOWN-REGULATION OF PROTEIN-KINASE-C AND KINASE INHIBITORS DISSOCIATE SHORT-TERM AND LONG-TERM ENHANCEMENT PRODUCED BY ONE-TRIAL CONDITIONING OF HERMISSENDA, JOURNAL OF NEUROPHYSIOLOGY 69: 636 (1993). (10.1152/jn.1993.69.2.636) / JOURNAL OF NEUROPHYSIOLOGY (1993)
DALE, N, SEROTONIN PRODUCES LONG-TERM CHANGES IN THE EXCITABILITY OF APLYSIA SENSORY NEURONS IN CULTURE THAT DEPEND ON NEW PROTEIN-SYNTHESIS, JOURNAL OF NEUROSCIENCE 7: 2232 (1987). (10.1523/JNEUROSCI.07-07-02232.1987) / JOURNAL OF NEUROSCIENCE (1987)
10.1038/345718a0
EMPTAGE N unpublished data.
EMPTAGE N.J. unpublished data.
GHIRARDI, M, ROLES OF PKA AND PKC IN FACILITATION OF EVOKED AND SPONTANEOUS TRANSMITTER RELEASE AT DEPRESSED AND NONDEPRESSED SYNAPSES IN APLYSIA SENSORY NEURONS, NEURON 9: 479 (1992). (10.1016/0896-6273(92)90185-G) / NEURON (1992)
GOLDSMITH, B.A., CAMP MODULATES MULTIPLE K+ CURRENTS, INCREASING SPIKE DURATION AND EXCITABILITY IN APLYSIA SENSORY NEURONS, PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 89: 11481 (1992). / PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA (1992)
HAMMER, M, SEROTONIN ACTS IN THE SYNAPTIC REGION OF SENSORY NEURONS IN APLYSIA TO ENHANCE TRANSMITTER RELEASE, NEUROSCIENCE LETTERS 104: 235 (1989). (10.1016/0304-3940(89)90360-1) / NEUROSCIENCE LETTERS (1989)
Hawkins, R. D., Psychological Review 91: 375 (1984). (10.1037/0033-295X.91.3.375) / Psychological Review (1984)
Hebb D. O. Organization of Behavior (1949).
HOCHNER, B, MODULATION OF A TRANSIENT K+ CURRENT IN THE PLEURAL SENSORY NEURONS OF APLYSIA BY SEROTONIN AND CAMP - IMPLICATIONS FOR SPIKE BROADENING, PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 89: 11476 (1992). / PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA (1992)
James W. Principles of Psychology (1890). (10.1037/10538-000)
MERCER, A.R., PHARMACOLOGICAL DISSOCIATION OF MODULATORY EFFECTS OF SEROTONIN IN APLYSIA SENSORY NEURONS, SCIENCE 254: 1811 (1991). (10.1126/science.1662413) / SCIENCE (1991)
10.1126/science.3775383
NAZIF, F.A., CAMP INDUCES LONG-TERM MORPHOLOGICAL-CHANGES IN SENSORY NEURONS OF APLYSIA, BRAIN RESEARCH 539: 324 (1991). (10.1016/0006-8993(91)91638-H) / BRAIN RESEARCH (1991)
OCORR, K.A., ASSOCIATIVE CONDITIONING ANALOG SELECTIVELY INCREASES CAMP LEVELS OF TAIL SENSORY NEURONS IN APLYSIA, PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 82: 2548 (1985). / PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA (1985)
10.1126/science.2454509
10.1126/science.2433766
10.1126/science.2837826
Schwartz, J. H., Journal of Neuroscience 1: 606 (1981). (10.1523/JNEUROSCI.01-06-00606.1981) / Journal of Neuroscience (1981)
SHALLICE, T, QUARTERLY JOURNAL OF EXPERIMENTAL PSYCHOLOGY 22: 261 (1970). (10.1080/00335557043000203) / QUARTERLY JOURNAL OF EXPERIMENTAL PSYCHOLOGY (1970)
SQUIRE, L.R., THE STRUCTURE AND ORGANIZATION OF MEMORY, ANNUAL REVIEW OF PSYCHOLOGY 44: 453 (1993). (10.1146/annurev.ps.44.020193.002321) / ANNUAL REVIEW OF PSYCHOLOGY (1993)
Squire L. R. Memory and Brain (1987). (10.1016/B978-0-12-268330-5.50013-5)
STARK L.L. unpublished data.
