The DOI matches its Crossref record; 22 of the 22 references it cites were found in a registry or an index.
Operant Reward Learning in Aplysia : Neuronal Correlates and Mechanisms
Open accessAbstract
Operant conditioning is a form of associative learning through which an animal learns about the consequences of its behavior. Here, we report an appetitive operant conditioning procedure in Aplysia that induces long-term memory. Biophysical changes that accompanied the memory were found in an identified neuron (cell B51) that is considered critical for the expression of behavior that was rewarded. Similar cellular changes in B51 were produced by contingent reinforcement of B51 with dopamine in a single-cell analog of the operant procedure. These findings allow for the detailed analysis of the cellular and molecular processes underlying operant conditioning.
Overview
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
The cited source doesn’t support the claim as written.
In the citing paper
“For example, Aplysia californica is only capable of modifying the strength of preexisting associations between reflex-eliciting stimuli, and thus its mode of AL does not meet condition ii (see Carew et al., 1981; Hawkins et al., 1983; Brembs et al., 2002; Hawkins and Byrne, 2015 provide a review).”
From The Transition to Minimal Consciousness through the Evolution of Associative Learning (2016) · cites this paper as Brembs et al., 2002
Checked by a reasoning model — may be wrong.
Experimental — accuracy not yet measured
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Citations
Cites
Multiple reward signals in the brain
Schultz, W. (2000) · Nature Reviews Neuroscience · doi:10.1038/35044563 · Cited by 1,303
Dopamine responses comply with basic assumptions of formal learning theory
Waelti, P., Dickinson, A., & Schultz, W. (2001) · Nature · doi:10.1038/35083500 · Cited by 1,018
A cellular mechanism of reward-related learning
Reynolds, J. N. J., Hyland, B. I., & Wickens, J. R. (2001) · Nature · doi:10.1038/35092560 · Cited by 879
Hammer, M. (1993) · Nature · doi:10.1038/366059a0 · Cited by 692
Hawkins, R. D., Abrams, T. W., Carew, T. J., & Kandel, E. R. (1983) · Science · doi:10.1126/science.6294833 · Cited by 617
Localization of a Short-Term Memory in Drosophila
Zars, T. D., Fischer, M., Schulz, R. A., & Heisenberg, M. (2000) · Science · doi:10.1126/science.288.5466.672 · Cited by 605
Associative Conditioning of Single Sensory Neurons Suggests a Cellular Mechanism for Learning
Walters, E. T., & Byrne, J. H. (1983) · Science · doi:10.1126/science.6294834 · Cited by 390
Inhibitory Cerebello-Olivary Projections and Blocking Effect in Classical Conditioning
Kim, J. J., Krupa, D. J., & Thompson, R. F. (1998) · Science · doi:10.1126/science.279.5350.570 · Cited by 212
Morton, D. W., & Chiel, H. J. (1993) · Journal of Comparative Physiology A · doi:10.1007/bf00214712 · Cited by 190
A Systems Approach to the Cellular Analysis of Associative Learning in the Pond Snail LymnaeaPreprint
Benjamin, P. R., Staras, K., & Kemenes, G. (2000) · Learning & Memory · doi:10.1101/lm.7.3.124 · Cited by 167
Flagged first, then by citations
Research works printed but not linked: 2
- I. P. Pavlov Conditioned Reflexes (Oxford University Press Oxford 1927).
