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Modeling neural mechanisms of vertebrate habituation: Locus specificity and pattern discrimination

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Abstract

A critical problem in neurobiology is to explain how the central nervous system coordinates pattern discrimination and locus specificity in learning. This problem is investigated in anuran amphibians who demonstrate both locus specificity and pattern discrimination in visual habituation. A neural mechanism is proposed whereby neural circuitry for pattern discrimination is shared by a spatial memory system. Such learning processes are argued to occur in the medial pallium (MP), the anuran's homolog of mammalian hippocampus. Necessary mapping from the shared network to spatial memory is set up by a mechanism that forms topographical connections, with desired orientation determined by activity gradient in presynaptic and postsynaptic layers. The model of MP is tested on both locus and stimulus specific habituation, which involve short-term as well as long-term synaptic plasticity. Successful modeling yields a set of predictions concerning MP organization and learning properties.

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References

  • Amari SI (1980) Topographic organization of nerve fields. Bulletin of Mathematical Biology. 42:339–364.

    PubMed  Google Scholar 

  • Brown TH and Zador AM (1990) Hippocampus. In GM Shepherd (Ed.), The synaptic organization of the brain (pp. 346–388). New York: Oxford University Press.

    Google Scholar 

  • Cervantes-Pérez F, Lara R, and Arbib MA (1985) A neural model of interactions subserving prey-predator discrimination and size preference in anuran amphibians. Journal of Theoretical Biology. 113:117–152.

    PubMed  Google Scholar 

  • Didday RL (1976) A model of visuomotor mechanisms in the frog optic tectum. Mathematical Bioscience. 30:169–180.

    Google Scholar 

  • Durbin R and Mitchison G (1990) A dimension reduction framework for understanding cortical maps. Nature. 343:644–647.

    PubMed  Google Scholar 

  • Eikmanns KH (1955) Verhaltensphysiologische Untersuchungen über den Beutefang und das Bewegungssehen der Erdkröte (Bufo bufo L.). Zeitschrift für Tierpsychologie. 12:229–253.

    Google Scholar 

  • Ewert J-P (1984) Tectal mechanisms that underlie prey-catching and avoidance behaviors in toads. In H Vanegas (Ed.), Comparative neurology of the optic tectum (pp. 246–416). New York: Plenum.

    Google Scholar 

  • Ewert J-P (1987) Neuroethology: toward a functional analysis of stimulus-response mediating and modulating neural circuitries. In P Ellen and C Thinus-Blonc (Eds). Congnitive processes and spatial orientation in animal and man (Pt. 1, pp. 177–200). Dordrecht. Martinus Nijhoff.

    Google Scholar 

  • Ewert J-P, Beneke TW, Buxbaum-Conradi H, Dinges AW, Fingerling S, Glagow M, Schürg-Pfeiffer E, and Schwippert WW (1992) Adapted and adaptive properties in neural networks for visual pattern dicrimination: A neurobiological analysis toward neural engineering. Adaptive Behavior. 1:123–154.

    Google Scholar 

  • Ewert J-P and Ingle D (1971) Excitatory effects following habituation of prey-catching activity in frogs and toads. Journal of Comparative and Physiological Psychology. 77:369–374.

    PubMed  Google Scholar 

  • Ewert J-P and Kehl W (1978) Configurational prey-selection by individual experience in the toad Bufo bufo. Journal of Comparative Physiology A. 126:105–114.

    Google Scholar 

  • Finkenstädt T (1989a) Stimulus-specific habituation in toads: 2DG studies and lesion experiments. In J-P Ewert and MA Arbib (Eds). Visuomotor coordination: amphibians, comparisons, models, and robots (pp. 767–797). New York: Plenum.

    Google Scholar 

  • Grossberg S (1976) Adaptive pattern classification and universal recoding: I. Parallel development and coding of neural feature detectors. Biological Cybermetics. 23:121–134.

    Google Scholar 

  • Grossberg S and Kuperstein M (1986) Neural dynamics of adaptive sensory-motor control. Amsterdam: North-Holland.

    Google Scholar 

  • Grossberg S and Schmajuk NA (1988) Neural dynamics of adaptive timing and temporal discrimination during associative learning. Neural Networks. 2:79–102.

    Google Scholar 

  • Hebb DO (1949) The organization of behavior. New York: Wiley & Sons.

    Google Scholar 

  • Herrick CJ (1933) The amphibian forebrain. VIII. Cerebral hemispheres and pallial primordia. Journal of Comparative Neurology. 58:737–759.

    Google Scholar 

  • Hoffman HH (1963) The olfactory bulb, accessory olfactory bulb and hemisphere of some anurans. Journal of Comparative Neurology. 120:317–368.

    PubMed  Google Scholar 

  • Hope RA, Hammond BJ, and Gaze RM (1976) The arrow model: retinotectal specificity and map formation in the goldfish visual system. Proceedings of Royal Society of London B. 194:447–466.

    Google Scholar 

  • Kandel ER (1976) Cellular basis of behavior: An introduction to behavioral neurobiology. New York: Freeman.

    Google Scholar 

  • Kicliter E and Ebbesson SOE (1976) Organization of the “nonol-factory” telencephalon. In R Llinás and W Precht (Eds.), Frog Neurobiology (pp. 946–972). Berlin Heidelberg New York: Springer-Verlag.