SUGITA, S, INVOLVEMENT OF PROTEIN-KINASE-C IN SEROTONIN-INDUCED SPIKE BROADENING AND SYNAPTIC FACILITATION IN SENSORIMOTOR CONNECTIONS OF APLYSIA, JOURNAL OF NEUROPHYSIOLOGY 68: 643 (1992). (10.1152/jn.1992.68.2.643) / JOURNAL OF NEUROPHYSIOLOGY (1992)
WALTERS, E.T., MECHANOAFFERENT NEURONS INNERVATING TAIL OF APLYSIA .2. MODULATION BY SENSITIZING STIMULATION, JOURNAL OF NEUROPHYSIOLOGY 50: 1543 (1983). (10.1152/jn.1983.50.6.1543) / JOURNAL OF NEUROPHYSIOLOGY (1983)
WALTERS, E.T., MULTIPLE SENSORY NEURONAL CORRELATES OF SITE-SPECIFIC SENSITIZATION IN APLYSIA, JOURNAL OF NEUROSCIENCE 7: 408 (1987). (10.1523/JNEUROSCI.07-02-00408.1987) / JOURNAL OF NEUROSCIENCE (1987)
ZHANG, Z.S., SEROTONINERGIC VARICOSITIES MAKE SYNAPTIC CONTACTS WITH PLEURAL SENSORY NEURONS OF APLYSIA, JOURNAL OF COMPARATIVE NEUROLOGY 311: 259 (1991). (10.1002/cne.903110207) / JOURNAL OF COMPARATIVE NEUROLOGY (1991)

Dates

Type	When
Created	18 years, 10 months ago (Oct. 5, 2006, 7:05 p.m.)
Deposited	1 year, 7 months ago (Jan. 15, 2024, 5:42 a.m.)
Indexed	1 month, 2 weeks ago (July 6, 2025, 1:44 p.m.)
Issued	31 years, 10 months ago (Oct. 8, 1993)
Published	31 years, 10 months ago (Oct. 8, 1993)
Published Print	31 years, 10 months ago (Oct. 8, 1993)

Funders 0

None

BibTeX

@article{Emptage_1993, title={Long-Term Synaptic Facilitation in the Absence of Short-Term Facilitation in Aplysia Neurons}, volume={262}, ISSN={1095-9203}, url={http://dx.doi.org/10.1126/science.8211146}, DOI={10.1126/science.8211146}, number={5131}, journal={Science}, publisher={American Association for the Advancement of Science (AAAS)}, author={Emptage, Nigel J. and Carew, Thomas J.}, year={1993}, month=oct, pages={253–256} }

JSON

{
  "indexed": {
    "date-parts": [
      [
        2025,
        7,
        6
      ]
    ],
    "date-time": "2025-07-06T17:44:47Z",
    "timestamp": 1751823887251
  },
  "reference-count": 40,
  "publisher": "American Association for the Advancement of Science (AAAS)",
  "issue": "5131",
  "content-domain": {
    "domain": [],
    "crossmark-restriction": false
  },
  "published-print": {
    "date-parts": [
      [
        1993,
        10,
        8
      ]
    ]
  },
  "abstract": "<jats:p>\n            Serotonin (5-HT) induces both short-term and long-term facilitation of the identified synaptic connections between sensory and motor neurons of\n            <jats:italic>Aplysia</jats:italic>\n            . Three independent experimental approaches showed that long-term facilitation can normally be expressed in the absence of short-term facilitation: (i) The 5-HT antagonist cyproheptadine blocked the induction of short-term but not long-term facilitation; (ii) concentrations of 5-HT below threshold