Summary
We have used specific antisera against protein-conjugatedγ-aminobutyric acid (GABA) in immunocytochemical preparations to investigate the distribution of putatively GABAergic neurons in the brain and suboesophageal ganglion of the sphinx mothManduca sexta. About 20000 neurons per brain hemisphere exhibit GABA-immunoreactivity. Most of these are optic-lobe interneurons, especially morphologically centrifugal neurons of the lamina and tangential neurons that innervate the medulla or the lobula complex. Many GABA-immunoreactive neurons, among them giant fibers of the lobula plate, project into the median protocerebrum. Among prominent GABA-immunoreactive neurons of the median protocerebrum are about 150 putatively negative-feedback fibers of the mushroom body, innervating both the calyces and lobes, and a group of large, fan-shaped neurons of the lower division of the central body. Several commissures in the supra- and suboesophageal ganglion exhibit GABA-immunoreactivity. In the suboesophageal ganglion, a group of contralaterally descending neurons shows GABA-like immunoreactivity. The frontal ganglion is innervated by immunoreactive processes from the tritocerebrum but does not contain GABA-immunoreactive somata. With few exceptions the brain nerves do not contain GABA-immunoreactive fibers.
Similar content being viewed by others
References
Abercrombie M (1946) Estimation of nuclear population from microtome sections. Anat Rec 94:239–247
Adams ME, O'Shea M (1983) Peptide cotransmitter at a neuromuscular junction. Science 221:286–289
Arnett DW (1972) Spatial and temporal integration properties of units in the first optic ganglion of dipterans. J Neurophysiol 35:429–444
Bacon JP (1980) An homologous interneurone in a locust, a cricket and a mantid. Verh Dtsch Zool Ges 73:300
Bell RA, Borg TK, Ittycheriak PI (1974) Neurosecretory cells in the frontal ganglion of the tobacco hornwormManduca sexta. J Insect Physiol 20:669–678
Bell RA, Joachim FA (1976) Techniques for rearing laboratory colonies of tobacco hornworms and pink bollworms. Ann Entomol Soc Am 69:365–373
Bethe A (1897) Vergleichende Untersuchungen über die Funktionen des Centralnervensystems der Arthropoden. Pflügers Arch 68:449–545
Bicker G, Schäfer S, Kingan TK (1985) Mushroom body feedback interneurons in the honeybee show GABA-like immunoreactivity. Brain Res 360:394–397
Bishop CA, O'Shea M (1982) Neuropeptide proctolin (H-Arg-Try-Leu-Pro-Thr-OH): Immunocytochemical mapping of neurons in the central nervous system of the cockroach. J Comp Neurol 207:223–238
Bishop CA, O'Shea M (1983) Serotonin immunoreactive neurons in the central nervous system of an insect (Periplaneta Americana). J Neurobiol 14:251–269
Boeckh J, Ernst KD, Sass H, Waldow U (1984) Anatomical and physiological characteristics of individual neurons in the central antennal pathway of insects. J Insect Physiol 30:15–26
Borg TK, Bell RA, Picard DJ (1973) Ultrastructure of neurosecretory cells in the frontal ganglion of the tobacco hornwormManduca sexta (L). Tissue Cell 5:259–267
Callec JJ (1974) Synaptic transmission in the central nervous system of insects. In: Treherne JE (ed) Insect neurobiology. Elsevier, Amsterdam, pp 119–185
Christensen TA, Waldrop BR, Hildebrand JG (1985) GABA-mediated inhibition in the antennal lobes of the mothManduca sexta. Soc Neurosci Abstr 11:163
Curtis DR, Johnston GAR (1974) Amino acid transmitters in the mammalian central nervous system. Ergebn Physiol 69:97–188
DeVoe R (1980) Movement sensitivities of cells in the fly's medulla. J Comp Physiol A 138:93–119
Duve H, Thorpe A (1984a) Immunocytochemical mapping of gastrin/CCK-like peptides in the neuroendocrine system of the blowflyCalliphora vormitoria (Diptera). Cell Tissue Res 237:309–320
