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

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 forms1–4. 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 conditioning6–8. 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.

[1]  W. F. Prokasy,et al.  Classical conditioning II: Current research and theory. , 1972 .

[2]  N. Strausfeld Atlas of an Insect Brain , 1976, Springer Berlin Heidelberg.

[3]  R. Menzel,et al.  Localization of short‐term memory in the brain of the bee, Apis mellifera , 1980 .

[4]  P. Mobbs The Brain of the Honeybee Apis Mellifera. I. The Connections and Spatial Organization of the Mushroom Bodies , 1982 .

[5]  H. Markl,et al.  Neuroethology and Behavioral Physiology: Roots and Growing Points , 1983 .

[6]  Ralph R. Miller,et al.  Information processing in animals : memory mechanisms , 1983 .

[7]  E. Kandel,et al.  Is there a cell-biological alphabet for simple forms of learning? , 1984 .

[8]  A Borst,et al.  Drosophila mushroom body mutants are deficient in olfactory learning. , 1985, Journal of neurogenetics.

[9]  R. F. Thompson,et al.  Classical conditioning using stimulation of the inferior olive as the unconditioned stimulus. , 1986, Proceedings of the National Academy of Sciences of the United States of America.

[10]  M. Heisenberg,et al.  ARE THE STRUCTURAL CHANGES IN ADULT DROSOPHILA MUSHROOM BODIES MEMORY TRACES? STUDIES ON BIOCHEMICAL LEARNING MUTANTS , 2007, Journal of neurogenetics.

[11]  V. Rehder Quantification of the honeybee's proboscis reflex by electromyographic recordings , 1987 .

[12]  R. Rescorla Behavioral studies of Pavlovian conditioning. , 1988, Annual review of neuroscience.

[13]  V. Rehder Sensory pathways and motoneurons of the proboscis reflex in the suboesophageal ganglion of the honey bee , 1989, The Journal of comparative neurology.

[14]  Gordon H. Bower,et al.  Computational models of learning in simple neural systems , 1989 .

[15]  R. Hawkins,et al.  Identified serotonergic neurons LCB1 and RCB1 in the cerebral ganglia of Aplysia produce presynaptic facilitation of siphon sensory neurons , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[16]  R. Hawkins A Biologically Based Computational Model for Several Simple Forms of Learning , 1989 .

[17]  D. Olton,et al.  Neurobiology of Comparative Cognition , 1990 .

[18]  Douglas A. Baxter,et al.  Small networks of empirically derived adaptive elements simulate some higher-order features of classical conditioning , 1990, Neural Networks.

[19]  B. Smith The Olfactory Memory of the Honeybee Apis Mellifera: I. Odorant Modulation of Short- and Intermediate-Term Memory After Single-Trial Conditioning , 1991 .

[20]  Ronald L. Davis,et al.  The cyclic AMP phosphodiesterase encoded by the drosophila dunce gene is concentrated in the mushroom body neuropil , 1991, Neuron.

[21]  Ronald L. Davis,et al.  Preferential expression of the drosophila rutabaga gene in mushroom bodies, neural centers for learning in insects , 1992, Neuron.

[22]  R. Menzel,et al.  Anatomy of the mushroom bodies in the honey bee brain: The neuronal connections of the alpha‐lobe , 1993, The Journal of comparative neurology.

[23]  M. Hammer,et al.  Functional Organization of Appetitive Learning and Memory in a Generalist Pollinator, the Honey Bee , 1993 .

[24]  J. Mauelshagen,et al.  Neural correlates of olfactory learning paradigms in an identified neuron in the honeybee brain. , 1993, Journal of neurophysiology.