Skip to main content

Part of the book series: Studies in Cognitive Systems ((COGS,volume 26))

  • 595 Accesses

Abstract

When faced with complex devices like most nervous systems, we invent schemes to make them easier to understand. Hierarchies, modules, feature detectors, command cells — these are all pious simplifications that we create to try to make sense of how a nervous system might function. We admit that they are simplifications, and assure ourselves that we will keep track of the complications as they arise. However, when we face data that doesn’t fit into these simple schemata, we are remarkably resistant to abandoning these comfortable mental constructs. In my own case, I started to look for the interneurons in the medicinal leech that produced a very simple reflexive response, a localized bending response to a mechanical stimulus. I expected to find interneurons that were activated during dorsal bending, others during lateral bending, and still others during ventral bending. None of the interneurons that I found were so finely tuned, so I abandoned the search. When Shawn Lockery picked up the search several years later, he found the same kind of interneurons as I had, but came to a different conclusion: that the behavior was caused by a neuronal organization that is quite different from what we expected; i.e., it was produced by a distributed network. The implications of this kind of network are not easy to grasp, because the outcome is the sum, often a nonlinear sum, of many competing interneuronal influences.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

eBook
USD 16.99
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 54.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  • Angstadt, J.D., & W.O. Friesen (1993). Modulation of swimming behavior in the medicinal leech. I. Effects of serotonin on the electrical properties of swim-gating cell 204. Journal of Comparative Physiology A 172, 223–234.

    Article  Google Scholar 

  • Baader, A., & W.B. Kristan Jr. (1992). Monitoring neuronal activity during discrete behaviors: A crawling, swimming and shortening device for tethered leeches. Journal of Neuroscience Methods 43, 215–223.

    Article  Google Scholar 

  • Bässler, U. (1993). The femur-tibia control system of stick insects — A model system for the study of joint control. Brain Research Review 18, 207–226.

    Article  Google Scholar 

  • Brodfuehrer, P.D., & W.O. Friesen (1986) From stimulation to undulation: A neuronal pathway for the control of swimming in the leech. Science 234, 1002–1004.

    Article  Google Scholar 

  • Erber, J., P. Kloppenburg, & A. Scheidler (1993). Neuromodulation by serotonin and octopamine in the honeybee: Behavior, neuroanatomy and electrophysiol-ogy. Experentia 49, 1073–1083.

    Article  Google Scholar 

  • Ehrlich, J.S., N.M. Boulis, T. Karrer, T. C.L. Sahley (1992). Differential effects of serotonin depletion on sensitization and dishabituation in the leech, Hirudo medicinalis. Journal of Neurobiology 23, 270–279.

    Article  Google Scholar 

  • Falk, C.X., J.Y. Wu, L.B. Cohen, & C. Tang, (1993). Non-uniform expression of habituation in the activity of distinct classes of neurons in the Aplysia abdominal ganglion. Journal of Neuroscience 13, 4072–4081.

    Google Scholar 

  • Friesen, W.O. (1989). Neuronal control of leech swimming movements. In J.W. Jacklet (ed.), Neuronal and cellular oscillators (pp. 269–316). New York: Marcel Dekker.

    Google Scholar 

  • Frost, W.N., G.A. Clark, & E.R. Kandel (1988). Parallel processing of short-term memory for sensitization in Aplysia. Journal of Neurobiology 19, 297–334.

    Article  Google Scholar 

  • Georgopoulos, A.P., A.B. Schwartz, & R.E. Kettner (1986). Neuronal population coding of movement direction. Science 233, 1416.

    Article  Google Scholar 

  • Granzow, B., W.O. Friesen, & W.B. Kristan Jr. (1985). Physiological and morphological analysis of synaptic transmission between leech motor neurons. Journal of Neuroscience 5, 2035–2050.

    Google Scholar 

  • Hammer, M., R. Menzel, & A. Scheidler (1993). Octopamine local injections into the mushroom body calyces substitute for the unconditioned stimulus in honeybee olfactory conditioning. In: N. Eisner & M. Hiesenberg (eds.), Gene-brain-behavior (p. 848). Stuttgart: Thieme Verlag.

    Google Scholar 

  • Hawkins, R.D., E.R. Kandel, & S.A. Siegelbaum (1993). Learning to modulate transmitter release: Themes and variations in synaptic plasticity. Annual Review of Neuroscience 16, 625–665.

    Article  Google Scholar 

  • Kristan, W.B., Jr. (1982). Sensory and motor neurones responsible for the local bending response in leeches. Journal of Experimental Biology 96, 161–180.

    Google Scholar 

  • Kristan, W.B., Jr., S.R. Lockery, G. Wittenberg, & D. Brody (1992). Making behavioral choices with interneurons in a distributed system. In J. Kien, C.R. Mc-Crohan, & W. Winlow (eds.), Neurobiology of motor programme selection (pp. 170–200). New York: Pergamon Press.

    Chapter  Google Scholar 

  • Kristan, W.B., Jr., S.J. McGirr, & G.V. Simpson (1982). Behavioural and mechanosen-sory neurone responses to skin stimulation in leeches. Journal of Experimental Biology 96, 143–160.

