Corollary discharge inhibition and preservation of temporal information in a sensory nucleus of mormyrid electric fish
Open accessAbstract
Knollenorgan electroreceptors in mormyrid fish are concerned with electrocommunication, i.e., with detecting electric organ discharges (EODs) of other electric fish. But knollenorgan electroreceptors are also activated by the fish's own EOD. Potential interference by such self-stimulation is blocked by an inhibitory corollary discharge in the nucleus of the electrosensory lateral line lobe (NELL), the first central relay of the knollenorgan pathway. This study used intracellular recording and staining to examine the mechanism of the corollary inhibition and the specializations in anatomy and physiology that permit the accurate relaying of temporal information about the EODs of other fish. Several events are recorded inside primary knollenorgan afferents in addition to a large orthodromic action potential. The additional events include small orthodromic electronic epsps, postsynaptic action potentials, and a corollary discharge inhibitory postsynaptic potential (ipsp) associated with the EOD motor command. These additional events are also recorded in NELL cells and almost certainly originate there. Electrical coupling between afferents and cells makes it possible to observe the events inside primary afferents. The corollary discharge ipsp in the cell is associated with a conductance increase and inverts rapidly when recorded with chloride- containing electrodes, supporting a hypothesis of GABA mediation. The ipsp lasts longer in cells than in afferents. Each electrotonic excitatory postsynaptic potential (epsp) is probably caused by a single primary afferent, and any one of several epsps in a given cell seems capable of eliciting a postsynaptic spike in that cell. The epsps follow stimulation rates as high as 500/sec with minimal variability. No lateral inhibition is observed in NELL. These and other properties indicate that the knollenorgan pathway is specialized for temporal information rather than spatial or intensity information.
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
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?
Electric fish send top-down corollary discharges to inhibit ascending sensory pathways.
“An example in lower vertebrates is seen in electric fish (Bell and Grant 1989), which send top-down corollary discharges to inhibit ascending sensory pathways.”
From Action and behavior: a free-energy formulation (2010) · cites this paper as Bell and Grant 1989
The knollenorgan corollary discharge inhibits the respective electroreceptor during electric-organ discharge.
“These systems differ from the ampullary system in that they require CDs that amplify (mormyromast) or inhibit (knollenorgan) the respective electroreceptor during EOD.”
From Corollary discharge across the animal kingdom (2008) · cites this paper as [51]
The mormyromast corollary discharge amplifies the respective electroreceptor during electric-organ discharge.
“These systems differ from the ampullary system in that they require CDs that amplify (mormyromast) or inhibit (knollenorgan) the respective electroreceptor during EOD.”
From Corollary discharge across the animal kingdom (2008) · cites this paper as [51]
The mormyrid has two additional electroreceptor subtypes, mormyromasts and knollenorgans, that are susceptible to electric-organ discharge feedback, and compensatory corollary discharge systems are in place to accommodate them.
“Interestingly, the mormyrid has two additional electroreceptor subtypes (mormyromasts and knollenorgans) that are susceptible to electric-organ discharge (EOD) feedback and, accordingly, compensatory CD systems are in place to accommodate them50,51.”
From Corollary discharge across the animal kingdom (2008) · cites this paper as [51]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
The Fine Structure of the Nervous System.
Tennyson, V. M. (1970) · Archives of Neurology · doi:10.1001/archneur.1970.00480240094019 · Cited by 1,946 · see citing works
fine structure of the nervous system
Peters, A., Palay, S. L., & Webster, H. D. (1976) · Cited by 592 · see citing works
Neuronal and behavioral sensitivity to binaural time differences in the owl
Moiseff, A., & Konishi, M. (1981) · Journal of Neuroscience · doi:10.1523/jneurosci.01-01-00040.1981 · Cited by 325 · see citing works
Time and intensity cues are processed independently in the auditory system of the owl
Takahashi, T. T., Moiseff, A., & Konishi, M. (1984) · Journal of Neuroscience · doi:10.1523/jneurosci.04-07-01781.1984 · Cited by 254 · see citing works
Temporal Coding of Species Recognition Signals in An Electric Fish
Hopkins, C. D., & Bass, A. H. (1981) · Science · doi:10.1126/science.7209524 · Cited by 246 · see citing works
Maler, L., Sas, E., & Rogers, J. (1981) · The Journal of Comparative Neurology · doi:10.1002/cne.901950107 · Cited by 215 · see citing works
Electrical Transmission: A Functional Analysis and Comparison to Chemical Transmission
Bennett, M. V. L. (1977) · Comprehensive physiology · doi:10.1002/cphy.cp010111 · Cited by 208 · see citing works
Properties of a modifiable efference copy in an electric fish.
