Summary
This paper describes the morphology and response characteristics of two types of paired descending neurons (DNs) (classified as DNVII1 and DNIV1) and two lobula neurons (HR1 and HP1) in the honeybee, Apis mellifera.
-
1.
The terminal arborizations of the lobula neurons are in juxtaposition with the dendritic branches of the DNs (Figs. 2, 3b, 5). Both of the DNs descend into the ipsilateral side of the thoracic ganglia via the dorsal intermediate tract (Fig. 6) and send out many blebbed terminal branches into the surrounding motor neuropil (Figs. 3c, 7).
-
2.
Both the lobula and descending neurons respond in a directionally selective manner to the motion of widefield, periodic square-wave gratings.
-
3.
The neurons have broad directional tuning curves (Figs. 10, 11). HR1 is maximally sensitive to regressive (back-to-front) motion and HP1 is maximally sensitive to progressive (front-to-back) motion over the ipsilateral eye (Fig. 11). DNVII1 is maximally sensitive when there is simultaneous regressive motion over the ipsilateral eye and progressive motion over the contralateral eye (Fig. 12a). Conversely, DNIV1 is optimally stimulated when there is simultaneous progressive motion over the ipsilateral eye and regressive motion over the contralateral eye (Fig. 12b).
-
4.
The response of DNIV1 is shown to depend on the contrast frequency (CF) rather than the angular velocity of the periodic gratings used as stimuli. The peak responses of both regressive and progressive sensitive DNs are shown to occur at CFs of 8–10 Hz (Figs. 13, 14).
Similar content being viewed by others
Abbreviations
- DN :
-
descending neuron
- CF :
-
contrast frequency (temporal frequency)
- λ sp :
-
spatial wavelength
- POT I :
-
posterior optic tract I
- POT II :
-
posterior optic tract II
References
Altman JS, Shaw MK, Tyrer NM (1980) Input synapses on to a locust sensory neuron revealed by cobalt-electron microscopy. Brain Res 189:245–250
Bacon JP, Altman JS (1977) A silver intensification method for cobalt-filled neurones in wholemount peparations. Brain Res 138:359–363
Buchner E (1984) Behavioral analysis of spatial vision in insects. In: Ali MA (ed) Photoreception and vision in invertebrates. Plenum Press, New York London, Series 74, pp 561–622
Carpenter RHS (1977) Movements of the eyes. PION Ltd, London
Collett TS, King AJ (1975) Vision during flight. In: Horridge GA (ed) The compound eye and vision of insects. Clarendon Press, Oxford, pp 437–466
DeVoe RD, Kaiser W, Ohm J, Stowe LS (1982) Horizontal movement detectors of honeybee: Directionally-selective visual neurons in the lobula and brain. J Comp Physiol 147:155–170
Egelhaaf M, Hausen K, Reichardt W, Wehrhahn C (1988) Visual course control in flies relies on neuronal computation of object and background motion. Trends Neurosci 11:351–358
Fermi G, Reichardt W (1963) Optomotorische Reaktionen der Fliege Musca domestica. Abhängigkeit der Reaktion von der Wellenlänge, der Geschwindigkeit, dem Kontrast und der mittleren Leuchtdichte bewegter periodischer Muster. Kybernetik 2:15–18
Florkin M, Jeuniaux C (1964) Haemolymph composition. In: Rockstein M (ed) The physiology of insects. Academic Press, New York, pp 109–152
Goodman LJ, Fletcher WA, Guy RG, Mobbs PG, Pomfrett CJD (1987) Motion sensitive descending interneurons, ocellar LD neurons and neck motor neurons in the bee: a neural substrate for visual course control in Apis mellifera. In: Menzel R, Mercer A (eds) Neurobiology and behaviour of honeybees. Springer, Berlin Heidelberg New York, pp 158–171
Götz KG, Hengstenberg B, Biesinger R (1979) Optomotor control of wing beat and body posture in Drosophila. Biol Cybern 35:101–112
Hausen K (1976) Functional characterization and anatomical identification of motion sensitive neurons in the lobula plate of the blowfly Calliphora erythrocephala. Z Naturforsch 31c:629–633
Hausen K (1982) Motion sensitive interneurons in the optomotor system of the fly. II. The horizontal cells: receptive field organization and response characteristics. Biol Cybern 46:67–79
Hausen K (1984) The lobula plate complex of the fly: structure, function and significance in visual behavior. In: Ali MA (ed) Photoreception and vision in invertebrates. Plenum Press, New York London, Series 74, pp 523–560
Hausen K, Wolburg-Bucholz K, Ribi WA (1980) The synaptic organization of visual interneurons in the lobula complex of flies. A light and electron microscopical study using silver-intensified cobalt-impregnations. Cell Tissue Res 208:371–387
Held R, Dichgars J, Bauer J (1975) Characteristics of moving visual scenes in influencing spatial orientation. Vision Res 15:357–365
Hensler K (1988) The pars intercerebralis neurone PI(2)5 of locusts: Convergent processing of inputs reporting head movements and deviations from straight flight. J Exp Biol 140:511–533
Hertel H, Maronde UK (1987) The physiology and morphology of centrally projecting visual interneurones in the honeybee brain. J Exp Biol 133:301–315