    Google Scholar 

  • Kristan, W.B., Jr., & B.K. Shaw (1997). Population coding and behavioral choice. Current Opinion in Neurobiology 7, 826–831.

    Article  Google Scholar 

  • Kristan, W.B., Jr., G.S. Stent, & C.A. Ort (1974a). Neuronal control of swimming in the medicinal leech. I. Dynamics of the swimming rhythm. Journal of Comparative Physiology 94, 97–119.

    Article  Google Scholar 

  • Kristan, W.B., Jr., G.S. Stent, & C.A. Ort (1974b). Neuronal control of swimming in the medicinal leech. III. Impulse patterns of motor neurons. Journal of Comparative Physiology 94, 155–176.

    Article  Google Scholar 

  • Kristan, W.B., Jr., & J.C. Weeks (1983). Neurons controlling the initiation, generation and modulation of leech swimming. In A. Roberts & B. Roberts (eds.), Neural origin of rhythmic movements (pp. 243–260). Society of Experimental Biology Symposium. Cambridge, UK: Cambridge University Press.

    Google Scholar 

  • Kristan, W.B., Jr., G. Wittenberg, M.R Nusbaum, & W. Stern-Tomlinson (1988). Multifunctional interneurons in behavioral circuits of the medicinal leech. In J. Camhi (ed.), Invertebrate neuroethology (pp. 383–389). Basel: Birkhäuser.

    Google Scholar 

  • Lehky, S., & T.J. Sejnowski (1988). Network model of shape-from-shading: neural function arises from both receptive and projection fields. Nature 333, 452–454.

    Article  Google Scholar 

  • Lent, C.M., & M.H. Dickinson (1984). Serotonin integrates the feeding behavior of the medicinal leech. Journal of Comparative Physiology 154, 457–471.

    Article  Google Scholar 

  • Lewis, J.E., & W.B. Kristan, Jr. (1998). A neuronal network for computing population vectors in the leech. Nature 391, 76–79.

    Article  Google Scholar 

  • Lewis, J.E., & W.B. Kristan, Jr. (1998). Quantitative analysis of a directed behavior in the medicinal leech: Implications for organizing motor output. Journal of Neuroscience 18, 1571–1582.

    Google Scholar 

  • Lisberger, S.G., & T.J. Sejnowski (1992). Motor learning in a recurrent network model based on the vestibuloocular reflex. Nature 360, 159–161.

    Article  Google Scholar 

  • Lockery, S.R., G. Wittenberg, W.B. Kristan Jr., & G.W. Cottrell (1989). Function of identified interneurons in the leech elucidated using networks trained by back-propagation. Nature 340, 468–471.

    Article  Google Scholar 

  • Lockery, S.R., & W.B. Kristan Jr. (1990a). Distributed processing of sensory information in the leech. I. Input-output relations of the local bending reflex. Journal of Neuroscience 10, 1811–1815.

    Google Scholar 

  • Lockery, S.R., & W.B. Kristan Jr. (1990b). Distributed processing of sensory information in the leech. II. Identification of interneurons contributing to the local bending reflex. Journal of Neuroscience 10, 1816–1829.

    Google Scholar 

  • Lockery, S.R., & W.B. Kristan Jr. (1991). Two forms of sensitization of the local bending reflex of the medicinal leech. Journal of Comparative Physiology 168, 165–167.

    Google Scholar 

  • Lockery, S.R., & T.J. Sejnowski (1992). Distributed processing of sensory information in the leech. III. A dynamical neural network model of the local bending refelex. Journal of Neuroscience 12, 3877–3895.

    Google Scholar 

  • Lockery, S.R., & T.J. Sejnowski (1993). A lower bound on the detectability of nonassociative learning in the local bending reflex on the medicinal leech. Behavioral Neural Biology 59, 208–224.

    Article  Google Scholar 

  • Loer, C.M., & W.B. Kristan Jr. (1989). Central synaptic inputs to identified leech neurons determined by peripheral targets. Science 244, 64–66.

    Article  Google Scholar 

  • Lytton, W.W., & W.B. Kristan Jr. (1989). Localization of a leech inhibitory synapse by photo-ablation of individual dendrites. Brain Research 504, 43–48.

    Article  Google Scholar 

  • Muller, K.J., J.G. Nicholls, & G.S. Stent (1981). Neurobiology of the leech. New York: Cold Spring Harbor Laboratory Press.

    Google Scholar 

  • Nicholls, J.G., & D.A. Baylor (1968). Specific modalities and receptive fields of sensory neurons in CNS of the leech. Journal of Neurophysiology 31, 740–756.

    Google Scholar 

  • Nicholls, J.G., & D. Purves (1970). Monosynaptic chemical and electrical connexions between sensory and motor cells in the central nervous system of the leech. Journal of Physiology 209, 647–667.

    Google Scholar 

  • Nusbaum, M.P., W.O. Friesen, W.B. Kristan Jr., & R.A. Pearce (1987). Neural mechanisms generating the leech swimming rhythm: Swim-initiator neurons excite the network of swim oscillator neurons. Journal of Comparative Physiology 161, 355–66.