Bell, C. C. (1982) · Journal of Neurophysiology · doi:10.1152/jn.1982.47.6.1043 · Cited by 169 · see citing works
Self-citationCentral connections of the posterior lateral line lobe in mormyrid fish
Bell, C. C., Finger, T. E., & Russell, C. J. (1981) · Experimental Brain Research · doi:10.1007/bf00235724 · Cited by 157 · see citing works
Self-citationJhaveri, S., & Morest, D. K. (1982) · Neuroscience · doi:10.1016/0306-4522(82)90045-8 · Cited by 155 · see citing works
Paintal, A. S. (1966) · The Journal of Physiology · doi:10.1113/jphysiol.1966.sp007948 · Cited by 153 · see citing works
Heiligenberg, W., & Dye, J. (1982) · Journal of Comparative Physiology A · doi:10.1007/bf00679013 · Cited by 150 · see citing works
Swadlow, H. A., & Waxman, S. G. (1976) · Experimental Neurology · doi:10.1016/0014-4886(76)90288-0 · Cited by 137 · see citing works
Characterization of HRP‐labeled globular bushy cells in the cat anteroventral cochlear nucleus
Smith, P. H., & Rhode, W. S. (1987) · The Journal of Comparative Neurology · doi:10.1002/cne.902660305 · Cited by 129 · see citing works
Electroreceptors in MormyridsPreprint
Bennett, M. V. L. (1965) · Cold Spring Harbor Symposia on Quantitative Biology · doi:10.1101/sqb.1965.030.01.027 · Cited by 129 · see citing works
A time-comparison circuit in the electric fish midbrain. II. Functional morphology
Carr, C., Maler, L., & Taylor, B. (1986) · Journal of Neuroscience · doi:10.1523/jneurosci.06-05-01372.1986 · Cited by 103 · see citing works
Bell, C. C., Myers, J. P., & Russell, C. J. (1974) · Journal of Comparative Physiology A · doi:10.1007/bf00694506 · Cited by 103 · see citing works
Self-citationBell, C. C., & Russell, C. J. (1978) · Journal of Comparative Neurology · doi:10.1002/cne.901820302 · Cited by 99 · see citing works
Self-citationTemporal hyperacuity in the electric sense of fish
Rose, G. J., & Heiligenberg, W. (1985) · Nature · doi:10.1038/318178a0 · Cited by 96 · see citing works
Getting, P. A. (1974) · Journal of Neurophysiology · doi:10.1152/jn.1974.37.5.846 · Cited by 94 · see citing works
Interaction of electrosensory and electromotor signals in lateral line lobe of a mormyrid fish
Zipser, B., & Bennett, M. V. L. (1976) · Journal of Neurophysiology · doi:10.1152/jn.1976.39.4.713 · Cited by 92 · see citing works
Neuronal responses to electrosensory input in mormyrid valvula cerebelli
Russell, C. J., & Bell, C. C. (1978) · Journal of Neurophysiology · doi:10.1152/jn.1978.41.6.1495 · Cited by 89 · see citing works
Self-citationKramer, B. (1974) · Journal of Comparative Physiology A · doi:10.1007/bf00607000 · Cited by 80 · see citing works
A time comparison circuit in the electric fish midbrain
Carr, C. E. (1987) · Proceedings annual meeting Electron Microscopy Society of America · doi:10.1017/s0424820100127852 · Cited by 76 · see citing works
Kramer, B. (1979) · Behavioral Ecology and Sociobiology · doi:10.1007/bf00293246 · Cited by 64 · see citing works
Mugnaini, E., & Maler, L. (1987) · Anatomy and Embryology · doi:10.1007/bf00310187 · Cited by 51 · see citing works
Time Coding in Electric Fish and Barn Owls
Carr, C. E. (2008) · Brain Behavior and Evolution · doi:10.1159/000118697 · Cited by 44 · see citing works
GABA and Glycine: Postsynaptic Actions
Alger, B. E. (1985) · Springer eBooks · doi:10.1007/978-1-4684-4961-7_2 · Cited by 34 · see citing works
Fast conducting electrosensory pathway in the mormyrid fish, Gnathonemus petersii
Enger, P. S., Libouban, S., & Szabo, T. L. (1976) · Neuroscience Letters · doi:10.1016/0304-3940(76)90004-5 · Cited by 31 · see citing works
Enger, P. S., Libouban, S., & Szabo, T. L. (1976) · Neuroscience Letters · doi:10.1016/0304-3940(76)90049-5 · Cited by 30 · see citing works
Denizot, J., Clausse, S., Elekes, K., Geffard, M., Grant, K., Libouban, S., Ravaille‐Veron, M., & SZABO, T. (1987) · Cell and Tissue Research · doi:10.1007/bf00215512 · Cited by 18 · see citing works
Self-citationSzabo, T. L., Ravaille‐Veron, M., & Libouban, S. (1978) · Neuroscience Letters · doi:10.1016/0304-3940(78)90040-x · Cited by 17 · see citing works
Primary afferent fibers conduct impulses in both directions under physiological stimulus conditions
Slesinger, P. A., & Bell, C. C. (1985) · Journal of Comparative Physiology A · doi:10.1007/bf00611090 · Cited by 17 · see citing works
Self-citationBinder, M. D., Hirokawa, N., & Windhorst, U. (2008) · Springer eBooks · doi:10.1007/978-3-540-29678-2_2955 · Cited by 1 · see citing works
Flagged first, then by citations
Research works printed but not linked: 6
- Bell, C. C. (1986) Electroreception in mormyrid fish, central physi- oloav. In Etectroreception. T. H. Bullock and W. Heilirrenbera. eds.. pp.423-452, Wiley,New'York.