- We thank E. Antzoulatos for helpful discussions and E. Wilkinson for invaluable technical assistance. B.B. is a scholar of the Emmy-Noether Programm of the Deutsche Forschungsgemeinschaft. Supported by NIH grant MH 58321. Supporting Online Material www.sciencemag.org/cgi/content/full/296/5573/1706/DC1 Materials and Methods SOM Text Fig. S1 and S2 References and Notes Movies S1 and S2
Cited by
Sorted by citations
Items 201–300 of 338
Rossini, L., & Rossini, P. (2006) · Cited by 6
Dopaminergic Central Neurons and Peripheral Sensory Systems in Pteropod and Nudibranch Molluscs
Norekian, T. P., & Moroz, L. L. (2025) · The Journal of Comparative Neurology · doi:10.1002/cne.70054 · Cited by 5
High fat takes the low road to the brain's reinforcement system
de Araújo, I. E. (2016) · Current Opinion in Behavioral Sciences · doi:10.1016/j.cobeha.2016.04.013 · Cited by 5
Jitsev, E. (2010) · Publication Server of Goethe University Frankfurt am Main (Goethe University Frankfurt) · Cited by 5
Hurwitz, I., Tam, S., Jing, J., Chiel, H. J., & Susswein, A. J. (2024) · Learning & Memory · doi:10.1101/lm.053880.123 · Cited by 4
Plasticity of Intrinsic Excitability as a Mechanism for Memory Storage ☆
Mozzachiodi, R., & Byrne, J. H. (2017) · Elsevier eBooks · doi:10.1016/b978-0-12-809324-5.21114-0 · Cited by 5
Neveu, C. L., Smolen, P. D., Baxter, D. A., & Byrne, J. H. (2023) · Journal of Neuroscience · doi:10.1523/jneurosci.0789-23.2023 · Cited by 5
Norekian, T. P., Liu, Y., Gribkova, E., Cui, J., & Gillette, R. (2024) · PLoS ONE · doi:10.1371/journal.pone.0296872 · Cited by 4
Auletta, G. (2011) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780199608485.003.0023 · Cited by 4
Hawkins, R. D. (2019) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2019.107049 · Cited by 4
Operant Learning in Invertebrates
Nargeot, R., & Puygrenier, L. (2019) · Elsevier eBooks · doi:10.1016/b978-0-12-809633-8.90788-x · Cited by 6
Reconsidering Food Reward, Brain Stimulation, and Dopamine: Incentives Act Forward
Newquist, G., & Gardner, R. A. (2015) · The American Journal of Psychology · doi:10.5406/amerjpsyc.128.4.0431 · Cited by 4
Electrical Synapses and Learning–Induced Plasticity in Motor Rhythmogenesis
Nargeot, R., & Bédécarrats, A. (2017) · Elsevier eBooks · doi:10.1016/b978-0-12-803471-2.00006-0 · Cited by 3
Action Selection and Operant Conditioning: A Neurorobotic Implementation
Cyr, A., & Thériault, F. (2015) · Journal of Robotics · doi:10.1155/2015/643869 · Cited by 3
Roles of Protein Kinase C and Protein Kinase M in Aplysia Learning
Hastings, M. H., Farah, C. A., & Sossin, W. S. (2013) · Handbook of behavioral neuroscience · doi:10.1016/b978-0-12-415823-8.00018-6 · Cited by 3
Analysis of Learning in Invertebrates
Krasne, F. B., Kemenes, G., & Glanzman, D. L. (2010) · Elsevier eBooks · doi:10.1016/b978-0-08-045396-5.00011-7 · Cited by 3
Menzel, R. (2008) · Elsevier eBooks · doi:10.1016/b978-012370509-9.00046-2 · Cited by 2
The Cell Biology of Learning and Memory in Aplysia
Glanzman, D. L. (2008) · Advances in psychology · doi:10.1016/s0166-4115(08)10021-8 · Cited by 2
Learning and Memory: How Sea Slug Behaviors Become Compulsive
Kemenes, G. (2009) · Current Biology · doi:10.1016/j.cub.2009.05.052 · Cited by 2
Weiss, S. J., & Rosales‐Ruiz, J. (2014) · International Journal of Comparative Psychology · doi:10.46867/ijcp.2014.27.04.07 · Cited by 2
Cellular and Molecular Mechanisms of Memory in Mollusks
Byrne, J. H., Hochner, B., & Kemenes, G. (2017) · Elsevier eBooks · doi:10.1016/b978-0-12-809324-5.21097-3 · Cited by 3
Operant Conditioning of Human Upper-Limb Stretch Reflexes
Abolhasani, E. (2018) · Scholarship@Western (Western University) · Cited by 2
Plasticity of Intrinsic Excitability as a Mechanism for Memory Storage
Mozzachiodi, R., & Byrne, J. H. (2008) · Elsevier eBooks · doi:10.1016/b978-012370509-9.00041-3 · Cited by 2
Sleep and conditioning of the siphon withdrawal reflex in Aplysia
Thiede, K. I., Jan Born, A., & Vorster, A. P. A. (2021) · Journal of Experimental Biology · doi:10.1242/jeb.242431 · Cited by 2
Cellular Mechanisms of Associative Learning in Aplysia
Lorenzetti, F. D., & Byrne, J. H. (2008) · Elsevier eBooks · doi:10.1016/b978-012370509-9.00012-7 · Cited by 2
Das gustatorische System und antennales Lernen in der Honigbiene (Apis mellifera L.)