    Google Scholar 

  • Kohonen T (1982) Self-organized formation of topologically correct feature maps. Biological Cybernetics. 43:59–69.

    Google Scholar 

  • Lara R and Arbib MA (1985) A model of the neural mechanisms responsible for pattern recognition and stimulus specific habituation in toads. Biological Cybernetics. 51:223–237.

    PubMed  Google Scholar 

  • Liberman MC (1978) Auditory-nerve response from cats raised in a low-noise chamber. Journal of Acoustical Society of America. 63:442–455.

    Google Scholar 

  • Montgomery N and Fite KV (1989) Retinotopic organization of central optic projections in Rana pipiens. Journal of Comparative Neurology. 283:526–540.

    PubMed  Google Scholar 

  • Neary TJ (1990) The pallium of anuran amphibians. In EG Jones, and Peters A (Eds.) Cerebral cortex (Vol. 8A, pp. 107–138). New York: Plenum.

    Google Scholar 

  • Northcutt RG and Kicliter E (1980) Organization of the amphibian telencephalon. In SOE Ebbesson (Ed.) Comparative neurology of the telencephalon (pp. 203–255). Plenum: New York.

    Google Scholar 

  • Obermayer K, Ritter H, and Schulten K (1990) A principle for the formation of the spatial structure of cortical feature maps. Proceedings of National Academy of Sciences USA. 87:8345–8349.

    Google Scholar 

  • O'Keefe J (1989) Computations the hippocampus might perform. In L Nadel, LA Cooper, P Culicover, and RM Harnish (Eds.) Neural connections, mental computation (pp. 225–284). Cambridge MA: MIT Press.

    Google Scholar 

  • O'Keefe J and Nadel L (1978) The hippocampus as a cognitive map. Oxford: Clarendon Press.

    Google Scholar 

  • Overton KJ and Arbib MA (1982) The extended branch-arrow model of the formation of retino-tectal connections. Biological Cybernetics. 45:157–175.

    PubMed  Google Scholar 

  • Popper AN and Fay RR (Eds. 1992) The mammalian auditory pathway: neurophysiology. New York: Springer-Verlag.

    Google Scholar 

  • Rolls ET (1988) Visual information processing in the primate temporal lobe. In M Imbert (Ed.), Models of visual perception: from natural to artificial. Oxford: Oxford University Press.

    Google Scholar 

  • Schiller PH (1970) The discharge characteristics of single units in the oculomotor and abducens nuclei of the unanesthetized monkey. Experimental Brain Research. 10:347–362.

    Google Scholar 

  • Sokolov EN (1966) Neuronal models and the orienting reflex. In MAB Brazier (Ed.), The central nervous system and behavior: III (pp. 187–276). New York: Macy Foundation.

    Google Scholar 

  • Sokolov EN (1990) The orienting response, and future directions of its development. Pavlov Journal of Biological Science. 25:142–150.

    Google Scholar 

  • Thompson RF and Spencer WA (1966) Habituation: A model phenomenon for the study of neuronal substrates of behavior. Psychological Review. 73:16–43.

    PubMed  Google Scholar 

  • Vinogradova O (1975) The hippocampus and the orienting reflex. In: EN Sokolov, and O Vinogradova (Eds.), Neuronal mechanisms of the orienting reflex (pp. 128–154). New York: Erlbaum.

    Google Scholar 

  • von der Malsburg C (1973) Self-organization of orientation sensitive cells in the striate cortex. Kybernetik. 14:85–100.

    PubMed  Google Scholar 

  • von der Malsburg C and Willshaw DJ (1977) How to label nerve cells so that they can interconnect in an orderly fashion. Proceedings of National Academy of Sciences USA. 74:5176–5178.

    Google Scholar 

  • Wang DL (1993) A neural model of synaptic plasticity underlying short-term and long-term habituation. Adaptive Behavior. 2:111–129.

    Google Scholar 

  • Wang DL and Arbib MA (1991) How does the toad's visual system discriminate different worm-like stimuli? Biological Cybernetics. 64:251–261.

    PubMed  Google Scholar 

  • Wang DL and Arbib MA (1992) Modeling the dishabituation hierarchy in toads: The role of the primordial hippocampus. Biological Cybernetics. 67:535–544.

    PubMed  Google Scholar 

  • Wang DL and Ewert J-P (1992) Configurational pattern discrimination responsible for dishabituation in common toads Bufo bufo (L.): Behavioral tests of the predictions of a neural model. Journal of Comparative Physiology A. 170:317–325.

    Google Scholar 

  • Willshaw DJ and von der Malsburg C (1976) How patterned neural connections can be set up by self-organization. Proceedings of Royal Society of London B. 194:431–445.

    Google Scholar 

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  1. Laboratory for AI Research, Department of Computer and Information Science, and Center for Cognitive Science, The Ohio State University, 43210, Columbus, OH, USA

    Deliang Wang

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  1. Deliang Wang
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Wang, D. Modeling neural mechanisms of vertebrate habituation: Locus specificity and pattern discrimination. J Comput Neurosci 1, 285–299 (1994). https://doi.org/10.1007/BF00961877

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  • DOI: https://doi.org/10.1007/BF00961877

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