Two visual systems in one brain: Neuropils serving the principal eyes of the spider Cupiennius salei

Principal (anterior median) eyes of the wandering spider Cupiennius are served by three successive neuropils, the organization of which is distinct from those serving secondary eyes. Photoreceptors terminate in the first optic neuropil amongst second order neurons with overlapping dendritic fields. Second order neurons terminate at various depths in anterior median eye medulla where they are visited by bush‐like dendritic trees of third order projection neurons. These supply tracts which extend into the “central body.” This crescent‐shaped neuropil lies midsagittally in the rear of the brain near its dorsal surface. It is organized into columns and it supplies both columnar and tangential efferents to other brain centers. The supply to and organization of the “central body” neuropil is reminiscent of retinotopic neuropils supplying the lobula of insects. Channels to the “central body” comprise one of two concurrent visual pathways, the other provided by the secondary eyes supplying the “mushroom body.” We suggest that principal eye pathways may be involved in form and texture perception whereas secondary eyes detect motion, as is known for jumping spiders. Our data do not support Hanström's classical view that the “central body” is specifically associated with web‐building, nor that it is homologous to its namesake in insect brains. © 1993 Wiley‐Liss, Inc.

[1]  M F Land,et al.  Movements of the retinae of jumping spiders (Salticidae: dendryphantinae) in response to visual stimuli. , 1969, The Journal of experimental biology.

[2]  T. S. Collett,et al.  Eidetic images in insects: their role in navigation , 1982, Trends in Neurosciences.

[3]  A. D. Blest The Fine Structure of Spider Photoreceptors in Relation to Function , 1985 .

[4]  Friedrich G. Barth,et al.  Neuroethology of the Spider Vibration Sense , 1985 .

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

[6]  Michael F. Land,et al.  The Morphology and Optics of Spider Eyes , 1985 .

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

[8]  I A Meinertzhagen,et al.  The organization of perpendicular fibre pathways in the insect optic lobe. , 1976, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[9]  K. S. Babu Patterns of Arrangement and Connectivity in the Central Nervous System of Arachnids , 1985 .

[10]  S. Laughlin Neural Principles in the Peripheral Visual Systems of Invertebrates , 1981 .

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

[12]  Martin Egelhaaf,et al.  Visual course control in flies relies on neuronal computation of object and background motion , 1988, Trends in Neurosciences.

[13]  Michael F. Land,et al.  Mechanisms of Orientation and Pattern Recognition by Jumping Spiders (Salticidae) , 1972 .

[14]  Peter Sterling,et al.  Microcircuitry and functional architecture of the cat retina , 1986, Trends in Neurosciences.

[15]  U. Homberg,et al.  Neuroarchitecture of the central complex in the brain of the locust Schistocerca gregaria and S. americana as revealed by serotonin immunocytochemistry , 1991, The Journal of comparative neurology.

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

[17]  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.

[18]  S. Yamashita Photoreceptor Cells in the Spider Eye: Spectral Sensitivity and Efferent Control , 1985 .

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

[20]  B. Hanström The olfactory centers in Crustaceans , 1925 .

[21]  M. Bastiani,et al.  From grasshopper to Drosophila: a common plan for neuronal development , 1984, Nature.

[22]  M. Land Orientation by jumping spiders in the absence of visual feedback. , 1971, The Journal of experimental biology.

[23]  N. Strausfeld,et al.  Neuronal basis for parallel visual processing in the fly , 1991, Visual Neuroscience.

[24]  M. Tabuchi,et al.  Histochemistry of acetylcholine receptors and acetylcholinesterase during the formation of neuromuscular junctions in the urodele Hynobius nigrescens , 1991, Journal of morphology.

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

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

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

[28]  F. Barth,et al.  Neurobiology of Arachnids , 1985, Springer Berlin Heidelberg.

[29]  M. Land,et al.  The physiological optics of Dinopis subrufus L. Koch: A fish-lens in a spider , 1977, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[30]  L G Bishop,et al.  Vertical motion detectors and their synaptic relations in the third optic lobe of the fly. , 1981, Journal of neurobiology.

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

[32]  P. Weygoldt Ontogeny of the Arachnid Central Nervous System , 1985 .

[33]  Bertil Hanström Vergleichende Anatomie des Nervensystems der wirbellosen Tiere: unter Berücksichtigung seiner Funktion , 1929, Nature.

[34]  F. Barth Slit Sensilla and the Measurement of Cuticular Strains , 1985 .

[35]  J. Hildebrand,et al.  Structure and function of the deutocerebrum in insects. , 1989, Annual review of entomology.

[36]  N. Strausfeld,et al.  The optic lobes of Lepidoptera. , 1970, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[37]  F. Barth,et al.  The quality of vision in the ctenid spider Cupiennius salei , 1992 .

[38]  Ernst-August Seyfarth,et al.  Spider Proprioception: Receptors, Reflexes, and Control of Locomotion , 1985 .

[39]  M. Colonnier THE TANGENTIAL ORGANIZATION OF THE VISUAL CORTEX. , 1964, Journal of anatomy.

[40]  G. Horridge,et al.  Structure and function in the nervous systems of invertebrates , 1965 .

[41]  D. Bodian The staining of paraffin sections of nervous tissues with activated protargol. The role of fixatives , 1937 .

[42]  K. Hausen The Lobula-Complex of the Fly: Structure, Function and Significance in Visual Behaviour , 1984 .

[43]  A. Spurr A low-viscosity epoxy resin embedding medium for electron microscopy. , 1969, Journal of ultrastructure research.

[44]  Erich Buchner,et al.  [3H]2-Deoxyglucose mapping of odor-induced neuronal activity in the antennal lobes of Drosophila melanogaster , 1984, Brain Research.

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

[46]  L. Forster Target Discrimination in Jumping Spiders (Araneae: Salticidae) , 1985 .

[47]  R. Devoe Dual Sensitivities of Cells in Wolf Spider Eyes at Ultraviolet and Visible Wavelengths of Light , 1972, The Journal of general physiology.

[48]  M F Land,et al.  Structure of the retinae of the principal eyes of jumping spiders (Salticidae: dendryphantinae) in relation to visual optics. , 1969, The Journal of experimental biology.

[49]  Roger C. Hardie,et al.  The photoreceptor array of the dipteran retina , 1986, Trends in Neurosciences.