Hostname: page-component-78c5997874-j824f Total loading time: 0 Render date: 2024-11-05T22:36:22.680Z Has data issue: false hasContentIssue false
  • English
  • Français

Sensitization and multiplicative noise in the descending contralateral movement detector (DCMD) of the locust

Published online by Cambridge University Press:  02 June 2009

Peter D.R. Barker
Peter D.R. Barker
Affiliation:
Kenneth Craik Building, Physiological Laboratory, Downing Site, Cambridge CB2 3EG, UK
Get access Rights & Permissions [Opens in a new window]

Abstract

Spike discharges from the descending contralateral movement detector (DCMD) were recorded extracellularly from the ventral nerve cord of the locust in complete darkness, in response to dim flashes of constant-intensity light, and in response to pairs of identical flashes presented different intervals apart. Three phenomena were discovered: novel long-term sensitization which changes the DCMD's sensitivity to light, a multiplicative cascade process driven by shot events, and the suppression of the spike discharge shortly after a dim flash.

The DCMD's spike discharge is stochastic. It can be considered as a two-stage cascade process producing intrinsic multiplicative noise. An effective photon, or thermal isomerization in complete darkness, produces an unseen shot event which in turn initiates a random number of DCMD spikes in a cluster. A shot initiates a variable number of spikes when it directs the rate of a Poisson process. The results of statistical analyses are consistent with this model when the amplitudes of shot events are variable. The transmission efficiency is low because at least 2.4–9.6 quantum bumps are required to produce one extra DCMD spike.

The DCMD has a constant mean discharge rate of 0.25–1.5 spikes/s in complete darkness. Clustering about particular points in time (shots) leads to a lack of independence between interspike intervals, and the overdispersion of interspike interval and number distributions compared with those from a simple Poisson process. The mean cluster size is 1.3–1.6 spikes in darkness. Similar clustering was found in response to flashes of light.

A dim flash changes the DCMD's sensitivity to light, even at threshold when no spike discharge results. Sensitization occurs because the average number of shot events produced by isoquantal flashes depends on the history of visual stimulation. This contributes to the nonlinear response-intensity function. The evolution of sensitization is roughly constant in different DCMD cells, lasting approximately 3 s after a flash. Sensitization was observed in response to light only, presumably because the intensity of dark-light is too low. It is proposed that sensitization is associated with a set of processes or molecular state in the presynaptic region of a chemical synapse.

Keywords

ShotSensitizationMultiplicative noiseNegative binomialNonrenewalQuantum efficiency
Type
Research Articles
Information
Visual Neuroscience , Volume 10 , Issue 5 , September 1993 , pp. 791 - 809
Copyright
Copyright © Cambridge University Press 1993