Hoffmann KP, Haber HP, Morkner C, Mayr M (1982) The role of central and peripheral retina in eliciting optokinetic nystagmus in cats. In: Roucous A, Crommelinck M (eds) Physiological and pathological aspects of eye movements. Junk, The Hague, pp 181–186
Ibbotson MR, Goodman LJ (1990) Response characteristics of four wide-field motion-sensitive descending interneurones in Apis mellifera. J Exp Biol 148:255–279
Kaiser W, Bishop LG (1970) Directionally selective motion detecting units in the optic lobe of the honey-bee. Z Vergl Physiol 67:403–413
Kunze P (1961) Untersuchung des Bewegungssehens fixiert fliegender Bienen. Z Vergl Physiol 44:656–684
Kuo BC (1963) Automatic control systems. Prentice-Hall, New Jersey Tokyo
Land MF (1975) Head movements and fly vision. In: Horridge GA (ed) The compound eye and vision in insects. Clarendon Press, Oxford, pp 469–489
Maddess T, Laughlin SB (1985) Adaptation of the motion-sensitive neuron H1 is generated locally and governed by contrast frequency. Proc R Soc Lond B 225:251–275
Maronde U (1988) Strukturelle und funktionelle Charakterisierung visueller Interneuronen-Populationen im Protocerebrum der Honigbiene Apis mellifera. PhD Thesis Berlin
Milde JJ, Strausfeld NJ (1986) Visuo-motor pathways in arthropods. Naturwissenschaften 73:151–154
Milde JJ, Seyan HS, Strausfeld NJ (1987) The neck motor system of the fly Calliphora erythrocephala. II. Sensory organization. J Comp Physiol A 160:225–238
Milde JJ, Gronenberg W, Strausfeld NJ (1990) The head-neck system of the blowfly Calliphora: functional organization and comparison with the sphinx moth Manduca sexta. In: Berthoz A, Graf W, Vidal PP (eds) Proceedings of the 2nd Headneck Symposium. Oxford Univ Press, Oxford (in press)
Mobbs PG (1984) Neural networks in the mushroom bodies. J Insect Physiol 30:43–58
Mobbs PG (1985) Brain structure. In: Kerkut GA, Gilbert LI (eds) Comprehensive insect physiology, biochemistry and pharmacology. Pergamon Press, Oxford, pp 299–369
Pan KC (1980) The neural organization of the ocellar system and associated pathways in the central nervous system of the worker honeybee. PhD Thesis London
Patterson JA, Pomfrett CJD (1988) A BBC microcomputer-based system for the on-line determination of directional selectivity in visual motion-sensitive neurones of the honeybee. J Physiol 399:2P
Rehder V (1988) A neuroanatomical map of the suboesophageal and prothoracic ganglia of the honey bee (Apis mellifera). Proc R Soc Lond B 235:179–202
Reichert H, Rowell CHF, Griss C (1985) Course correction circuitry translates feature detection into behavioural action in locusts. Nature 31:142–144
Rind FC (1983a) A directionally-selective motion detection neuron in the brain of a moth. J Exp Biol 102:253–271
Rind FC (1983b) The role of an identified brain neurone in mediating optomotor movements in a moth. J Exp Biol 102:273–284
Robert D (1988) Visual steering under closed-loop conditions by flying locusts: flexibility of optomotor response and mechanisms of correctional steering. J Comp Physiol 164:15–24
Rowell CHF, Reichert H (1986) Three descending interneurones reporting deviation from course in the locust. II. Physiology. J Comp Physiol A 158:775–794
Sandeman D (1977) Compensatory eye movements in crabs. In: Hoyle G (ed) Identified neurons and behavior of arthropods. Plenum, New York London, pp 131–147
Simmons PJ (1980) A locust wind and ocellar brain neurone. J Exp Biol 85:281–294
Strausfeld NJ (1976) Atlas of an insect brain. Springer, Berlin Heidelberg New York
Strausfeld NJ, Bacon JP (1983) Multimodal convergence in the central nervous system of dipterous insects. In: Horn E (ed) Multimodel convergence in sensory systems. Fortschr Zool 28. G Fischer, Stuttgart New York, pp 47–76
Strausfeld NJH, Bassemir U (1983) Cobalt coupled neurons of a giant fibre system in Diptera. J Neurocytol 12:971–991
Strausfeld NJ, Bassemir U (1985a) Lobula plate and ocellar interneurons converge onto a cluster of descending neurons leading to neck and leg motor neuropile in Calliphora erythrocephala. Cell Tissue Res 240:617–640
Strausfeld NJ, Bassemir U (1985b) The organization of giant horizontal-motion-sensitive neurons and their synaptic relationship in the lateral deutocerebrum of Calliphora erythrocephala and Musca domestica. Cell Tissue Res 242:531–550
Strausfeld NJ, Seyan HS, Milde JJ (1987) The neck motor system of the fly Calliphora erythrocephala I, II. J Comp Physiol A 160:205–238
Watson AHD, Burrows M (1982) The ultrastructure of identified locust motor neurones and their synaptic relationship. J Comp Neurol 205:383–397
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Ibbotson, M.R. Wide-field motion-sensitive neurons tuned to horizontal movement in the honeybee, Apis mellifera . J Comp Physiol A 168, 91–102 (1991). https://doi.org/10.1007/BF00217107
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00217107