Duve H, Thorpe A (1984b) Comparative aspects of insect-vertebrate neurohormones. In: Bořkovec AB, Kelly TJ (eds) Insect neurochemistry and neurophysiology. Plenum, New York, pp 171–196
El-Salhy M, Falkmer S, Kramer KJ, Speirs RD (1983) Immunohistochemical investigations of neuropeptides in the brain, corpora cardiaca, and corpora allata of an adult lepidopteran insect,Manduca sexta L. Gen Comp Endocrinol 54:85–88
El-Salhy M, Falkmer S, Kramer KJ, Speirs RD (1984) Immunocytochemical evidence for the occurrence of insulin in the frontal ganglion of a lepidopteran insect, the tobacco hormworm moth,Manduca sexta L. Gen Comp Endocrinol 54:85–88
Erber J (1982) Electrophysiological analysis of central neurons in the bee and correlations with behavior. In: Breed MD, Michener CD, Evans HE (eds) The biology of social insects. Westview, Boulder, pp 343–346
Erber J, Masuhr T, Menzel R (1980) Localization of short-term memory in the brain of the beeApis mellifera. Physiol Entomol 5:343–358
Erber J, Homberg U, Gronenberg W (1987) The functional roles of the mushroom bodies in insects. In: Gupta AP (ed) Arthropod brain: its evolution, development, structure and functions. Wiley, New York (in press)
Gerschenfeld HM (1973) Chemical transmission in invertebrate central nervous system and neuromuscular junctions. Physiol Rev 53:1–118
Goll W (1967) Strukturuntersuchungen am Gehirn vonFormica. Z Morphol Ökol Tiere 59:143–210
Graham D (1985) Pattern and control of walking in insects. Adv Insect Physiol 18:31–132
Goodman L, Mobbs P, Guy R (1982) Descending neurons in the brain and thorax of the honeybee. In: Breed MD, Michener CD, Evans HE (eds) The biology of social insects. Westview, Boulder, p 396
Gronenberg W (1984) Das Protocerebrum der Honigbiene im Bereich des Pilzkörpers — eine neurophysiologisch-anatomische Charakterisierung. PhD Dissertation, Berlin
Harrow ID, Hildebrand JG (1982) Synaptic interactions in the olfactory lobe of the mothManduca sexta. Soc Neurosci Abstr 8:528
Hausen K (1984) The lobula complex of the fly: structure, function and significance in visual behaviour. In: Ali MA (ed) Photoreception and vision in invertebrates. Plenum, New York, pp 523–560
Heisenberg M, Borst A, Wagner S, Byers D (1985)Drosophila mushroom body mutants are deficient in olfactory learning. J Neurogenet 2:1–30
Hertel H (1980) Chromatic properties of identified interneurons in the optic lobes of the bee. J Comp Physiol 137:215–231
Homberg U (1982) Das mediane Protocerebrum der Honigbiene (Apis mellifica) im Bereich des Zentralkörpers: Physiologische und morphologische Charakterisierung. PhD Dissertation, Berlin
Homberg U (1984) Processing of antennal information in extrinsic mushroom body neurons of the bee brain. J Comp Physiol A 154:825–836
Homberg U (1985) Interneurons of the central complex in the bee brain (Apis mellifica, L.) J Insect Physiol 31:251–264
Homberg U (1987) Structure and functions of the central complex in insects. In: Gupta AP (ed) Arthropod brain: its evolution, development, structure and functions. Wiley, New York (in press)
Homberg U, Erber J (1979) Response characteristics and identification of extrinsic mushroom body neurons of the bee. Z Naturforsch 34:612–615
Homberg U, Hoskins SG, Hildebrand JG (1985) Immunocytochemical mapping of peptides in the brain and suboesophageal ganglion ofManduca sexta. Soc Neurosci Abstr 11:942
Honegger H-W (1980) Receptive fields of sustained medulla neurons in crickets. J Comp Physiol 136:191–201
Hoskins SG, Homberg U, Kingan TG, Hildebrand JG (1985) Neurochemical anatomy of the brain of the sphinx mothManduca sexta. In: Neuropharmacology and pesticide action (Neurotox 85). Soc Chem Industry, London, pp 84–87
Hoskins SG, Homberg U, Kingan TG, Christensen TA, Hildebrand JG (1986) Immunocytochemistry of GABA in the antennal lobes of the sphinx mothManduca sexta. Cell Tissue Res 244:243–252