for the induction of short-term facilitation nonetheless induced long-term facilitation; and (iii) localized application of 5-HT to the sensory neuron cell body and proximal synapses induced long-term facilitation in distal synapses that were not exposed to 5-HT and had not expressed short-term facilitation. These results suggest that short-term and long-term synaptic facilitation are induced in parallel in the sensory neurons and that the short-term process, because it is induced and expressed at the synapse, can occur locally, but the long-term process, because of its dependence on a nuclear signal, is expressed throughout the neuron.\n          </jats:p>",
  "DOI": "10.1126/science.8211146",
  "type": "journal-article",
  "created": {
    "date-parts": [
      [
        2006,
        10,
        5
      ]
    ],
    "date-time": "2006-10-05T23:05:09Z",
    "timestamp": 1160089509000
  },
  "page": "253-256",
  "source": "Crossref",
  "is-referenced-by-count": 158,
  "title": "Long-Term Synaptic Facilitation in the Absence of Short-Term Facilitation in\n            <i>Aplysia</i>\n            Neurons",
  "prefix": "10.1126",
  "volume": "262",
  "author": [
    {
      "given": "Nigel J.",
      "family": "Emptage",
      "sequence": "first",
      "affiliation": [
        {
          "name": "Departments of Psychology and Biology, Yale University, New Haven, CT 06520."
        }
      ]
    },
    {
      "given": "Thomas J.",
      "family": "Carew",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Departments of Psychology and Biology, Yale University, New Haven, CT 06520."
        }
      ]
    }
  ],
  "member": "221",
  "reference": [
    {
      "key": "e_1_2_1_1_1",
      "doi-asserted-by": "crossref",
      "first-page": "89",
      "DOI": "10.1016/S0079-7421(08)60422-3",
      "volume": "2",
      "year": "1968",
      "unstructured": "Atkinson, R. C., Psychology of Learning and Motivation: Advances in Research and Theory 2: 89 (1968).",
      "journal-title": "Psychology of Learning and Motivation: Advances in Research and Theory"
    },
    {
      "key": "e_1_2_1_2_1",
      "doi-asserted-by": "crossref",
      "first-page": "176",
      "DOI": "10.1016/S0022-5371(70)80048-2",
      "volume": "9",
      "year": "1970",
      "unstructured": "BADDELEY, A.D., AMNESIA AND DISTINCTION BETWEEN LONG-AND SHORT-TERM MEMORY, JOURNAL OF VERBAL LEARNING AND VERBAL BEHAVIOR 9: 176 (1970).",
      "journal-title": "JOURNAL OF VERBAL LEARNING AND VERBAL BEHAVIOR"
    },
    {
      "key": "e_1_2_1_3_1",
      "doi-asserted-by": "crossref",
      "first-page": "181",
      "DOI": "10.1111/j.1749-6632.1991.tb25924.x",
      "volume": "627",
      "year": "1991",
