A new ascending sensory tract to the calyces of the honeybee mushroom body, the subesophageal‐calycal tract

The mushroom bodies of the honeybee are important neuropils for learning and memory. Therefore, knowledge about their input and output connections is essential to understanding how these neuropils function. A newly described input tract to the mushroom body is presented here, which is called the subesophageal‐calycal tract (SCT) and connects the subesophageal ganglion with the calyces of the mushroom bodies. The neuronal somata of the SCT neurons lie in one cluster between the lobula of the optic lobe and a neuropil area that is formed from the fusion of the tritocerebrum and the subesophageal ganglion. Within the subesophageal ganglion, the dendritic fibers of SCT neurons overlap with terminals of sensory neurons from the proboscis 1 . Therefore, we conclude that the SCT neurons might process gustatory and mechanosensory information from the proboscis. Individual SCT neurons receive unilateral input within the subesophageal ganglion and may connect to either the ipsilateral or the contralateral mushroom body. On their way to the mushroom bodies, the SCT neuron axons meet the roots of the antennocerebralis tracts (ACTs) and from this point follow the same path as the median ACT neurons for a short distance. Within the calyces, the SCT neurons innervate two separate areas, a small area within the dorsal collar just below the lip and a part of the basal ring. Double‐labeling experiments show that the projections of the SCT neurons do not overlap with the projections of the olfactory projection neurons and visual projection neurons from the dorsal medulla. The possible function of the SCT neurons and the relation of the SCT to known input tracts of the mushroom bodies in other insects are discussed. J. Comp. Neurol. 465:168–178, 2003. © 2003 Wiley‐Liss, Inc.

[1]  G. Bicker,et al.  Histochemistry of acetylcholinesterase and immunocytochemistry of an acetylcholine receptor‐like antigen in the brain of the honeybee , 1989, The Journal of comparative neurology.

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

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

[4]  A. T. Whitehead,et al.  Electrophysiological responses of galeal contact chemoreceptors of Apis mellifera to selected sugars and electroylytes. , 1976, Journal of insect physiology.

[5]  R. Menzel Searching for the memory trace in a mini-brain, the honeybee. , 2001, Learning & memory.

[6]  N. Strausfeld Organization of the honey bee mushroom body: Representation of the calyx within the vertical and gamma lobes , 2002, The Journal of comparative neurology.

[7]  B. Hansson,et al.  Olfactory protocerebral pathways processing sex pheromone and plant odor information in the male moth Agrotis segetum , 2001, The Journal of comparative neurology.

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

[9]  Manfred Schmidt,et al.  Neurons with dopamine-like immunoreactivity target mushroom body Kenyon cell somata in the brain of some hymenopteran insects , 1999 .

[10]  M. Galić Die sinnesorgane an der glossa, dem epipharynx und dem hypopharynx der arbeiterin von Apis mellifica L. (Insecta, Hymenoptera) , 1971, Zeitschrift für Morphologie der Tiere.

[11]  R. Menzel,et al.  Structure and response patterns of olfactory interneurons in the honeybee, Apis mellifera , 2001, The Journal of comparative neurology.

[12]  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.

[13]  R. Menzel,et al.  GABA‐immunoreactive neurons in the mushroom bodies of the honeybee: An electron microscopic study , 2001, The Journal of comparative neurology.

[14]  M. Hammer,et al.  Learning and memory in the honeybee , 1995 .

[15]  J. Boeckh,et al.  A neuroanatomical study on the organization of the central antennal pathways in insects , 2004, Cell and Tissue Research.

[16]  P. Mobbs Neural networks in the mushroom bodies of the honeybee , 1984 .

[17]  M. J. Weiss Structural patterns in the corpora pedunculata of orthoptera: A reduced silver analysis , 1981, The Journal of comparative neurology.

[18]  J. Hildebrand,et al.  Synaptic organization of the uniglomerular projection neurons of the antennal lobe of the moth Manduca sexta: A laser scanning confocal and electron microscopic study , 1997, The Journal of comparative neurology.

[19]  M. Hammer An identified neuron mediates the unconditioned stimulus in associative olfactory learning in honeybees , 1993, Nature.

[20]  M. Hammer,et al.  Multiple sites of associative odor learning as revealed by local brain microinjections of octopamine in honeybees. , 1998, Learning & memory.

[21]  D. J. Aidley Nervous system : structure and motor function , 1985 .

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

[23]  F. C. Kenyon The brain of the bee. A preliminary contribution to the morphology of the nervous system of the arthropoda , 1896 .

[24]  F. Schürmann,et al.  Synaptic Connectivity in the Mushroom Bodies of the Honeybee Brain: Electron Microscopy and Immunocytochemistry of Neuroactive Compounds , 1987 .

[25]  I. Meinertzhagen,et al.  Synaptic organization of the mushroom body calyx in Drosophila melanogaster , 2002, The Journal of comparative neurology.

[26]  M. Hammer,et al.  Learning and memory in the honeybee. , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[27]  A. T. Whitehead Electrophysiological response of honey bee labial palp contact chemoreceptors to sugars and electrolytes , 1978 .

[28]  A. T. Whitehead,et al.  Ultrastructure of the contact chemoreceptors of Apis mellifera L. (Hymenoptera : Apidae) , 1976 .

[29]  W. Gronenberg Physiological and anatomical properties of optical input-fibres to the mushroom body in the bee brain , 1986 .

[30]  J. Boeckh,et al.  A neuroanatomical study on the organization of the central antennal pathways in insects , 1977, Cell and Tissue Research.

[31]  W. Gronenberg Subdivisions of hymenopteran mushroom body calyces by their afferent supply , 2001, The Journal of comparative neurology.

[32]  B. Grünewald,et al.  Physiological properties and response modulations of mushroom body feedback neurons during olfactory learning in the honeybee, Apis mellifera , 1999, Journal of Comparative Physiology A.

[33]  Kim,et al.  Effect of an amino acid on feeding preferences and learning behavior in the honey bee, Apis mellifera. , 2000, Journal of insect physiology.

[34]  B. K. Mitchell,et al.  Peripheral and central structures involved in insect gustation , 1999, Microscopy research and technique.

[35]  D. Vowles The Structure and Connexions of the Corpora Pedunculata in Bees and Ants , 1955 .

[36]  R. Menzel,et al.  Learning and memory in honeybees: from behavior to neural substrates. , 1996, Annual review of neuroscience.

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

[38]  W. Gronenberg,et al.  Segregation of visual input to the mushroom bodies in the honeybee (Apis mellifera) , 2002, The Journal of comparative neurology.