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The command neuron concept

Published online by Cambridge University Press:  04 February 2010

Irving Kupfermann
Affiliation:
Department of Psychiatry and Division of Neurobiology and Behavior, College of Physicians and Surgeons of Columbia University, New York, NY 10032
Klaudiusz R. Weiss
Affiliation:
Department of Psychiatry and Division of Neurobiology and Behavior, College of Physicians and Surgeons of Columbia University, New York, NY 10032

Abstract

The notion of the command cell has been highly influential in invertebrate neurobiology, and related notions have been increasingly used in research on the vertebrate nervous system. The term “command neuron” implies that the neuron has some critical function in the generation of a normally occurring behavior. Nevertheless, most authors either explicitly or implicitly use a strictly operational definition, independent of considerations of normal behavioral function. That is, command neurons are often defined as neurons which, when stimulated by the experimenter, evoke some behavioral response. Even when utilizing such an operational definition, investigators frequently differ on what they consider to be the exact characteristics that a neuron must have (or not have) to be considered a command cell. A few authors appear to treat command neurons in relation to normal function, but a precise behaviorally relevant definition has not been specified. Because of the ambiguity in the definition of command neurons, the term can refer to a wide variety of neurons which may play divergent behavioral roles. In some ways the attempt to label a cell as a command neuron may interfere with the process of discovering the complex causal determinants of behavior. Nevertheless, the notion that individual cells are responsible for certain behaviors is highly appealing, and an attempt to define the command neuron rigorously could be worthwhile. We suggest that a command neuron be defined as a neuron that is both necessary and sufficient for the initiation of a given behavior. These criteria can by tested by: (1) establishing the response pattern of the putative command neuron during presentation of a given stimulus and execution of a well specified behavior; (2) removing the neuron and showing that the response is no longer elicited by the stimulus (necessary condition); and (3) firing the neuron in its normal pattern and showing that the complete behavioral response occurs (sufficient condition). In some cases, groups of neurons, when treated as a whole, may satisfy the necessity and sufficiency criteria for a given behavior, even though individual neurons of the group fail to meet the criteria. We suggest that such a group be termed a “command system” for the behavior in question. Individual neurons in the command system can be termed “command elements” if, when fired in their normally occurring pattern, they elicit a part of the behavior, or “modulatory elements” if they do not in isolation elicit any response, but alter the behavior produced by other elements in the command system.