      "unstructured": "BAILEY, C.H., MORPHOLOGICAL ASPECTS OF SYNAPTIC PLASTICITY IN APLYSIA - AN ANATOMICAL SUBSTRATE FOR LONG-TERM-MEMORY, ANNALS OF THE NEW YORK ACADEMY OF SCIENCES 627: 181 (1991).",
      "journal-title": "ANNALS OF THE NEW YORK ACADEMY OF SCIENCES"
    },
    {
      "key": "e_1_2_1_4_1",
      "doi-asserted-by": "crossref",
      "first-page": "1774",
      "DOI": "10.1523/JNEUROSCI.09-05-01774.1989",
      "volume": "9",
      "year": "1989",
      "unstructured": "BAILEY, C.H., TIME COURSE OF STRUCTURAL-CHANGES AT IDENTIFIED SENSORY NEURON SYNAPSES DURING LONG-TERM SENSITIZATION IN APLYSIA, JOURNAL OF NEUROSCIENCE 9: 1774 (1989).",
      "journal-title": "JOURNAL OF NEUROSCIENCE"
    },
    {
      "key": "e_1_2_1_5_1",
      "doi-asserted-by": "crossref",
      "first-page": "665",
      "DOI": "10.1152/jn.1989.62.3.665",
      "volume": "62",
      "year": "1989",
      "unstructured": "BAXTER, D.A., SEROTONERGIC MODULATION OF 2 POTASSIUM CURRENTS IN THE PLEURAL SENSORY NEURONS OF APLYSIA, JOURNAL OF NEUROPHYSIOLOGY 62: 665 (1989).",
      "journal-title": "JOURNAL OF NEUROPHYSIOLOGY"
    },
    {
      "key": "e_1_2_1_6_1",
      "doi-asserted-by": "crossref",
      "first-page": "978",
      "DOI": "10.1152/jn.1990.64.3.978",
      "volume": "64",
      "year": "1990",
      "unstructured": "BAXTER, D.A., DIFFERENTIAL-EFFECTS OF CAMP AND SEROTONIN ON MEMBRANE CURRENT, ACTION-POTENTIAL DURATION, AND EXCITABILITY IN SOMATA OF PLEURAL SENSORY NEURONS OF APLYSIA, JOURNAL OF NEUROPHYSIOLOGY 64: 978 (1990).",
      "journal-title": "JOURNAL OF NEUROPHYSIOLOGY"
    },
    {
      "key": "e_1_2_1_7_1",
      "doi-asserted-by": "crossref",
      "first-page": "420",
      "DOI": "10.1126/science.2165631",
      "volume": "249",
      "year": "1990",
      "unstructured": "BUONOMANO, D.V., LONG-TERM SYNAPTIC CHANGES PRODUCED BY A CELLULAR ANALOG OF CLASSICAL-CONDITIONING IN APLYSIA, SCIENCE 249: 420 (1990).",
      "journal-title": "SCIENCE"
    },
    {
      "key": "e_1_2_1_8_1",
      "first-page": "47",
      "volume": "27",
      "year": "1993",
      "unstructured": "BYRNE, J.H., ROLES OF 2ND MESSENGER PATHWAYS IN NEURONAL PLASTICITY AND IN LEARNING AND MEMORY - INSIGHTS GAINED FROM APLYSIA, ADVANCES IN SECOND MESSENGER AND PHOSPHOPROTEIN RESEARCH 27: 47 (1993).",
      "journal-title": "ADVANCES IN SECOND MESSENGER AND PHOSPHOPROTEIN RESEARCH"
    },
    {
      "key": "e_1_2_1_9_1",
      "doi-asserted-by": "crossref",
      "first-page": "435",
      "DOI": "10.1146/annurev.ne.09.030186.002251",
      "volume": "9",
      "year": "1986",
      "unstructured": "Carew, T. J., Annu. Rev. Neurosci. 9: 435 (1986).",
      "journal-title": "Annu. Rev. Neurosci."