- Bennett, M. V. L. (1971) Electric organs. In Fish Physiology, W. S. Hoar and D. J. Randall, eds., pp. 34749 1, Academic, New York.
- Bennett, M. V. L., and D. C. Spray (1987) Intracellular communication mediated by gap junctions can be controlled in many ways. In Syn- aptic Function, G. M. Edelman, W. E. Gall, and W. M. Cowan, eds., pp. 109-135, Wiley, New York.
- Bennett, M. V. L., and A. B. Steinbach (1969) Influence of electric organ control system on electrosensory afferent pathways in mor- myrids. In Neurobiology of Cerebellar Evolution and Development, R. Llinas, ed., pp. 207-214, Am. Med. Assoc., Chicago.
- Heiligenberg, W. (1986) Jamming avoidance responses: Model sys- tems for neuroethology. In Electroreception, T. H. Bullock and W. Heiligenberg, eds., pp. 6 13-650, Wiley, New York.
- Szabo. T.. and A. Fessard (1974) Phvsiologv of electrorecentors. In Handbook of Sensory Physiolo& Electroreceptors, Other Specialized Receptors in Other Vertebrates, A. Fessard, ed., p. 124, Springer- Verlag, Berlin.
Cited by
Sorted by citations
Energy limitation as a selective pressure on the evolution of sensory systems
Niven, J. E., & Laughlin, S. B. (2008) · Journal of Experimental Biology · doi:10.1242/jeb.017574 · Cited by 1,056 · see citing works
Action and behavior: a free-energy formulation
Friston, K. J., Daunizeau, J., Kilner, J., & Kiebel, S. J. (2010) · Biological Cybernetics · doi:10.1007/s00422-010-0364-z · Cited by 866 · see citing works
“An example in lower vertebrates is seen in electric fish (Bell and Grant 1989), which send top-down corollary discharges to inhibit ascend-”
BackgroundCorollary discharge across the animal kingdom
Crapse, T. B., & Sommer, M. A. (2008) · Nature Reviews Neuroscience · doi:10.1038/nrn2457 · Cited by 789 · see citing works
A circuit for motor cortical modulation of auditory cortical activity
Nelson, A., Schneider, D. M., Takatoh, J., Sakurai, K., Wang, F., & Mooney, R. (2013) · The Journal of Neuroscience · doi:10.1523/jneurosci.2275-13.2013 · Cited by 213 · see citing works
The Cellular Basis of a Corollary Discharge
Poulet, J. F. A., & Hedwig, B. (2006) · Science · doi:10.1126/science.1120847 · Cited by 234 · see citing works
von der Emde, G., & Bleckmann, H. (1992) · Journal of Comparative Physiology A · doi:10.1007/bf00194116 · Cited by 68 · see citing works
Mohr, C., Roberts, P. D., & Bell, C. C. (2003) · Journal of Neurophysiology · doi:10.1152/jn.00211.2003 · Cited by 59 · see citing works
Self-citation
- Authors
- Bell, C., & Grant, K.
- Affiliations
- Legacy Good Samaritan Medical Center (US)
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 1989-03-01
- Volume
- 9
- Issue
- 3
- Pages
- 1029-1044
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC6569966
- OpenAlex
- W2101963026
- Cited by
- 122
- References
- 34
- Citations by year
- 2026: 2 · 2025: 2 · 2024: 1 · 2023: 7 · 2022: 2 · 2021: 3 · 2020: 6 · 2019: 7 · 2018: 5 · 2017: 5 · 2016: 5 · 2015: 4 · 2014: 3 · 2013: 6 · 2012: 3
- FWCI
- 5.09
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Science Foundation
- National Institutes of Health
- Topics
- Physical Sciences › Environmental Science › Nature and Landscape Conservation › Fish biology, ecology, and behavior
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Keywords
- temporal coding, electric organ discharge, inhibitory postsynaptic potentials, GABAergic inhibition, electrical coupling, primary afferents, electrocommunication, electroreception
- MeSH terms
- Action Potentials, Animals, Electric Fish, Electric Organ, Intracellular Membranes, Nerve Fibers, Nervous System Physiological Phenomena, Neural Inhibition, Neurons, Afferent, Sensation, Time Perception
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