Haupt, S. S. (2005) · doi:10.14279/depositonce-1239 · Cited by 2
Operant and classical learning in Drosophila melanogaster: the ignorant gene (ign)
Bertolucci, F. (2008) · Online Publication Service of Würzburg University (Würzburg University) · Cited by 2
Learning and Memory in Invertebrates: Aplysia
Byrne, J. H., Antzoulatos, E. G., & Fioravante, D. (2009) · Elsevier eBooks · doi:10.1016/b978-008045046-9.00797-x · Cited by 2
Birch, J. (2024) · The Edge of Sentience · doi:10.1093/9780191966729.003.0003 · Cited by 1
Summary of the Framework and Proposals
Birch, J. (2024) · Oxford University Press eBooks · doi:10.1093/9780191966729.003.0001 · Cited by 1
Plasticity of intrinsic excitability as a mechanism for memory storage
Mozzachiodi, R., & Byrne, J. H. (2024) · Elsevier eBooks · doi:10.1016/b978-0-443-15754-7.00041-9 · Cited by 1
Cognitive primitives of the insect brain
Waddell, S., & Park, A. (2025) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2025.11.013 · Cited by 1
Vanaki, S., Gonzalez, N. O., Neveu, C. L., Momohara, Y., Aazhang, B., & Byrne, J. H. (2025) · Communications Biology · doi:10.1038/s42003-025-09357-1 · Cited by 1
Beach, G. A., Young, A. P., Wyeth, R. C., & Croll, R. P. (2025) · Biological Bulletin · doi:10.1086/741017 · Cited by 1
Prompt carefully! ChatGPT displays rule-based insensitivity to contingencies
Ruiz, F. J., & Cardona-Betancourt, V. (2026) · Journal of Contextual Behavioral Science · doi:10.1016/j.jcbs.2026.101012 · Cited by 2
Centimetre-scale landscapes to assess the motion behaviour and cognition of gastropods and bivalves
Seuront, L. (2026) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2024.0384 · Cited by 1
A Systems Analysis of Neural Networks Underlying Gastropod Learning and Memory
Benjamin, P. R. (2013) · Handbook of behavioral neuroscience · doi:10.1016/b978-0-12-415823-8.00014-9 · Cited by 1
Learning Theory and Behavior: Introduction and Overview ☆
Menzel, R. (2017) · Elsevier eBooks · doi:10.1016/b978-0-12-809324-5.21002-x · Cited by 1
Large Language Models and the Gaming Problem
Birch, J. (2024) · Oxford University Press eBooks · doi:10.1093/9780191966729.003.0017 · Cited by 4
Neurobiologia do condicionamento pavloviano e condicionamento operante – Revisão narrativa
Silva, W. D. S. (2024) · Research Society and Development · doi:10.33448/rsd-v13i11.47523 · Cited by 3
Estudios Sobre Cooperación en Perros Domésticos: una Revisión Crítica
Carballo, F., Freidín, E., & Bentosela, M. (2015) · Revista Colombiana de Psicología · doi:10.15446/rcp.v24n1.41221 · Cited by 1
Dorenbosch, M. M. (2015) · Journal of consciousness exploration & research · Cited by 1
Development and Control of Behaviour
Kappeler, P. M. (2021) · Springer eBooks · doi:10.1007/978-3-030-82879-0_12 · Cited by 1
Peters, B. G., & Peters, G. (2002) · Routledge eBooks · doi:10.4324/9780203455494-12 · Cited by 1
Behavioral and Circuit Analysis of Learning and Memory in Mollusks ☆
Benjamin, P. R., & Kemenes, G. (2017) · Elsevier eBooks · doi:10.1016/b978-0-12-809324-5.21023-7 · Cited by 1
Learning and control with large dynamic neural networks
Daucé, E. (2007) · The European Physical Journal Special Topics · doi:10.1140/epjst/e2007-00060-8 · Cited by 2
Williams, W. A. (2017) · Springer eBooks · doi:10.1007/978-3-319-47829-6_1114-1 · Cited by 1
Winters-Bostwick, G. C., Giancola-Detmering, S. E., Bostwick, C. J., & Crook, R. J. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.04.14.589438 · Cited by 1
Entwicklung und Kontrolle des Verhaltens
Kappeler, P. M. (2011) · Springer-Lehrbuch · doi:10.1007/978-3-642-20653-5_11
Neural plasticity: cellular and molecular mechanisms of neural plasticity
Selzer, M. A., Clarke, S., Cohen, L. G., Kwakkel, G., & Miller, R. H. (2014) · Cambridge University Press eBooks · doi:10.1017/cbo9780511995583.003
