The DOI matches its Crossref record; 60 of the 62 references it cites were found in a registry or an index.
Mushroom Body Output Neurons Encode Odor–Reward Associations
Open accessAbstract
Neural correlates of learning and memory formation have been reported at different stages of the olfactory pathway in both vertebrates and invertebrates. However, the contribution of different neurons to the formation of a memory trace is little understood. Mushroom bodies (MBs) in the insect brain are higher-order structures involved in integration of olfactory, visual, and mechanosensory information and in memory formation. Here we focus on the ensemble spiking activity of single MB output neurons (ENs) when honeybees learned to associate an odor with reward. A large group of ENs (∼50%) changed their odor response spectra by losing or gaining sensitivity for specific odors. This response switching was dominated by the rewarded stimulus (CS+), which evoked exclusively recruitment. The remaining ENs did not change their qualitative odor spectrum but modulated their tuning strength, again dominated by increased responses to the CS+. While the bees showed a conditioned response (proboscis extension) after a few acquisition trials, no short-term effects were observed in the neuronal activity. In both EN types, associative plastic changes occurred only during retention 3 h after conditioning. Thus, long-term but not short-term memory was reflected by increased EN activity to the CS+. During retention, the EN ensemble separated the CS+ most differently from the CS− and control odors ∼140 ms after stimulus onset. The learned behavioral response appeared ∼330 ms later. It is concluded that after memory consolidation, the ensemble activity of the MB output neurons predicts the meaning of the stimulus (reward) and may provide the prerequisite for the expression of the learned behavior.
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 source backs part of the claim, not all of it — or backs it for a different population, condition or comparison.
In the citing paper
“It is well established that Hebbian-like plasticity in connections at the output of the mushroom body can support various forms of reinforcement learning [71,76–78].”
From Phenomenal interface theory: a model for basal consciousness (2025) · cites this paper as [78]
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
Predictive reward signal of dopamine neurons
Schultz, W. (1998) · Journal of Neurophysiology · doi:10.1152/jn.1998.80.1.1 · Cited by 4,564
Long-Term Potentiation--A Decade of Progress?
Malenka, R. C., & Nicoll, A. R. A. (1999) · Science · doi:10.1126/science.285.5435.1870 · Cited by 2,729
Cellular basis of working memory
Goldman-Rakic, P. S. (1995) · Neuron · doi:10.1016/0896-6273(95)90304-6 · Cited by 2,663
Cognitive Neuroscience and the Study of Memory
Milner, B. A., Squire, L. R., & Kandel, E. R. (1998) · Neuron · doi:10.1016/s0896-6273(00)80987-3 · Cited by 1,335
Mushroom body memoir: from maps to models
Heisenberg, M. (2003) · Nature Reviews Neuroscience · doi:10.1038/nrn1074 · Cited by 1,286
Sparse Coding and Decorrelation in Primary Visual Cortex During Natural Vision
Vinje, W. E., & Gallant, J. L. (2000) · Science · doi:10.1126/science.287.5456.1273 · Cited by 1,286
Harris, K. D., Henze, D. A., Csicsvari, J. L., Hirase, H., & Buzsáki, G. (2000) · Journal of Neurophysiology · doi:10.1152/jn.2000.84.1.401 · Cited by 1,153
Classical conditioning of proboscis extension in honeybees (Apis mellifera).
Bitterman, M. E., Menzel, R., Fietz, A., & Sch?fer, S. (1983) · Journal of comparative psychology · doi:10.1037/0735-7036.97.2.107 · Cited by 1,077
Self-citationOscillations and Sparsening of Odor Representations in the Mushroom Body
Pérez-Orive, J., Mazor, O., Turner, G. C., Cassenaer, S., Wilson, R. I., & Laurent, G. (2002) · Science · doi:10.1126/science.1070502 · Cited by 792
Drosophila Mushroom Body Mutants are Deficient in Olfactory Learning
Heisenberg, M., Borst, A., Wagner, S., & Byers, D. (1985) · Journal of Neurogenetics · doi:10.3109/01677068509100140 · Cited by 697
Research works printed but not linked: 2
- Strube-Bloss MF (2008) Characterization of mushroom body extrinsic neurons of the honeybee: odor specificity, response reliability, and learning related plasticity. Dissertation (Freie Universitaet Berlin).
- 10.1080/713663277 · DOI
Cited by
Sorted by citations
The honeybee as a model for understanding the basis of cognition
Menzel, R. (2012) · Nature reviews. Neuroscience · doi:10.1038/nrn3357 · Cited by 467
Self-citationGiurfa, M., & Sandoz, J. (2012) · Learning & Memory · doi:10.1101/lm.024711.111 · Cited by 413
Heterosynaptic plasticity underlies aversive olfactory learning in Drosophila
Hige, T., Aso, Y., Modi, M. N., Rubin, G. M., & Turner, G. C. (2015) · Neuron · doi:10.1016/j.neuron.2015.11.003 · Cited by 354
Insects have the capacity for subjective experience
Klein, C., & Barron, A. B. (2016) · Animal Sentience · doi:10.51291/2377-7478.1113 · Cited by 243
The neurobiology of insect olfaction: Sensory processing in a comparative context
Martin, J. P., Beyerlein, A., Dacks, A. M., Reisenman, C. E., Riffell, J. A., Lei, H., & Hildebrand, J. G. (2011) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2011.09.007 · Cited by 225
Metadata
- Authors
- Strube-Bloss, M. F., Nawrot, M. P., & Menzel, R.
- Affiliations
- Freie Universität Berlin (DE)
- Arizona State University (US)
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2011-02-23
- Volume
- 31
- Issue
- 8
- Pages
- 3129-3140
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC6623757
- OpenAlex
- W1985449617
- Cited by
- 157
- References
- 62
- Citations by year
- 2026: 3 · 2025: 16 · 2024: 4 · 2023: 5 · 2022: 9 · 2021: 8 · 2020: 12 · 2019: 5 · 2018: 8 · 2017: 11 · 2016: 11 · 2015: 17 · 2014: 13 · 2013: 19 · 2012: 11
- FWCI
- 6.36
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- HAL (submittedVersion)
- PUB – Publications at Bielefeld University (Bielefeld University) (submittedVersion)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurobiology and Insect Physiology Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Keywords
- mushroom body, output neurons, olfactory conditioning, Apis mellifera, memory consolidation, long-term memory, associative plasticity, memory traces, proboscis extension
- MeSH terms
- Animals, Bees, Electrophysiology, Female, Memory, Neurons, Odorants, Reward, Smell, Mushroom Bodies
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