    Article  Google Scholar 

  • Nusbaum, M.P., & W.B. Kristan Jr. (1986). Swim initiation in the leech by serotonin-containing interneurones, cells 21 and 61. Journal of Experimental Biology 122, 277–302.

    Google Scholar 

  • Ort, C.A., W.B. Kristan Jr., & G.S. Stent (1974). Neuronal control of swimming in the medicinal leech. II. Identification and connection of motor neurons. Journal of Comparative Physiology 94, 121–154.

    Article  Google Scholar 

  • Poon, M., W.O. Friesen, & G.S. Stent (1978). Neuronal control of swimming in the medicinal leech. V. Connexions between the oscillatory interneurones and the motor neurones. Journal of Experimental Biology 75, 45–63.

    Google Scholar 

  • Rumelhart, D.E., & J.L. McClelland (1986). Parallel distributed processing. Cambridge, MA: MIT Press.

    Google Scholar 

  • Sawyer, R.T. (1986). Leech biology and behaviour. Vols. 1–3. Oxford: Clarendon Press.

    Google Scholar 

  • Shaw, B.K., & W.B. Kristan Jr. (1995). The whole-body shortening reflex of the medicinal leech: Motor pattern, sensory basis, and interneuronal pathways. Journal of Comparative Physiology A 177, 667–681.

    Google Scholar 

  • Shaw, B.K., & W.B. Kristan Jr. (1997). The neuronal basis of the behavioral choice between swimming and shortening in the leech: Control is not selectively exercised at higher circuit levels. Journal of Neuroscience 17, 786–95.

    Google Scholar 

  • Sparks, D.L., C. Lee, & W.H. Rohrer (1990). Population coding of the direction, amplitude, and velocity of saccadic eye movements by neurons in the superior colliculus. Cold Spring Harbor Symposium of Quantitative Biology, vol. 55 (pp. 805–811).

    Article  Google Scholar 

  • Sparks, D.L., W.B. Kristan Jr., & B.K. Shaw (1997). The role of population coding in the control of movement. In P.S.G. Stein, S. Grillner, A.I. Selverston, & D.G. Stuart (eds.), Neurons, networks, and motor behavior (pp. 21–32). Cambridge, MA: MIT Press.

    Google Scholar 

  • Stent, G.S., W.B. Kristan Jr., W.O. Friesen, C.A. Ort, M. Poon, & R.L. Calabrese (1978). Neuronal generation of the leech swimming movement. An oscillatory network of neurons driving a locomotory rhythm has been identified. Science 200, 1348–1357.

    Article  Google Scholar 

  • Stent, G.S., W.B. Kristan Jr., S.A. Torrence, K.A. French, & D.A. Weisblat (1992). Development of the leech nervous system. Inernational Review of Neurobiology 33, 109–193.

    Article  Google Scholar 

  • Stern-Tomlinson, W., M.P. Nusbaum, L.E. Perez, & W.B. Kristan Jr. (1986). A kinematic study of crawling behavior in the leech, Hirudo medicinalis. Journal of Comparative Physiology 158, 593–603.

    Article  Google Scholar 

  • Stuart, A.E. (1970). Physiological and morphological properties of motoneurones in the central nervous system of the leech. Journal of Physiology London 209, 627–646.

    Google Scholar 

  • Willard, A.L. (1981). Effects of serotonin on the generation of the motor program for swimming by the leech. Journal of Neuroscience 1, 936–944.

    Google Scholar 

  • Wittenberg, G., & W.B. Kristan Jr. (1992a). Analysis and modeling of the multi-segmental coordination of shortening behavior in the medicinal leech. I. Motor output pattern. Journal of Neurophysiology 68, 1683–1692.

    Google Scholar 

  • Wittenberg, G., & W.B. Kristan Jr. (1992b). Analysis and modeling of the multi-segmental coordination of shortening behavior in the medicinal leech. II. Role of identified interneurons. Journal of Neurophysiology 68, 1693–1707.

    Google Scholar 

  • Zipser, D., & R.A. Anderson (1988). A back-propagation programmed network that simulates response properties of a subset of posterior parietal neurons. Nature 133, 679–684.

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2000 Springer Science+Business Media Dordrecht

About this chapter

Cite this chapter

Kristan, W.B. (2000). Distributed Processing vs. Dedicated Neurons in the Production of Simple Behavioral Acts. In: Cruse, H., Dean, J., Ritter, H. (eds) Prerational Intelligence: Adaptive Behavior and Intelligent Systems Without Symbols and Logic, Volume 1, Volume 2 Prerational Intelligence: Interdisciplinary Perspectives on the Behavior of Natural and Artificial Systems, Volume 3. Studies in Cognitive Systems, vol 26. Springer, Dordrecht. https://doi.org/10.1007/978-94-010-0870-9_18

Download citation

  • DOI: https://doi.org/10.1007/978-94-010-0870-9_18

  • Publisher Name: Springer, Dordrecht

  • Print ISBN: 978-94-010-3792-1

  • Online ISBN: 978-94-010-0870-9

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics