Summary
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1.
Intracellular recordings have been made from both input (ipsilateral) and output (contralateral) ends of directionally-selective optomotor neurons in the left lobulae of worker honeybees. Optical stimuli were two, monocular, horizontally-moving vertical gratings placed on opposite sides of the bee's head. The eyes could be stimulated separately or together.
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2.
Horizontal regressive motion-sensitive (HR) cells are strongly excited (and depolarized) by ipsilateral regressive motion. They are moderately excited by contralateral progressive motion but are inhibited by contralateral regressive motion. Ipsilateral progressive motion has little effect (Figs. 1 and 2). The HR cells (HRLeft and HRRight cells) are bilateral, reciprocal neurons which run from one lobula to the other via the anterior optic tracts, the optic tubercles, and the intertubicular tract. They have co-extensive dendrites and terminals in the distal lamellae of the lobulae (Figs. 4–6). HR cells are the bees' optomotor neurons, known hitherto from extracellular recordings.
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3.
Horizontal progressive-motion sensitive (HP) cells (HPRight and HPLeft cells) are excited and depolarized by ipsilateral progressive motion but are inhibited and hyperpolarized by ipsilateral regressive motion. It is uncertain if there are bilateral influences on HP cells (Figs. 7 and 8). No stained HP cells have been recovered.
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4.
Other directionally-selective cells with and without spikes have also been stained and reconstructed (Figs. 9 and 10).
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5.
A model network is proposed between HR and HP cells in which a) HR cells mutually inhibit each other; b) the ipsilateral, input end of each HR cell inhibits the HP cell originating in the same lobula; and c) the contralateral, output terminals of each HP cell excite the HR cell originating in the opposite lobula (Fig. 11 A). It is discussed how the model could explain the observed directional selectivities of cells (Figs. 11B, C and 12). Additionally, the possible role of such a model network in optomotor behavior is considered.
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Abbreviations
- AOT :
-
anterior optic tract
- HP :
-
horizontal progressive motion-sensitive (cells)
- HR :
-
horizontal regressive motion-sensitive (cells)
- LOB :
-
lobula
References
Baumann F, Hadjilazaro B (1972) A depolarizing aftereffect of intense light in the drone visual system. Vision Res 12:17–31
Bishop LG (1970) The spectral sensitivity of motion detector units recorded in the optic lobe of the honeybee. Z Vergl Physiol 70:374–381
Collett T (1971) Connections between wide-field monocular and binocular movement detectors in the brain of a hawk moth. Z Vergl Physiol 75:1–31
Collett T (1972) Visual neurones in the anterior optic tract of the privet hawk moth. J Comp Physiol 78:396–433
DeVoe RD (1980) Movement sensitivities of cells in the fly's medulla. J Comp Physiol 138:93–119
DeVoe RD, Ockleford EM (1976) Intracellular responses from cells of the medulla of the fly,Calliphora erythrocephala. Biol Cybern 23:13–24
DeVoe RD, Kaiser W, Ohm J (1981) Identified horizontal movement detectors in the bee's brain. Invest Ophthalmol Visual Sci 20 (Suppl):180
Dvorak DR, Bishop LG, Eckert HE (1975) On the identification of movement detectors in the fly optic lobe. J Comp Physiol 100:5–23
Eckert H (1980) Functional properties of the Hl-neurone in the third optic ganglion of the blowfly,Phaenicia. J Comp Physiol 135:29–39
Eckert H (1981) The horizontal cells in the lobula plate of the blowfly,Phaenicia sericata. J Comp Physiol 143:511–526
Eckert H, Bishop LG (1978) Anatomical and physiological properties of the vertical cells in the third optic ganglion ofPhaenicia sericata. J Comp Physiol 126:27–86
Erber J (1978) Response characteristics and after effects of multimodal neurons in the mushroom body area of the honeybee. Physiol Entomol 3:77–89
Geiger G, Goulin R, Bücher R (1981) How the two eyes add together: Monocular properties of the visually guided orientation behaviour of flies. Biol Cybern 41:71–78
Guy RG, Goodman LJ, Mobbs PG (1979) Visual interueurones in the bee brain: Synaptic organization and transmission by graded potentials. J Comp Physiol 134:253–264
Hausen K (1976a) Struktur, Funktion und Konnektivität bewegungsempfindlicher Interneuronen im dritten optischen Neuropil der SchmeissfliegeCalliphora erythrocephala. Dissertation Eberhard-Karls-Universität, Tübingen
Hausen K (1976b) Functional characterization and anatomical identification of motion sensitive neurons in the lobula plate of the blowflyCalliphora erythrocephala. Z Naturforsch 31 c:631–633
Heitler WJ, Goodman CS, Rowell CHF (1977) The effects of temperature on the threshold of identified neurons in the locust. J Comp Physiol 117:163–182
Hengstenberg R (1977) Spike responses of “non-spiking” visual interneurone. Nature 270:338–349
Hertl H (1980) Chromatic properties of identified interneurones in the optic lobe of the bee. J Comp Physiol 137:215–231
Jawlowski H (1963) On the origin of corpora pedunculata and the structure of the tuberculum opticum (Insecta). Acta Anat 53:346–359
Jensen R, DeVoe RD (1982) Comparisons of directionally-selective with other ganglion cells of the turtle retina: Intracellular recording and staining (in preparation)
Jonescu CN (1909) Vergleichende Untersuchungen über das Gehirn der Honigbiene. Z Naturwiss 45:11–180