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Barker, P.D.R. (1987). Statistics of spike discharges from a visual unit in the locust. Ph.D. Thesis, Cambridge University.Google Scholar
Barlow, H.B. & Levick, W.R. (1969). Changes in the maintained discharge with adaptation level in the cat retina. Journal of Physiology 202, 699–718.CrossRefGoogle ScholarPubMed
Barlow, H.B., Levick, W.R. & Yoon, M. (1971). Responses to single quanta of light in retinal ganglion cells of the cat. Vision Research (Suppl.) 3, 87–101.CrossRefGoogle Scholar
Baylor, D.A. & Fettiplace, R. (1977 a). Transmission from photoreceptors to ganglion cells in turtle retina. Journal of Physiology 271, 391–424.CrossRefGoogle ScholarPubMed
Baylor, D.A. & Fettiplace, R. (1977 b). Kinetics of synaptic transfer from receptors to ganglion cells turtle retina. Journal of Physiology 271, 425–448.CrossRefGoogle ScholarPubMed
Boswell, M.T. & Patil, G.P. (1970). Chance mechanisms generating the negative binomial distribution. In Random Counts in Models and Structures, Vol. 1, ed. Patil, G.P., Chap. 1. State College, PA: Pennsylvania State University Press.Google Scholar
Burrows, M. & Rowell, C.H.F. (1973). Connections between descending visual interneurons and metathoracic motoneurons in the locust. Journal of Comparative Physiology 85, 221–234.CrossRefGoogle Scholar
Burtt, E.T. & Catton, W.T. (1954). Visual perception of movement in the locust. Journal of Physiology 125, 455–580.CrossRefGoogle ScholarPubMed
Burtt, E.T. & Catton, W.T. (1962). A diffraction theory of insect vision. I: An experimental study of visual acuity in certain insects. Proceedings of the Royal Society B (London) 157, 53–82.Google Scholar
Burtt, E.T. & Catton, W.T. (1966). The role of diffraction in compound eye vision. In The Functional Organization of the Compound Eye. New York: Pergamon Press.Google Scholar
Burtt, E.T. & Catton, W.T. (1969). Resolution of the locust eye measured by the rotation of radial striped gratings. Proceedings of the Royal Society B (London) 173, 513–529.Google Scholar
Catton, W.T. (1976). Peaking of response in locust visual interneurones to objects of small angular subtense. Journal of Insect Physiology 22, 1475–1484.CrossRefGoogle Scholar
Catton, W.T. (1978 a). Spatial-frequency peaks in the response of the locust DCMD axon to rotation of periodic patterns, lines, and dot arrays. Journal of Insect Physiology 24, 355–362.CrossRefGoogle Scholar
Catton, W.T. (1978 b). Responses of locust visual interneurones to transiently illuminated slits, paired spots, annuli, and disk arrays. Journal of Insect Physiology 24, 285–292.CrossRefGoogle Scholar
Catton, W.T. (1980). Tonic effects of stationary luminous slits on the discharge rates of some locust visual interneurones. Journal of Insect Physiology 26, 373–379.CrossRefGoogle Scholar
Cornwall, M.C. & Thomas, M.V. (1979). A rapid cycling dual shutter control system. Vision Research (Technical Note) 19, 957–959.CrossRefGoogle ScholarPubMed
Cox, D.R. & Lewis, P.A.W. (1966). The Statistical Analysis of Series of Events. Monographs on Applied Probability and Statistics. London: Chapman and Hall, Ltd.CrossRefGoogle Scholar
Feller, W. (1957). An Introduction to Probability Theory and Its Applications, second edition. New York: Wiley.Google Scholar
Heitler, W.J. (1983). Suppression of a locust visual interneurone (DCMD) during defensive kicking. Journal of Experimental Biology 104, 203–215.CrossRefGoogle Scholar
Horn, G. & Rowell, C.H.F. (1968). Medium- and long-term changes in the behavior of visual neurones in the tritocerebrum of locusts. Journal of Experimental Biology 49, 143–169.CrossRefGoogle Scholar
Horridge, G.A. (1966). The retina of the locust. In The Functional Organization of the Compound Eye, ed. Bernhard, C.G., pp. 513–541. New York: Pergamon Press.Google Scholar
Lewis, P.A.W. (1965). Some results on tests for Poisson processes. Biometrika 52, 67–78.CrossRefGoogle Scholar
Lillywhite, P.G. (1977). Single photon signals and transduction in an insect eye. Journal of Comparative Physiology 122, 189–200.CrossRefGoogle Scholar
Lillywhite, P.G. (1978). Coupling between locust photoreceptors revealed by a study of quantum bumps. Journal of Comparative Physiology 125, 13–27.CrossRefGoogle Scholar
Lillywhite, P.G. & Dvorak, D.R. (1981). Responses to single photons in a fly optomotor neurone. Vision Research 21, 279–290.CrossRefGoogle Scholar
Lillywhite, P.G. & Laughlin, S.B. (1979). Transducer noise in a photoreceptor. Nature 277, 569–572.CrossRefGoogle ScholarPubMed
Mastebroek, H.A.K. (1974). Stochastic structure of neural activity in the visual system of the blowfly. Ph.D. Thesis, Groningen University, The Netherlands.Google Scholar
Mastebroek, H.A.K., Zaagman, W.H. & Kuiper, J.W. (1977). Intensity and structure of visually evoked neural activity: Rivals in modelling a visual system. Vision Research 17, 29–35.CrossRefGoogle Scholar