    },
    {
      "key": "e_1_2_1_10_1",
      "first-page": "2577",
      "volume": "81",
      "year": "1984",
      "unstructured": "Clark, G. A., Proceedings of the National Academy of Sciences of the United States of America 81: 2577 (1984).",
      "journal-title": "Proceedings of the National Academy of Sciences of the United States of America"
    },
    {
      "key": "e_1_2_1_11_1",
      "first-page": "390",
      "volume": "13",
      "year": "1987",
      "unstructured": "CLARK, G.A., SOC NEUR ABSTR 13: 390 (1987).",
      "journal-title": "SOC NEUR ABSTR"
    },
    {
      "key": "e_1_2_1_12_1",
      "first-page": "692",
      "volume": "11",
      "year": "1985",
      "unstructured": "CLEARY, L, SOC NEUR ABSTR 11: 692 (1985).",
      "journal-title": "SOC NEUR ABSTR"
    },
    {
      "key": "e_1_2_1_13_1",
      "doi-asserted-by": "crossref",
      "first-page": "636",
      "DOI": "10.1152/jn.1993.69.2.636",
      "volume": "69",
      "year": "1993",
      "unstructured": "CROW, T, DOWN-REGULATION OF PROTEIN-KINASE-C AND KINASE INHIBITORS DISSOCIATE SHORT-TERM AND LONG-TERM ENHANCEMENT PRODUCED BY ONE-TRIAL CONDITIONING OF HERMISSENDA, JOURNAL OF NEUROPHYSIOLOGY 69: 636 (1993).",
      "journal-title": "JOURNAL OF NEUROPHYSIOLOGY"
    },
    {
      "key": "e_1_2_1_14_1",
      "doi-asserted-by": "crossref",
      "first-page": "2232",
      "DOI": "10.1523/JNEUROSCI.07-07-02232.1987",
      "volume": "7",
      "year": "1987",
      "unstructured": "DALE, N, SEROTONIN PRODUCES LONG-TERM CHANGES IN THE EXCITABILITY OF APLYSIA SENSORY NEURONS IN CULTURE THAT DEPEND ON NEW PROTEIN-SYNTHESIS, JOURNAL OF NEUROSCIENCE 7: 2232 (1987).",
      "journal-title": "JOURNAL OF NEUROSCIENCE"
    },
    {
      "key": "e_1_2_1_15_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/345718a0"
    },
    {
      "key": "e_1_2_1_16_1",
      "unstructured": "EMPTAGE N unpublished data."
    },
    {
      "key": "e_1_2_1_17_1",
      "unstructured": "EMPTAGE N.J. unpublished data."
    },
    {
      "key": "e_1_2_1_18_1",
      "doi-asserted-by": "crossref",
      "first-page": "479",
      "DOI": "10.1016/0896-6273(92)90185-G",
      "volume": "9",
      "year": "1992",
      "unstructured": "GHIRARDI, M, ROLES OF PKA AND PKC IN FACILITATION OF EVOKED AND SPONTANEOUS TRANSMITTER RELEASE AT DEPRESSED AND NONDEPRESSED SYNAPSES IN APLYSIA SENSORY NEURONS, NEURON 9: 479 (1992).",
      "journal-title": "NEURON"
    },
    {
      "key": "e_1_2_1_19_1",
      "first-page": "11481",
      "volume": "89",
      "year": "1992",
      "unstructured": "GOLDSMITH, B.A., CAMP MODULATES MULTIPLE K+ CURRENTS, INCREASING SPIKE DURATION AND EXCITABILITY IN APLYSIA SENSORY NEURONS, PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 89: 11481 (1992).",
      "journal-title": "PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA"
    },
    {
      "key": "e_1_2_1_20_1",
      "doi-asserted-by": "crossref",
      "first-page": "235",
      "DOI": "10.1016/0304-3940(89)90360-1",
      "volume": "104",
      "year": "1989",
      "unstructured": "HAMMER, M, SEROTONIN ACTS IN THE SYNAPTIC REGION OF SENSORY NEURONS IN APLYSIA TO ENHANCE TRANSMITTER RELEASE, NEUROSCIENCE LETTERS 104: 235 (1989).",
      "journal-title": "NEUROSCIENCE LETTERS"
    },
    {
      "key": "e_1_2_1_21_1",
      "doi-asserted-by": "crossref",
      "first-page": "375",
      "DOI": "10.1037/0033-295X.91.3.375",
      "volume": "91",
      "year": "1984",
      "unstructured": "Hawkins, R. D., Psychological Review 91: 375 (1984).",
      "journal-title": "Psychological Review"
    },
    {
      "key": "e_1_2_1_22_1",
      "unstructured": "Hebb D. O. Organization of Behavior (1949)."