Huber F (1955) Sitz und Bedeutung nervöser Zentren für Instinkthandlungen beim Männchen vonGryllus campestris L. Z Tierpsychol 12:12–48
Huber F (1960a) Experimentelle Untersuchungen zur nervösen Atmungsregulation der Orthopteren (Saltatoria, Gryllidae). Z Vgl Physiol 43:359–391
Huber F (1960b) Untersuchungen über die Funktion des Zentralnervensystems und insbesondere des Gehirns bei der Fortbewegung und Lauterzeugung der Grillen. Z Vgl Physiol 44:60–132
Huber F (1962) Lokalisation und Plastizität im Zentralnervensystem der Tiere. Zool Anz [Suppl] 26, Verh Dtsch Zool Ges 1962:200–267
Huber F (1983) Neural correlates of orthopteran and cicada phonotaxis. In: Huber F, Markl H (eds) Neuroethology and behavioral physiology. Springer, Berlin Heidelberg New York, pp 108–135
Kenyon FC (1896) The brain of the bee. A preliminary contribution to the morphology of the nervous system of the Arthropoda. J Comp Neurol 6:133–210
Kien J, Menzel R (1977a) Chromatic properties of interneurons in the optic lobes of the bee. I. Broad band neurons. J Comp Physiol 113:17–34
Kien J, Menzel R (1977b) Chromatic properties of interneurons in the optic lobes of the bee. II. Narrow band and colour opponent neurons. J Comp Physiol 113:35–53
Kingan TG, Hildebrand JG (1985)γ-Aminobutyric acid in the central nervous system of metamorphosing and matureManduca sexta. Insect Biochem 15:667–675
Klemm N (1983) Detection of serotonin-containing neurons in the insect central nervous system by antibodies to 5-HT. In: Strausfeld NJ (ed) Functional neuroanatomy. Springer, Berlin Heidelberg New York, pp 302–316
Klemm N, Steinbusch WM, Sundler F (1984) Distribution of serotonin-containing neurons and their pathways in the suboesophageal ganglion of the cockroachPeriplaneta americana (L) as revealed by immunocytochemistry. J Comp Neurol 225:387–395
Laughlin SB (1981) Neural principles in the peripheral visual system of invertebrates. In: Autrum H, Jung R, Loewenstein WR, MacKay DM, Teuber HL (eds) Handbook of sensory physiology VII/6B. Springer, Berlin Heidelberg New York, pp 133–280
Levy RA (1977) The role of GABA in primary afferent depolarization. Prog Neurobiol 9:211–267
Matsumoto SG, Hildebrand JG (1981) Olfactory mechanisms in the mothManduca sexta: Response characteristics and morphology of central neurons in the antennal lobes. Proc R Soc Lond [Biol] 213:249–277
Maxwell GD, Tait JF, Hildebrand JG (1978) Regional synthesis of neurotransmitter candidates in the CNS of the mothManduca sexta. Comp Biochem Physiol 61C:109–119
Maynard DM (1956) Electrical activity in cockroach cerebrum. Nature (Lond) 177:529
Menzel R, Erber J, Masuhr T (1974) Learning and memory in the honeybee. In: Barton-Browne L (ed) Experimental analysis of insect behavior. Springer, Berlin Heidelberg New York, pp 195–217
Meyer EP, Matute C, Streit P, Nässel DR (1986) Insect optic lobe neurons identifiable with monoclonal antibodies to GABA. Histochemistry 84:207–216
Mobbs PG (1982) The brain of the honeybeeApis mellifera. I. The connections and spatial organisation of the mushroom bodies. Phil Trans R Soc Lond [Biol] 298:309–354
Nässel DR, Meyer EP, Klemm N (1985) Mapping and ultrastructure of serotonin-immunoreactive neurons in the optic lobes of three insect species. J Comp Neurol 232:190–204
O'Shea M, Evans PD (1979) Potentiation of neuromuscular transmission by an octopaminergic neuron in the locust. J Exp Biol 79:169–190
Pearson L (1971) The corpora pedunculata ofSphinx L. and other Lepidoptera, an anatomical study. Phil Trans R Soc Lond [Biol] 259:477–752
Pierantoni R (1965) A look into the cock-pit of the fly. The architecture of the lobula plate. Cell Tissue Res 171:101–122
Roberts E, Chase TN, Tower DB (1976) GABA in nervous function. Raven Press, New York
Robertson RM, Pearson KG (1985) Neural networks controlling locomotion in insects. In: Selverston (ed) Model neural networks and behavior. Plenum, New York, pp 21–37