O'Shea, M. (1975). Two Sites of axonal spike initiation in a bimodal interneuron. Brain Research 96, 93–98.CrossRefGoogle Scholar
O'Shea, M. & Rowell, C.H.F. (1975 a). Protection from habituation by lateral inhibition. Nature 254, 53–55.CrossRefGoogle ScholarPubMed
O'Shea, M. & Rowell, C.H.F. (1975 b). A spike-transmitting electrical synapse between visual interneurones in the locust movement detector system. Journal of Comparative Physiology 97, 143–158.CrossRefGoogle Scholar
O'Shea, M. & Rowell, C.H.F. (1976). Part II: Response decrement, convergence and the nature of the excitatory afferents to the fan-like dendrite of the LGMD. Journal of Experimental Biology 65, 289–308.CrossRefGoogle Scholar
O'Shea, M., Rowell, C.H.F. & Williams, J.W.L. (1974). The anatomy of a locust visual interneurone: The descending contralateral movement detector. Journal of Experimental Biology 60, 1–12.CrossRefGoogle Scholar
O'Shea, M. & Williams, J.L.D. (1974). The anatomy and output connection of a locust visual interneurone: The lobula giant movement detector (LGMD) neurone. Journal of Comparative Physiology 91, 257–266.CrossRefGoogle Scholar
Osorio, D. (1987). The temporal properties of non-linear transient cells in the locust medulla. Journal of Comparative Physiology A 161, 431–440.CrossRefGoogle Scholar
Osorio, D. (1991 a). Mechanisms of early visual processing in the medulla of the locust optic lobe: How self-inhibition, spatial-pooling, and signal rectification contribute to the properties of transient cells. Visual Neuroscience 7, 345–355.CrossRefGoogle Scholar
Osorio, D. (1991 b). Patterns of function and evolution in the arthropod optic lobe. In Vision and Visual Dysfunction, Vol. II: Evolution of the Eye and Visual System, ed. Cronly-Dillon, J.R. & Gregory, R. Chap. 10. London: Macmillan.Google Scholar
Palka, J. (1967 a). An inhibitory process influencing visual responses in a fibre of the ventral nerve cord of locusts. Journal of Insect Physiology 13, 235–248.CrossRefGoogle Scholar
Palka, J. (1967 b). Head movement inhibits locust visual units response to target movement. American Zoology 7, 728.Google Scholar
Pearson, K.G. & Goodman, C.S. (1979). Correlation of variability in structure with variability in synaptic connections of an identified interneuron in locusts. Journal of Neurology 184, 141–166.Google ScholarPubMed
Pearson, K.G. & Goodman, C.S. (1981). Presynaptic inhibition of transmission from identified interneurones in the locust central nervous system. Journal of Neurophysiology 45, 501–515.CrossRefGoogle ScholarPubMed
Pearson, K.G., Heitler, W.J. & Steeves, J.D. (1980). Triggering of locust jump by multimodal inhibitory interneurones. Journal of Neurophysiology 43, 257–278.CrossRefGoogle Scholar
Pearson, K.G. & Robertson, R.M. (1981). Interneurones co-activating hindleg flexor and extensor motorneurones in locust. Journal of Comparative Physiology 144, 391–400.CrossRefGoogle Scholar
Pinter, R.B. (1977). Visual discrimination between small objects and large, textured backgrounds. Nature 270, 429–431.CrossRefGoogle ScholarPubMed
Pinter, R.B. (1979). Inhibition and excitation in the locusts DCMD receptive field: Spatial frequency, temporal and spatial characteristics. Journal of Experimental Biology 80, 191–216.CrossRefGoogle Scholar
Pinter, R.B., Olberg, R.M. & Abrams, T.W. (1982). Is the locust DCMD a looming detector? Journal of Experimental Biology 101, 327–331.CrossRefGoogle Scholar
Rees, D. (1974). The spontaneous release of transmitter from insect nerve terminals as predicted by the negative binomial theorem. Journal of Physiology 236, 129–142.CrossRefGoogle ScholarPubMed
Rind, F.C. (1984). A chemical synapse between two motion-detecting neurones in the locust brain. Journal of Experimental Biology 110, 143–168.CrossRefGoogle ScholarPubMed
Rind, F.C. (1987). Non-directional, movement-sensitive neurones of the locust optic lobe. Journal of Comparative Physiology 161, 477–494.CrossRefGoogle Scholar
Rind, F.C. (1990). Identification of directionally selective motion-detecting neurones in the locust lobula and their synaptic connections with an identified descending neurone. Journal of Experimental Biology 149, 21–43.CrossRefGoogle Scholar
Rind, F.C. & Simmons, P.J. (1992). The orthopteran DCMD neuron: A re-evaluation of responses to moving objects. I. Selective responses to approaching objects. Journal of Neurophysiology 68(5), 1654–1666.CrossRefGoogle Scholar
Rodieck, R.W. (1967). Maintained activity of cat retinal ganglion cells. Journal of Neurophysiology 30, 1043–1071.CrossRefGoogle ScholarPubMed
Rowell, C.H.F. (1971 a). The Orthopteran descending movement-detector (DCMD) neurons: A characterization and review. Journal of Comparative Physiology 73, 167–194.Google Scholar
Rowell, C.H.F. (1971 b). Variable responsiveness of a visual interneurone in the free-moving locust and its relation to behaviour and arousal. Journal of Experimental Biology 55, 727–747.CrossRefGoogle Scholar