    },
    {
      "key": "e_1_2_1_23_1",
      "first-page": "11476",
      "volume": "89",
      "year": "1992",
      "unstructured": "HOCHNER, B, MODULATION OF A TRANSIENT K+ CURRENT IN THE PLEURAL SENSORY NEURONS OF APLYSIA BY SEROTONIN AND CAMP - IMPLICATIONS FOR SPIKE BROADENING, PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 89: 11476 (1992).",
      "journal-title": "PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA"
    },
    {
      "key": "e_1_2_1_24_1",
      "doi-asserted-by": "crossref",
      "unstructured": "James W. Principles of Psychology (1890).",
      "DOI": "10.1037/10538-000"
    },
    {
      "key": "e_1_2_1_25_1",
      "doi-asserted-by": "crossref",
      "first-page": "1811",
      "DOI": "10.1126/science.1662413",
      "volume": "254",
      "year": "1991",
      "unstructured": "MERCER, A.R., PHARMACOLOGICAL DISSOCIATION OF MODULATORY EFFECTS OF SEROTONIN IN APLYSIA SENSORY NEURONS, SCIENCE 254: 1811 (1991).",
      "journal-title": "SCIENCE"
    },
    {
      "key": "e_1_2_1_26_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1126/science.3775383"
    },
    {
      "key": "e_1_2_1_27_1",
      "doi-asserted-by": "crossref",
      "first-page": "324",
      "DOI": "10.1016/0006-8993(91)91638-H",
      "volume": "539",
      "year": "1991",
      "unstructured": "NAZIF, F.A., CAMP INDUCES LONG-TERM MORPHOLOGICAL-CHANGES IN SENSORY NEURONS OF APLYSIA, BRAIN RESEARCH 539: 324 (1991).",
      "journal-title": "BRAIN RESEARCH"
    },
    {
      "key": "e_1_2_1_28_1",
      "first-page": "2548",
      "volume": "82",
      "year": "1985",
      "unstructured": "OCORR, K.A., ASSOCIATIVE CONDITIONING ANALOG SELECTIVELY INCREASES CAMP LEVELS OF TAIL SENSORY NEURONS IN APLYSIA, PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 82: 2548 (1985).",
      "journal-title": "PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA"
    },
    {
      "key": "e_1_2_1_29_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1126/science.2454509"
    },
    {
      "key": "e_1_2_1_30_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1126/science.2433766"
    },
    {
      "key": "e_1_2_1_31_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1126/science.2837826"
    },
    {
      "key": "e_1_2_1_32_1",
      "doi-asserted-by": "crossref",
      "first-page": "606",
      "DOI": "10.1523/JNEUROSCI.01-06-00606.1981",
      "volume": "1",
      "year": "1981",
      "unstructured": "Schwartz, J. H., Journal of Neuroscience 1: 606 (1981).",
      "journal-title": "Journal of Neuroscience"
    },
    {
      "key": "e_1_2_1_33_1",
      "doi-asserted-by": "crossref",
      "first-page": "261",
      "DOI": "10.1080/00335557043000203",
      "volume": "22",
      "year": "1970",
      "unstructured": "SHALLICE, T, QUARTERLY JOURNAL OF EXPERIMENTAL PSYCHOLOGY 22: 261 (1970).",
      "journal-title": "QUARTERLY JOURNAL OF EXPERIMENTAL PSYCHOLOGY"
    },
    {
      "key": "e_1_2_1_34_1",
      "doi-asserted-by": "crossref",
      "first-page": "453",
      "DOI": "10.1146/annurev.ps.44.020193.002321",
      "volume": "44",
      "year": "1993",
      "unstructured": "SQUIRE, L.R., THE STRUCTURE AND ORGANIZATION OF MEMORY, ANNUAL REVIEW OF PSYCHOLOGY 44: 453 (1993).",
      "journal-title": "ANNUAL REVIEW OF PSYCHOLOGY"
    },
    {
      "key": "e_1_2_1_35_1",
      "doi-asserted-by": "crossref",
      "unstructured": "Squire L. R. Memory and Brain (1987).",
      "DOI": "10.1016/B978-0-12-268330-5.50013-5"
    },
    {
      "key": "e_1_2_1_36_1",
      "unstructured": "STARK L.L. unpublished data."