Princípios de condicionamento à luz da análise neural do estímulo antecedente
Guerra, L. G. G. C. (2006) · Digital Library of Theses and Dissertations (Universidade de São Paulo) · doi:10.11606/t.47.2006.tde-28052006-213453
Memory (Mechanisms Other than LTP )
Debanne, D., & Campanac, E. (2014) · Wiley eBooks · doi:10.1002/9780470015902.a0021398.pub2
Proliferative Diabetic Retinopathy: Current Treatment Strategies for Progression
Scheindlin, J. A. (2002) · Springer eBooks · doi:10.1007/978-94-010-0614-9_9
Time series forecasting with appetitive reward-based pseudo-outer-product fuzzy neural network
Cheu, E. Y., Quek, C. H., & Ng, S. K. (2010) · International Joint Conference on Neural Networks (IJCNN) · doi:10.1109/ijcnn.2010.5596738
Klassiches und operantes Lernen bei Larven der Drosophila
Eschbach, C. (2011)
On the Origin and Evolution of Affective Capacities in Lower Vertebrates
Casimir, M. J. (2008) · Springer eBooks · doi:10.1007/978-0-387-09546-2_4
2 Quantum and Classical Information and Entropy
Auletta, G. (2011) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780199608485.003.0003
20 Intentionality and Conceptualization
Auletta, G. (2011) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780199608485.003.0021
13 The Brain as an Information‐Control System
Auletta, G. (2011) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780199608485.003.0014
5 Dealing with Target Motion and Our Own Movement
Auletta, G. (2011) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780199608485.003.0006
Auletta, G. (2011) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780199608485.003.0004
Weatherill, D. B., Dunn, T. W., McCamphill, P. K., & Sossin, W. S. (2013) · Neuromethods · doi:10.1007/978-1-62703-517-0_3
Auletta, G. (2011) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780199608485.003.0020
6 Complexity: A Necessary Condition
Auletta, G. (2011) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780199608485.003.0007
1 Quantum Mechanics as a General Framework
Auletta, G. (2011) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780199608485.003.0002
Auletta, G. (2011) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780199608485.003.0025
8 The Organism as a Semiotic and Cybernetic System
Auletta, G. (2011) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780199608485.003.0009
Auletta, G. (2011) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780199608485.003.0008
14 Decisional, Emotional, and Cognitive Systems
Auletta, G. (2011) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780199608485.003.0015
25 Final Philosophical Remarks
Auletta, G. (2011) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780199608485.003.0026
Auletta, G. (2011) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780199608485.003.0019
PACAP and Learning in Invertebrates
Kemenes, I., & Kemenes, G. (2016) · Current topics in neurotoxicity · doi:10.1007/978-3-319-35135-3_4
Technology, Psychology, and Evolution
Kool, V. K., & Agrawal, R. (2016) · Springer eBooks · doi:10.1007/978-3-319-45333-0_2
No Ritmo de um Silêncio: a Música como Produtora de Processos Psicológicos
Ribeiro, A. R. M., & Gonçalves, C. M. (2017) · Pensando Psicología · doi:10.16925/pe.v13i22.1989
Operant Place Aversion in the Rusty Crayfish, Orconectes rusticus
Bhimani, R. V. (2014) · OhioLink ETD Center (Ohio Library and Information Network)
Plasticity and Learning in Motor Control Networks
Simmers, J., & Sillar, K. T. (2017) · Wiley eBooks · doi:10.1002/9781118873397.ch13
B31/B32 of Aplysia Currents Contributing to Decision Making in Neurons
Ophir, A., Korngreen, A., Koester, J., & Susswein, A. J. (2013)
MODIFICATION OF APLYSIA FEEDING NETWORK BY L-DOPA AND DOPAMINE-DEPENDENT LEARNING
Neveu, C. L. (2017) · Digital Commons-TMC (Texas Medical Center)
Memory, anticipation, action – working with Troy D. Zars
