Abstract
Sharks detect their prey using an extremely sensitive electrosensory system that is capable of distinguishing weak external stimuli from a relatively strong background noise generated by the animal itself. Experiments indicate that part of the shark’s hindbrain, the dorsal octavolateralis nucleus (DON), is responsible for extracting the external stimulus using an adaptive filter mechanism to suppress signals correlated with the shark’s breathing motion. The DON’s principal neuron integrates input from afferents as well as many thousands of parallel fibres transmitting, inter alia, breathing-correlated motor command signals. There are a number of models in the literature, studying how this adaptive filtering mechanisms occurs, but most of them are based on a spike-train model approach.
This paper presents a biophysically based computational simulation which demonstrates a mechanism for adaptive noise filtering in the DON. A spatial model of the neuron uses the Hodgkin–Huxley equations to simulate the propagation of action potentials along the dendrites. Synaptic inputs are modelled by applied currents at various positions along the dendrites, whose input conductances are varied according to a simple learning rule.
Simulation results show that the model is able to demonstrate adaptive filtering in agreement with previous experimental and modelling studies. Furthermore, the spatial nature of the model does not greatly affect its learning properties, and in its present form is effectively equivalent to an isopotential model which does not incorporate a spatial element.
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References
Bell, C. C., Caputi, A., Grant, K., & Serrier, J. (1993). Storage of a sensory pattern by anti-Hebbian synaptic plasticity in an electric fish. Proc. Natl. Acad. Sci. USA, 90(10), 4650–4654.
Bell, C. C., Han, V., & Sawtell, N. B. (2008). Cerebellum-like structures and their implications for cerebellar function. Annu. Rev. Neurosci., 31, 1–24.
Bodznick, D. (1993). The specificity of an adaptive filter that suppresses unwanted reafference in electrosensory neurons of the skate medulla. Biol. Bull., 185(2), 312–314.
Bodznick, D., Montgomery, J. C., & Bradley, D. J. (1992). Suppression of common mode signals within the electrosensory system of the little skate (Raja erinacea). J. Exp. Biol., 171(1), 107–125.
Bodznick, D., Montgomery, J. C., & Carey, M. (1999). Adaptive mechanisms in the elasmobranch hindbrain. J. Exp. Biol., 202(10), 1357–1364.
Fujita, M. (1982). Adaptive filter model of the cerebellum. Biol. Cybern., 45(3), 195–206.
Keener, J., & Sneyd, J. (1998). Mathematical physiology, I: cellular physiology (Vol. 1). Berlin: Springer.
Linden, D. J. (1999). The return of the spike: review postsynaptic action potentials and the induction of ltp and ltd. Neuron, 22, 661–666.
Migliore, M., & Shepherd, G. M. (2002). Emerging rules for the distributions of active dendritic conductances. Nat. Rev. Neurosci., 3(5), 362–370.
Montgomery, J. C. (1984). Noise cancellation in the electrosensory system of the thornback ray; common mode rejection of input produced by the animal’s own ventilatory movement. J. Comp. Physiol., A Sens. Neural Behav. Physiol., 155(1), 103–111.
Montgomery, J. C., & Bodznick, D. (1994). An adaptive filter that cancels self-induced noise in the electrosensory and lateral line mechanosensory systems of fish. Neurosci. Lett., 174(2), 145–148.
Montgomery, J. C., & Bodznick, D. (1999). Signals and noise in the elasmobranch electrosensory system. J. Exp. Biol., 202(10), 1349–1355.
Napper, R. M. A., & Harvey, R. J. (1988). Number of parallel fiber synapses on an individual Purkinje cell in the cerebellum of the rat. J. Comp. Neurol., 274(2), 168–177.
Nelson, M. E. (2011). Electrophysiological models of neural processing. Wiley Interdiscip. Rev., Syst. Biol. Med., 3(1), 74–92.
Nelson, M. E., & Paulin, M. G. (1995). Neural simulations of adaptive reafference suppression in the elasmobranch electrosensory system. J. Comp. Physiol., A Sens. Neural Behav. Physiol., 177(6), 723–736.
Paulin, M. G. (2005). Evolution of the cerebellum as a neuronal machine for Bayesian state estimation. J. Neural Eng., 2(3), S219.
Porrill, J., Dean, P., & Anderson, S. R. (2012). Adaptive filters and internal models: multilevel description of cerebellar function. Neural Netw. doi:10.1016/j.neunet.2012.12.005. ISSN 0893-6080. http://www.sciencedirect.com/science/article/pii/S0893608012003206.
Roberts, P. D., & Bell, C. C. (2000). Computational consequences of temporally asymmetric learning rules, II. Sensory image cancellation. J. Comput. Neurosci., 9(1), 67–83.
Sejnowski, T. J. (1977). Storing covariance with nonlinearly interacting neurons. J. Math. Biol., 4(4), 303–321.
von Holst, E., & Mittelstaedt, H. (1950). Das Reafferenzprinzip: Wechselwirkungen zwischen Zentralnervensystem und Peripherie. Naturwissenschaften, 37, 464–476.
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Appendix: Hodkgin–Huxley Equations
Appendix: Hodkgin–Huxley Equations
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Bratby, P., Montgomery, J. & Sneyd, J. A Biophysical Model of Adaptive Noise Filtering in the Shark Brain. Bull Math Biol 76, 455–475 (2014). https://doi.org/10.1007/s11538-013-9928-0
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DOI: https://doi.org/10.1007/s11538-013-9928-0