Mushroom bodies of the cockroach: Activity and identities of neurons recorded in freely moving animals

This article describes novel attributes of the mushroom bodies of cockroaches revealed by recording from neurons in freely moving insects. The results suggest several hitherto unrecognized functions of the mushroom bodies: extrinsic neurons that discriminate between imposed and self‐generated sensory stimulation, extrinsic neurons that monitor motor actions, and a third class of extrinsic neurons that predict episodes of locomotion and modulate their activity depending on the turning direction. Electrophysiological units have been correlated with neurons that were partially stained by uptake of copper ions and silver intensification. Neurons so revealed correspond to Golgi‐impregnated or Lucifer yellow‐filled neurons and demonstrate that their processes generally ascend to other areas of the protocerebrum. The present results support the idea of multiple roles for the mushroom bodies. These include sensory discrimination, the integration of sensory perception with motor actions, and, as described in the companion article, a role in place memory. J. Comp. Neurol. 402:501–519, 1998. © 1998 Wiley‐Liss, Inc.

[1]  F. C. Kenyon.  The Meaning and Structure of the So-Called "Mushroom Bodies" of the Hexapod Brain , 1896, The American Naturalist.

[2]  D. Bodian.  A new method for staining nerve fibers and nerve endings in mounted paraffin sections , 1936 .

[3]  W. Kloot,et al.  COCOON CONSTRUCTION BY THE CECROPIA SILKWORM III. THE ALTERATION OF SPINNING BEHAVIOR BY CHEMICAL AND SURGICAL TECHNIQUES , 1954 .

[4]  T. Narahashi,et al.  The effects of potassium and sodium ions on the resting and action potentials of the cockroach giant axon , 1959 .

[5]  Franz Huber.  Auslösung von Bewegungsmustern durch elektrische Reizung des Oberschlundganglions bei Orthopteren (Saltatoria: Gryllidae, Acridiidae) , 1959 .

[6]  D. Vowles,et al.  OLFACTORY LEARNING AND BRAIN LESIONS IN THE WOOD ANT (FORMICA RUFA). , 1964, Journal of comparative and physiological psychology.

[7]  P. Howse.  Design and Function in the Insect Brain , 1974 .

[8]  J. S. Altman,et al.  A silver intensification method for cobalt-filled neurones in wholemount preparations , 1977, Brain Research.

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

[10]  G. E. Gregory.  The Bodian Protargol Technique , 1980 .

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

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

[13]  Nicholas J. Strausfeld,et al.  Organizational principles of outputs from Dipteran brains , 1984 .

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

[15]  W. Gronenberg.  Anatomical and physiological properties of feedback neurons of the mushroom bodies in the bee brain. , 1987, Experimental biology.

[16]  W. Gronenberg,et al.  Descending neurons supplying the neck and flight motor of diptera: Organization and neuroanatomical relationships with visual pathways , 1990, The Journal of comparative neurology.

[17]  J. Erber,et al.  FMRFamide-like immunoreactivity in the brain of the honeybee (Apis mellifera). A light- and electron microscopical study , 1990, Neuroscience.

[18]  H. Gee.  Something completely different , 1992, Nature.

[19]  Cole Gilbert,et al.  Small‐field neurons associated with oculomotor and optomotor control in muscoid flies: Functional organization , 1992, The Journal of comparative neurology.

[20]  Gordon M. Shepherd,et al.  Modules for molecules , 1992, Nature.

[21]  Ronald L. Davis.  Mushroom bodies and drosophila learning , 1993, Neuron.

[22]  J. Boeckh,et al.  Connections between the deutocerebrum and the protocerebrum, and neuroanatomy of several classes of deutocerebral projection neurons in the brain of male Periplaneta americana , 1993, The Journal of comparative neurology.

[23]  Nicholas J. Strausfeld,et al.  A new role for the insect mushroom bodies: place memory and motor control , 1993 .

[24]  C. Strambi,et al.  Neurogenesis in an adult insect brain and its hormonal control , 1994, Nature.

[25]  R. Menzel,et al.  Development and experience lead to increased volume of subcompartments of the honeybee mushroom body. , 1994, Behavioral and neural biology.

[26]  JF Ferveur,et al.  Genetic feminization of brain structures and changed sexual orientation in male Drosophila , 1995, Science.

[27]  E. Kandel,et al.  Neuropeptides, adenylyl cyclase, and memory storage. , 1995, Science.

[28]  G. Robinson,et al.  Effects of experience and juvenile hormone on the organization of the mushroom bodies of honey bees. , 1995, Journal of neurobiology.

[29]  N. Strausfeld,et al.  Subdivision of the drosophila mushroom bodies by enhancer-trap expression patterns , 1995, Neuron.

[30]  N. Strausfeld,et al.  Morphology and sensory modality of mushroom body extrinsic neurons in the brain of the cockroach, Periplaneta americana , 1997, The Journal of comparative neurology.

[31]  D. Yamamoto,et al.  The Drosophila mushroom body is a quadruple structure of clonal units each of which contains a virtually identical set of neurones and glial cells. , 1997, Development.

[32]  Ryuichi Okada,et al.  Modular structures in the mushroom body of the cockroach , 1997, Neuroscience Letters.

[33]  N. Strausfeld,et al.  Evolution, discovery, and interpretations of arthropod mushroom bodies. , 1998, Learning & memory.

[34]  N. Strausfeld,et al.  The organization of extrinsic neurons and their implications in the functional roles of the mushroom bodies in Drosophila melanogaster Meigen. , 1998, Learning & memory.

[35]  N. Strausfeld,et al.  Mushroom bodies of the cockroach: Their participation in place memory , 1998, The Journal of comparative neurology.

[36]  M. Heisenberg.  What do the mushroom bodies do for the insect brain? an introduction. , 1998, Learning & memory.