Rowell, C.H.F. (1971 c). Antennal cleaning, arousal, and visual interneurone responsiveness in a locust. Journal of Experimental Biology 55, 749–761.CrossRefGoogle Scholar
Rowell, C.H.F. (1974). Boredom and attention in a cell in the locust visual system. In The Experimental Analysis of Insect Behavior, ed. Browne, L.B., New York: Springer.Google Scholar
Rowell, C.H.F. (1976). Small-system neurophysiology and the study of plasticity. In Neural Mechanisms of Learning and Memory, ed. Rosenzweig, M.L. & Bennet, M.V.L., Cambridge, MA: M.I.T. Press.Google Scholar
Rowell, C.H.F. & Horn, G. (1967). Response characteristics of neurones in an insect brain. Nature 216, 702–703.CrossRefGoogle Scholar
Rowell, C.H.F. & Horn, G. (1968). Dishabituation and arousal in the response of single nerve cells in an insect brain. Journal of Experimental Biology 49, 171–183.CrossRefGoogle Scholar
Rowell, C.H.F. & O'Shea, M. (1976 a). Part I: Effects of simple increment and decremental stimuli in light- and dark-adapted animals. Journal of Experimental Biology 65, 273–288.CrossRefGoogle Scholar
Rowell, C.H.F. & O'Shea, M. (1976 b). Part III: Control of response amplitude by tonic lateral inhibition. Journal of Experimental Biology 65, 617–625.CrossRefGoogle Scholar
Rowell, C.H.F. & O'Shea, M. (1980). Modulation of transmission at an electrical synapse in the locust movement-detector system. Journal of Comparative Physiology 137, 233–241.CrossRefGoogle Scholar
Rowell, C.H.F., O'Shea, M. & Williams, J.L.D. (1977). Part IV: The preference for small-field stimuli. Journal of Experimental Biology 68, 157–185.CrossRefGoogle Scholar
Saleh, B.E.A. & Teich, M.C. (1982). Multiplied-Poisson noise in pulse, particule, and photon detection. Proceedings of the IEEE 70, 229–245.CrossRefGoogle Scholar
Saleh, B.E.A. & Teich, M.C. (1985). Multiplication and refractoriness in the cat's retinal-ganglion-cell discharge at low light levels. Biological Cybernetics 52, 101–107.CrossRefGoogle ScholarPubMed
Schlotterer, G.R. (1977). Response of the locust DCMD neuron to rapidly approaching and withdrawing visual stimuli. Canadian Journal of Zoology 55, 1372–1376.CrossRefGoogle Scholar
Siegel, S. (1956). Non-Parametric Statistics for the Behavioural Sciences. London: McGraw Hill.Google Scholar
Simmons, P. (1980). Connections between a movement-detecting visual interneurone and flight motoneurones of a locust. Journal of Experimental Biology 86, 87–97.CrossRefGoogle Scholar
Simmons, P. (1981). Ocellar excitation of the DCMD: An identified locust interneurone. Journal of Experimental Biology 91, 355–359.CrossRefGoogle Scholar
Simmons, P.J. & Rind, F.C. (1992). The orthopteran DCMD neuron: A re-evaluation of responses to moving objects. II. Critical cues for detecting approaching objects. Journal of Neurophysiology 68(5), 1667–1682.CrossRefGoogle Scholar
Smith, D.R. & Smith, G.K. (1965). A statistical analysis of the continual activity of single cortical neurones in the cat un-anaesthetized isolated forebrain. Biophysical Journal 5, 47–74.CrossRefGoogle Scholar
Steeves, J.D. & Pearson, K.G. (1982). Proprioceptive gating of inhibitory pathways to hind leg flexor motoneurons of the locust. Journal of Comparative Physiology 146, 507–515.CrossRefGoogle Scholar
Teich, M.C. (1981). Role of the doubly-stochastic Neyman type A and Thomas counting distributions in photon detection. Applied Optics 20, 2457–2467.CrossRefGoogle Scholar
Teich, M.C. (1989). Fractal character of the auditory neural spike train. IEEE Transactions on Biomedical Engineering 30(1), 150–160.CrossRefGoogle Scholar
Teich, M.C. & Saleh, B.E.A. (1981). Interevent-time statistics for shot-noise-driven self-exciting point processes in photon detection. Journal of the Optical Society of America 71, 771–776.CrossRefGoogle Scholar
Teich, M.C., Johnson, D.H., Kumar, A.R. & Turcott, R.G. (1990). Rate fluctuations and fractional power-law noise recorded from cells in the lower auditory pathway of the cat. Hearing Research 46, 41–52.CrossRefGoogle ScholarPubMed
van der Kloot, W., Kita, H. & Cohen, I. (1975). The timing of the appearance of miniature end-plate potentials. Progress in Neurobiology 4, 269–326.CrossRefGoogle Scholar
Wetherill, G.B. (1967). Elementary Statistical Methods, third edition. London: Chapman&Hall, Ltd.Google Scholar
Williams, D.S. (1983). Changes in photoreceptor performance associated with the daily turnover of photoreceptor membrane in locusts. Journal of Comparative Physiology 150, 509–519.CrossRefGoogle Scholar
Yeandle, S. & Spiegler, J.B. (1973). Light-evoked and spontaneous discrete waves in the ventral nerve photoreceptors of Limulus. Journal of Comparative Physiology 61, 552–571.Google ScholarPubMed
Zaretsky, M. & Rowell, C.H.F. (1979). Saccadic suppression by corollary discharge in the locust. Nature 280, 571–583.CrossRefGoogle ScholarPubMed