Type
Target Article
Copyright
Copyright © Cambridge University Press 1978

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References

REFERENCES

Atwood, H. L. and Wiersma, C. A. G.Command interneurons in the crayfish central nervous system. Journal of Experimental Biology 46:249261, 1967CrossRefGoogle ScholarPubMed
Berry, M. S. and Pentreath, V. W.Properties of a symmetric pair of serotonin-containing neurones in the cerebral ganglia of Planorbis. Journal of Experimental Biology. 65:361380, 1976.CrossRefGoogle ScholarPubMed
Bowerman, R. F. and Larimer, J. L.Command fibres in circumoesophageal connectives of crayfish. 1. Tonic fibres. Journal of Experimental Biology. 60:95117, 1974.CrossRefGoogle Scholar
Command neurons in crustaceans. Comparative Biochemistry and Physiology. 54A: 15, 1976.CrossRefGoogle Scholar
Bryant, H. The command neuron. Sixth Annual Winter Conference on Brain Research. Brain Information Service, University of California, Los Angeles, 1973.Google Scholar
Burrows, M.Co-ordinating interneurones of the locust which convey two patterns of motor commands: their connexions with flight motoneurones. Journal of Experimental Biology. 63:713733. 1975CrossRefGoogle ScholarPubMed
Byrne, J.Input-output characteristics ot the defensive gill-withdrawal reflex in Aplysia californica. Neuroscience Abstracts. 1:591, 1975.Google Scholar
Davis, W. J Organizational concepts in the central motor networks of invertebrates. In: Herman, R. M., Grillner, S., Stein, P. S. G. and Sturart, D. G. (eds.), Neural Control of Locomotion. Plenum, New York, pp. 265292, 1976.CrossRefGoogle Scholar
The command neuron. In: Hoyle, G. (ed.), Identified Neurons and Arthropod Behavior. In press, 1977.CrossRefGoogle Scholar
and Kennedy, D. Command interneurons controlling swimmeret movements in the lobster. II. Interaction of effects on motoneurons. Journal of Neurophysiology. 35:1319, 1972Google Scholar
Diamond, J. The Mauthner cell. In: Hoar, W. S. and Randall, D. J. (eds.) Fish Physiology, Vol. 5: Sensory Systems and Electric Organs. Academic Press, New York, pp. 265346, 1971.CrossRefGoogle Scholar
Doty, R. W. The concept of neural centers. In: Fentress, J. C. (ed.) Simpler Networks and Behavior, Sinauer Assoc, Inc., Sunderland, Mass., pp. 251265, 1976Google Scholar
Evans, P. D., Talamo, B. R., and Kravitz, E. A.Octopamine neurons: morphology, release of octopamine and possible physiological role. Brain Research. 90:340347, 1975.CrossRefGoogle ScholarPubMed
Gelperin, A.Identified serotonergic neurons modulate feeding in the terrestrial mullusc, Limax maximus. Physiologist 19:204, 1976.Google Scholar
Getting, P. A.Neuronal organization of escape swimming in Tritonia. Journal of Comparative Physiology. In Press.Google Scholar
Gillette, R. and Davis, W. J.Control of feeding behavior by the metacerebral giant neuron ofPleurobranchaea. Neuroscience Abstracts. 1:571, 1975.Google Scholar
The role of the metacerebral giant neuron in the feeding behavior of Pleurobranchaea. Journal of Comparative Physiology. 116:129159, 1977.CrossRefGoogle Scholar
and Kovac, M. P.Command neurons receive synaptic feedback from the motor network they excite. Science, 199:798801, 1978.Google Scholar
Grillner, S.Locomotion in vertebrates: central mechanisms and reflex interaction Physiological Reviews 55:247304, 1975.CrossRefGoogle ScholarPubMed
Harth, E. and Lewis, N. S.The escape of Tritonia: dynamics of a neuromuscular control mechanism. Journal of Theoretical Biology. 55:201228, 1975.CrossRefGoogle ScholarPubMed
Hoyle, G.A function for neurons (DUM) neurosecretory on skeletal muscle of insects. Journal of Experimental Zoology. 189:401406, 1974.CrossRefGoogle ScholarPubMed
Ikeda, K Genetically patterned neural activity. In: Fentress, J. C. (ed.) Simpler Networks and Behavior. Sinauer Assoc, Inc., Sunderland, Mass., pp. 140152, 1976.Google Scholar
Kandel, E. R. and Tauc, L.Anomalous rectification in the metacerebral giant cells and its consequences for synaptic transmission. Journal of Physiology. 183:287304, 1966.CrossRefGoogle ScholarPubMed
Kater, S. B.Feeding in Helisoma trivolvis: the morphological and physiological bases of a fixed action pattern. American Zoologist 14:10171036, 1974.CrossRefGoogle Scholar
Kennedy, D The control of output by central neurons. In: Brazier, M. A. B., The Interneuron. University of California Press, Berkeley and Los Angeles, pp. 2136, 1969.CrossRefGoogle Scholar