Wolf, R., Heisenberg, M., Brembs, B., Waddell, S., Mishra, A., Kehrer-Dunlap, A. L., & Simenson, A. (2020) · Journal of Neurogenetics · doi:10.1080/01677063.2020.1715976
From Stimulus to Behavioral Decision-Making
Manière, G., & Coureaud, G. (2020) · Frontiers research topics · doi:10.3389/978-2-88963-463-7
A funny thing happened on the way to the maze
Danek, R. H. (2010) · doi:10.17077/etd.srii9jji
Auletta, G. (2011) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780199608485.003.0016
Auletta, G. (2011) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780199608485.003.0012
Auletta, G. (2011) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780199608485.003.0018
(2008) · Springer-Lehrbuch · doi:10.1007/978-3-540-68792-4_10
Entwicklung und Kontrolle des Verhaltens
Kappeler, P. M. (2020) · Springer eBooks · doi:10.1007/978-3-662-60546-2_12
(2006) · Springer-Lehrbuch · doi:10.1007/3-540-29977-7_10
Functional characterization of a neuropeptide receptor exogenously expressed in Aplysia neuronsPreprint
Zhang, G., Guo, S., Yin, S., Yuan, W.-D., Chen, P., Kim, J., Wang, H., Zhou, H., Susswein, A. J., Kaang, B., et al. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.02.14.480444
(2017) · Elsevier eBooks · doi:10.1016/b978-0-12-805159-7.01001-9
Auletta, G. (2011) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780199608485.003.0001
Auletta, G. (2011) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780199608485.003.0010
Auletta, G. (2011) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780199608485.003.0024
Auletta, G. (2011) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780199608485.003.0017
Auletta, G. (2011) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780199608485.003.0022
Auletta, G. (2011) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780199608485.003.0005
Memory: Mechanisms Other than LTP
Debanne, D., & Campanac, E. (2009) · Wiley eBooks · doi:10.1002/9780470015902.a0021398
Auletta, G. (2011) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780199608485.003.0013
Metadata
- Authors
- Brembs, B., Lorenzetti, F. D., Reyes, F. D., Baxter, D. A., & Byrne, J. H.
- Affiliations
- Department of Neurobiology and Anatomy, W. M. Keck Center for the Neurobiology of Learning and Memory, The University of Texas–Houston Medical School, Houston, TX 77030, USA.
- Corresponding author
- Lorenzetti, Fred D.
- Byrne, John H.
- ORCID
- Byrne, John H.
- Venue
- Science
- Published
- 2002-05-31
- Volume
- 296
- Issue
- 5573
- Pages
- 1706-1709
- ISSN
- 0036-8075 (ISSN-L)
- 1095-9203
- OpenAlex
- W2055848231
- Cited by
- 338
- References
- 22
- Citations by year
- 2026: 5 · 2025: 5 · 2024: 32 · 2023: 5 · 2022: 8 · 2021: 8 · 2020: 10 · 2019: 9 · 2018: 6 · 2017: 24 · 2016: 13 · 2015: 14 · 2014: 18 · 2013: 12 · 2012: 13
- FWCI
- 7.34
- Type
- journal article
- Language
- en
- Open access
- green
- doi.org
- Locations
- Science (publishedVersion)
- PubMed (publishedVersion)
- University of Regensburg Publication Server (University of Regensburg) (acceptedVersion)
- University of Regensburg Publication Server (University of Regensburg)
- Funders
- National Institute of Mental Health (R01MH058321, MH58321)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurobiology and Insect Physiology Research
- Keywords
- operant conditioning, Aplysia, appetitive learning, long-term memory, dopamine, contingent reinforcement, associative learning
- MeSH terms
- Animals, Aplysia, Cells, Cultured, Conditioning, Operant, Dopamine, Eating, Electric Stimulation, Electrophysiology, Esophagus, Feeding Behavior, Food, Iontophoresis, Membrane Potentials, Memory, Nerve Net, Neuronal Plasticity, Neurons, Reinforcement, Psychology, Reward, Ganglia, Invertebrate, Patch-Clamp Techniques
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