Kaiser W (1972) A preliminary report on the analysis of the optomotor system of the honey bee — single unit recordings during stimulation with spectral lights. In: Wehner R (ed) Information processing in the visual system of arthropods. Springer, Berlin Heidelberg New York, pp 167–170
Kaiser W (1974) The spectral sensitivity of the honeybee's optomotor walking response. J Comp Physiol 90:405–408
Kaiser W (1975) The relationship between visual movement detection and colour vision in insects. In: Horridge GA (ed) The compound eye and vision of insects. Clarendon Press, Oxford, pp 359–377
Kaiser W (1979) Circadian variations in the sensitivity of single visual interneurones of the beeApis mellifica carnica. Verh Dtsch Zool Ges 1979:211
Kaiser W (1982) Sensory and neuronal bases of visually guided behavioural patterns in bees. Insects Soc (in press)
Kaiser W, Bishop LG (1970) Directionally selective motion detecting units in the optic lobe of the honeybee. Z Vergl Physiol 67:403–413
Kaiser W, Liske E (1972) A preliminary report on the analysis of the optomotor system of the bee — behavioral studies with spectral lights. In: Wehner R (ed) Information processing in the visual system of arthropods. Springer, Berlin Heidelberg New York, pp 163–165
Kaiser W, Liske E (1974) Die optomotorischen Reaktionen von fixiert fliegenden Bienen bei Reizung mit Spektrallichtern. J Comp Physiol 89:391–408
Kaiser W, Seidl R, Vollmar J (1977) The participation of all three colour receptors in the phototactic behaviour of fixed walking honeybees. J Comp Physiol 122:27–44
Kaiser W, DeVoe R, Ohm J (1981) The influence of non-optic stimuli on the sensitivity of identified visual interneurons in the optic lobe of the honey bee. Verh Dtsch Zool Ges 1981:173
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 (1977) Chromatic properties of interneurones in the optic lobes of the bee: I. Broad band neurons. J Comp Physiol 113:17–34
Kunze P (1961) Untersuchung des Bewegungssehens fixiert fliegender Bienen. Z Vergl Physiol 44:656–684
Marchiafava PL (1979) The responses of retinal ganglion cells to stationary and moving visual stimuli. Vision Res 19:1203–1211
McCann GD, Foster SF (1971) Binocular interactions of motion detection fibers in the optic lobes of flies. Kybernetik 8:193–203
Menzel R (1973) Spectral response of moving detecting and “sustaining” fibres in the optic lobe of the bee. J Comp Physiol 82:135–150
Mimura K (1971) Movement discrimination by the visual system of flies. Z Vergl Physiol 73:105–138
Nelson R, Famiglietti EV Jr, Kolb H (1978) Intracellular staining reveals different levels of stratification for on- and off-center ganglion cells in cat retina. J Neurophysiol 41:472–483
Norton AL, Spekreijse H, Wagner HG, Wolbarsht ML (1970) Responses to directional stimuli in retinal preganglionic units. J Physiol 206:93–107
Ohm J (1981) Intrazelluläre Ableitungen aus Vertikal-Bewegungsdetektoren in der Lobula der BieneApis melliflca carnica. Verh Dtsch Zool Ges 1981:172
O'Shea M, Williams JLD (1974) The anatomy and output connection of a locust visual interneurone: the lobular giant movement detector (LGMD) neurone. J Comp Physiol 91:257–266
O'Shea M, Rowell CHF, Williams JLD (1974) The anatomy of a locust visual interneurone: The descending contralateral movement detector. J Exp Biol 60:1–12
Palmgren A (1960) Specific silver staining of nerve fibers. I. Technique for vertebrates. Acta Zool (Stockh) 41:239–265
Poggio T, Reichardt W, Hausen K (1981) A neuronal circuitry for relative movement discrimination by the visual system of the fly. Naturwissenschaften 68:443–446
Seidl R, Kaiser W (1981) Visual field size, binocular domain and the ommatidial array of the compound eyes in worker honey bees. J Comp Physiol 143:17–26
Srinivasan MV, Dvorak DR (1980) Spatial processing of visual information in the movement detecting pathway of the fly. J Comp Physiol 140:1–23
Strausfeld NJ (1970) Golgi studies on insects. Part II. The optic lobes of Diptera. Philos Trans R Soc Land [Biol] 258:175–223
Strausfeld NJ (1976) Atlas of an insect brain. Springer, Berlin Heidelberg New York
Strausfeld NJ, Nässel DR (1980) Neuroarchitecture of brain regions that subserve the compound eye of Crustacea and insects. In: Autrum H (ed) Comparative physiology and evolution of vision in invertebrates. Invertebrate visual centers and behavior. Springer, Berlin Heidelberg New York (Handbook of sensory physiology, vol VII/6B, pp 1–132)
Suzuki H (1975) Convergence of olfactory inputs from both antennae in the brain of the honeybee. J Exp Biol 62:11–26
Wehrhahn C (1981) Fast and slow flight torque responses in flies and their possible role in visual orientation behaviour. Biol Cybern 40:213–221
Wehrhahn C, Hausen K (1980) How is tracking and fixation accomplished in the nervous system of the fly? Biol Cybern 38:179–186
Werblin FS (1970) Response of retinal cells to moving spots: Intracellular recording inNecturus maculosus. J Neurophysiol 33:342–350
Wiitanen W (1973) Some aspects of visual physiology of the honeybee. J Neurophysiol 36:1080–1089
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Dedicated to Prof. Dr. Dr. h.c. H. Autrum on the occasion of his 75th birthday
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DeVoe, R.D., Kaiser, W., Ohm, J. et al. Horizontal movement detectors of honeybees: Directionally-selective visual neurons in the lobula and brain. J. Comp. Physiol. 147, 155–170 (1982). https://doi.org/10.1007/BF00609840
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DOI: https://doi.org/10.1007/BF00609840