and Davis, W. J. The organization of invertebrate motor systems. In: Kandel, E. R. (ed.) Handbook of Physiology, Vol. 2: Neurophysiology. American Physiological Society, Bethesda, Md. pp. 10231087, 1977.Google Scholar
Evoy, W. H., Dane, B, and Hanawalt, J. T.The central nervous organization underlying control of antagonistic muscles in the crayfish. II. Coding of position by command fibres. Journal of Experimental Zoology. 165:239248, 1967.Google Scholar
Koester, J., Mayeri, E., Liebeswar, G., and Kandel, E. R.Neural control of circulation in Aplysia. II. Interneurons. Journal of Neurophysiology 37:476496, 1974.CrossRefGoogle ScholarPubMed
Kupfermann, I.Stimulation of egg laying by extracts of neuroendocrine cells (bag cells) of abdominal ganglion of Aplysia. Journal of Neurophysiology. 33:877881, 1970.CrossRefGoogle ScholarPubMed
Feeding behavior in Aplysia: a simple system for the study of motivation. Behavioral Biology. 10:126, 1974.CrossRefGoogle Scholar
Pinsker, H., Castellucci, V., and Kandel, E. R.Central and peripheral control of gill movements in Aplysia. Science 174:12521256, 1971.Google Scholar
Larimer, J. L., Eggleston, A. C, Masukawa, L. M., and D., KennedyThe different connections and motor outputs of lateral and medial giant fibres in the crayfish. Journal of Experimental Biology. 54:391402, 1971.CrossRefGoogle ScholarPubMed
Mountcastle, V. B., Lynch, J. C, Georgopoulos, A., Sakata, H., and Acuno, C.Posterior parietal association cortex of the monkey: command functions for operations within extrapersonal space. Journal of Neurophysiology. 38:871908, 1975.CrossRefGoogle ScholarPubMed
Nabias, B. de, Récherches histologique et organologiques sur les centres nerveux de gastéropodes. Actes Societée Linnae. (Bordeaux) 47:1202, 1894.Google Scholar
Peaison, K G and Foiutnei, C R.Nonspiking uiterneurons m walking system of cockroach. Journal of Neurophystology 38:3352, 1975CrossRefGoogle Scholar
Roberts, K.Disinhibition as an organzung priciple in the nervou system—the role of gama-ammobutyric acid Advances in Neurology 5:127143, 1974.Google Scholar
Selverston, A I. Nenronal mechanisms for rhythmic motor pattern geneiation in a simple system. In: Fentress, J C. (ed.) Simpler Networks and Behavior. Sinnauer Assoc, Inc., Sunderland, Mass., pp. 377399, 1976.Google Scholar
Senseman, D. and Gelperm, A.Comparative aspects of the morphology and physiology of a single identifiable neuron in Helix aspersa, Limax maximus, and Ariolimax califonica. Malacologwal Review. 7:5152, 1974.Google Scholar
Weiss, K. R., Cohen, J., and Kupfermann, I.Potentiation of muscle contraction: a possible modulatory function of an identified serotonergiccell in Aplysia. Brain Research. 99:381386, 1975CrossRefGoogle Scholar
Modulatory control of buccal musculature by a serotonergic neuron (metacerebral cell) in Aplysia. Journal of Neurophysiology 41:181201, 1978.CrossRefGoogle Scholar
Weiss, K. R. and Kupfermann, I.Homology of the giant serotonergic neurons (metacerebral cells) in Aplysia and pulmonate molluscs. Brain Research. 117:3349, 1976CrossRefGoogle ScholarPubMed
Weiss, K. R., Schonberg, M., Cohen, J, Mandelbaum, D., and Kupfermann, I.Modulation of muscle contraction by a serotonergic neuron: possible role of cAMP. Neuroscience Abstracts 2:338, 1976.Google Scholar
Wiersma, C. A G.Function of the giant fibers of the central nervous system of the crayfish. Proceedings of the Society of Experimental Biology and Medicine United States of America 38:661662, 1938.CrossRefGoogle Scholar
Neurons of arthropods. Cold Spring Harbor Symposium oti Quantitative Biology. 17:155163, 1952.CrossRefGoogle Scholar
and Ikeda, K.Interneurons commanding swimmeret movements in the crayfish, Procambarus clarkii (Girard). Comparative Biochemistry and Physiology. 12:509525, 1964.Google Scholar
Willows, A. O. D. and Hoyle, G.Neuronal network truggering a fixed action pattern Science. 166:15491551, 1969.CrossRefGoogle ScholarPubMed
Wine, J. J. and Krasne, F. B.The organization of escape behavior m the crayfish. Journal of Experimental Biology. 56:118, 1972.CrossRefGoogle Scholar
Winlow, W. and Laverack, M. S.The control of hindgut motility in the lobster, Homarus gammarus (L.). 3. Structure of the sixth abdominal ganglion (6 A. G.) and associated ablation and microelectrode studies. Marine Behavior and Physiology. 1:93121, 1972.Google Scholar