Roeder KD (1937) The control of tonus and locomotor activity in the praying mantis (Mantis religiosa L.) J Exp Zool 76:353–374
Riehle A (1981) Color opponent neurons of the honeybee in a heterochromatic flicker test. J Comp Physiol 142:81–88
Rowell CHF, O'Shea M, Williams JLD (1977) The neuronal basis of a sensory analyser, the acridid movement detector system. IV. The preference for small field stimuli. J Exp Biol 68:157–185
Schäfer S, Bicker G (1986) Distribution of GABA-like immunore-activity in the brain of the honeybee. J Comp Neurol 246:287–300
Schildberger K (1983) Local interneurons associated with the mushroom bodies and the central body in the brain ofAcheta domesticus. Cell Tissue Res 230:573–586
Schildberger K (1984) Multimodal interneurons in the cricket brain: properties of identified extrinsic mushroom body cells. J Comp Physiol 154:71–79
Schürmann F-W (1974) Bemerkungen zur Funktion der Corpora pedunculata im Gehirn der Insekten aus morphologischer Sicht. Exp Brain Res 19:406–432
Schürmann F-W, Klemm N (1984) Serotonin-immunoreactive neurons in the brain of the honeybee. J Comp Neurol 225:570–580
Simmonds MA (1984) Physiological and pharmacological characterization of the actions of GABA. In: Bowery NG (ed) Actions and interactions of GABA and benzodiazepines. Raven Press, New York, pp 27–41
Steiger U (1967) Über den Feinbau des Neuropils im Corpus pedunculatum der Waldameise. Z Zellforsch 81:511–536
Sternberger LA (1979) Immunocytochemistry. Wiley, New York
Storm-Mathisen J, Leknes AK, Bore AT, Vaaland JL, Edminson P, Haug FMS, Ottersen OP (1983) First visualization of glutamate and GABA in neurons by immunocytochemistry. Nature (Lond) 301:517–520
Strausfeld NJ (1976) Atlas of an insect brain. Springer, Berlin
Strausfeld NJ (1984) Functional neuroanatomy of the blowfly's visual system. In: Ali MA (ed) Photoreception and vision in invertebrates. Plenum, New York, pp 483–522
Strausfeld NJ, Blest AD (1970) Golgi studies on insects. Part I. The optic lobes of Lepidoptera. Phil Trans R Soc Lond [Biol] 258:81–134
Strausfeld NJ, Nässel DR (1981) Neuroarchitecture serving compound eyes. In: Autrum H, Jung R, Loewenstein WR, MacKay DM, Teuber HL (eds) Handbook of sensory physiology VII/6B Vision in invertebrates. Springer, Berlin Heidelberg New York, pp 1–132
Swihart SL (1968) Single unit activity in the visual pathway of the butterflyHeliconius erato. J Insect Physiol 14:1589–1601
Usherwood PNR (1978) Amino acids as neurotransmitters. Adv Comp Physiol Biochem 7:227–309
Usherwood PNR, Grundfest H (1965) Peripheral inhibition in skeletal muscle of insects. J Neurophysiol 28:497–518
Wadepuhl M (1983) Control of grasshopper singing behavior by the brain: responses to electrical stimulation. Z Tierpsychol 63:173–200
Williams JLD (1972) Some observations on the neuronal organisation of the supra-oesophageal ganglion inSchistocerca gregaria Forskål with particular reference to the central complex. PhD Thesis, University of Wales
Williams JLD (1975) Anatomical studies of the insect central nervous system: A ground-plan of the midbrain and an introduction to the central complex in the locust,Schistocerca gregaria (Orthoptera). J Zool (Lond) 167:67–86
Wilson JA, Phillips CE, Adams ME, Huber F (1982) Structural comparison of a homologous neuron in gryllid and acridid insects. J Neurobiol 13:459–467
Witthöft W (1967) Absolute Zahl und Verteilung der Zellen im Hirn der Honigbiene. Z Morphol Tiere 61:160–184
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Homberg, U., Kingan, T.G. & Hildebrand, J.G. Immunocytochemistry of GABA in the brain and suboesophageal ganglion ofManduca sexta . Cell Tissue Res. 248, 1–24 (1987). https://doi.org/10.1007/BF01239957
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF01239957