    },
    {
      "key": "e_1_2_1_37_1",
      "doi-asserted-by": "crossref",
      "first-page": "643",
      "DOI": "10.1152/jn.1992.68.2.643",
      "volume": "68",
      "year": "1992",
      "unstructured": "SUGITA, S, INVOLVEMENT OF PROTEIN-KINASE-C IN SEROTONIN-INDUCED SPIKE BROADENING AND SYNAPTIC FACILITATION IN SENSORIMOTOR CONNECTIONS OF APLYSIA, JOURNAL OF NEUROPHYSIOLOGY 68: 643 (1992).",
      "journal-title": "JOURNAL OF NEUROPHYSIOLOGY"
    },
    {
      "key": "e_1_2_1_38_1",
      "doi-asserted-by": "crossref",
      "first-page": "1543",
      "DOI": "10.1152/jn.1983.50.6.1543",
      "volume": "50",
      "year": "1983",
      "unstructured": "WALTERS, E.T., MECHANOAFFERENT NEURONS INNERVATING TAIL OF APLYSIA .2. MODULATION BY SENSITIZING STIMULATION, JOURNAL OF NEUROPHYSIOLOGY 50: 1543 (1983).",
      "journal-title": "JOURNAL OF NEUROPHYSIOLOGY"
    },
    {
      "key": "e_1_2_1_39_1",
      "doi-asserted-by": "crossref",
      "first-page": "408",
      "DOI": "10.1523/JNEUROSCI.07-02-00408.1987",
      "volume": "7",
      "year": "1987",
      "unstructured": "WALTERS, E.T., MULTIPLE SENSORY NEURONAL CORRELATES OF SITE-SPECIFIC SENSITIZATION IN APLYSIA, JOURNAL OF NEUROSCIENCE 7: 408 (1987).",
      "journal-title": "JOURNAL OF NEUROSCIENCE"
    },
    {
      "key": "e_1_2_1_40_1",
      "doi-asserted-by": "crossref",
      "first-page": "259",
      "DOI": "10.1002/cne.903110207",
      "volume": "311",
      "year": "1991",
      "unstructured": "ZHANG, Z.S., SEROTONINERGIC VARICOSITIES MAKE SYNAPTIC CONTACTS WITH PLEURAL SENSORY NEURONS OF APLYSIA, JOURNAL OF COMPARATIVE NEUROLOGY 311: 259 (1991).",
      "journal-title": "JOURNAL OF COMPARATIVE NEUROLOGY"
    }
  ],
  "container-title": "Science",
  "original-title": [],
  "language": "en",
  "link": [
    {
      "URL": "https://www.science.org/doi/pdf/10.1126/science.8211146",
      "content-type": "unspecified",
      "content-version": "vor",
      "intended-application": "similarity-checking"
    }
  ],
  "deposited": {
    "date-parts": [
      [
        2024,
        1,
        15
      ]
    ],
    "date-time": "2024-01-15T10:42:07Z",
    "timestamp": 1705315327000
  },
  "score": 1,
  "resource": {
    "primary": {
      "URL": "https://www.science.org/doi/10.1126/science.8211146"
    }
  },
  "subtitle": [],
  "short-title": [],
  "issued": {
    "date-parts": [
      [
        1993,
        10,
        8
      ]
    ]
  },
  "references-count": 40,
  "journal-issue": {
    "issue": "5131",
    "published-print": {
      "date-parts": [
        [
          1993,
          10,
          8
        ]
      ]
    }
  },
  "alternative-id": [
    "10.1126/science.8211146"
  ],
  "URL": "http://dx.doi.org/10.1126/science.8211146",
  "relation": {},
  "ISSN": [
    "0036-8075",
    "1095-9203"
  ],
  "subject": [],
  "container-title-short": "Science",
  "published": {
    "date-parts": [
      [
        1993,
        10,
        8
      ]
    ]
  }
}