Nature 366, 59 - 63 (04 November 1993); doi:10.1038/366059a0

An identified neuron mediates the unconditioned stimulus in associative olfactory learning in honeybees

Martin Hammer

Institut für Neurobiologie, Freie Universität Berlin, Königin-Luise Strasse 28/30, 14195 Berlin, Germany

DURING classical conditioning, animals learn to associate a neutral stimulus with a meaningful, or unconditioned, stimulus. The unconditioned stimulus is essential for forming associations, and modifications in the processing of the unconditioned stimulus are thought to underlie more complex learning forms^1–4. Information on the neuronal representation of the unconditioned stimulus is therefore required for understanding both basic and higher-order features of conditioning. In honeybees, conditioning of the proboscis extension reflex occurs after a single pairing of an odour (conditioned stimulus) with food (unconditioned stimulus)^5,6 and shows several higher-order features of conditioning^6–8. I report here the identification of an interneuron that mediates the unconditioned stimulus in this associative learning. Its physiology is also compatible with a function in complex forms of associative learning. This neuron provides the first direct access to the cellular mechanisms underlying the reinforcing properties of the unconditioned stimulus pathway.

References

1.	Rescorla, R. A. A. Rev. Neurosci. 11, 329−352 (1988).
2.	Rescorla, R. A. & Wagner, A. R. in Classical Conditioning II: Current Research and Theory (eds Black, A. H. & Prokasy, W. F.) 64−99 (Appleton-Century-Crofts, New York, 1972).
3.	Wagner, A. R. in Information Processing in Animals: Memory Mechanisms (eds Spear, N. E. & Miller, R. R.) 5−47 (Erlbaum, Hillsdale, N J, 1981).
4.	Hawkins, R. D. & Kandel, E. R. Psychol. Rev. 91, 375−391 (1984).
5.	Menzel, R. & Bitterman, M. E. in Neuroethology and Behavioral Physiology (eds Huber, F. & Markel, H.) 206−215 (Springer, Berlin, 1988).
6.	Menzel, R. in Nerobiology of Comparative Cognition (eds Kesner, R. P. & Olton, D. S.) 237−292 (Erlbaum, Hillsdale, NJ, 1990).
7.	Bitterman, M. E., Menzel, R., Fietz, A. & Schäfer, S. J. comp. Physiol. A97, 107−119 (1983).
8.	Smith, B. H. J. exp. Biol. 161, 367−382 (1991).
9.	Arnold, G., Masson, C. & Budharugsa, S. Cell Tissue Res. 242, 593−605 (1985).
10.	Mobbs, P. Phil. Trans. R. Soc. B298, 309−354 (1982).
11.	Menzel, R., Greggers, U. & Hammer, M. in Insect Learning: Ecological and Evolutionary Perceptives (eds Papaj, D. R. & Lewis, A. C.) 79−125 (Chapman & Hall, New York, London, 1993).
12.	Rehder, V. J. Insect Physiol. 33, 303−311 (1987).
13.	Mackey, S. L., Kandel, E. R. & Hawkins, R. D. J. Neurosci. 9, 4227−4235 (1989).
14.	Mauk, M. D., Steinmetz, J. E. & Thompson, R. F. Proc. natn. Acad. Sci. U.S.A. 83, 5349−5353 (1986).
15.	Farley, J. Behavl Neurosci. 101, 28−56 (1987).
16.	Erber, J., Mazur, T. & Menzel, R. Physiol. Entomol. 5, 343−358 (1980).
17.	Mauelshagen, J. J. Neurophysiol. 69, 609−625 (1993).
18.	Heisenberg, M., Borst, A., Wagner, S. & Byers, D. J. Neurogenet. 2, 1−30 (1985).
19.	Balling, A., Technau, G. M. & Heisenberg, M. J. Neurogenet. 4, 65−73 (1987).
20.	Nighorn, A., Healy, M. J. & Davis, R. L. Neuron 6, 455−467 (1991).
21.	Han, P.-L., Levin, L. R., Reed, R. R. & Davis, R. L. Neuron 9, 619−627 (1992).
22.	Buonomano, D. V., Baxter, D. A. & Byrne, J. H. Neural Networks 3, 507−523 (1990).
23.	Hawkins, R. D. in Computational Models of Learning in Simple Neural Systems (eds Hawkins, R. D. & Bower, G. H.) 65−108 (Academic, San Diego, 1989).
24.	Rybak, J. & Menzel, R. J. comp. Neurol., 334, 444−465 (1993).
25.	Rehder, V. J. comp. Neurol. 279, 499−513 (1989).
26.	Strausfeld, N. Atlas of an Insect Brain (Springer, Berlin, Heidelberg, New York, 1976).