Abstract
In this work we study the connection between some dynamic effects at the synaptic level and fast reorganization of cortical sensory maps. By using a biologically plausible computational model of the primary somatosensory system we obtained simulation results that can be used to relate the dynamics of the interactions of excitatory and inhibitory neurons to the process of somatotopic map reorganization immediately after peripheral lesion. The model consists of three regions integrated into a single structure: tactile receptors representing the glabrous surface of the hand, ventral posterior lateral nucleus of the thalamus and area 3b of the primary somatosensory cortex, reproducing the main aspects of the connectivity of these regions. By applying informational measures to the simulation results of the dynamic behavior of AMPA, NMDA and GABA synaptic conductances we draw some conjectures about how the several neuronal synaptic elements are related to the initial stage of the digit-induced reorganization of the hand map in the somatosensory cortex.
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References
Arbib MA, Érdi P, Szentágothai J (1998) Neural Organization: Structure, Function and Dynamics. MIT Press, Cambridge, MA.
Armentrout SL, Reggia JA, Weinrich M (1994) A neural model of cortical map reorganization following a focal lesion. Artif. Intell. Med. 6: 383-400.
Ascher P, Nowak L (1988) The role of divalent cations in the N-methyl-D-aspartate responses of mouse central neurons in culture. J. Physiol. Lond. 399: 247-266.
Baldi P, Vanier MC, Bower JM (1998) On the use of Bayesian methods for evaluating compartmental neural models. J. Comp. Neurosci. 5: 285-314.
Bear MF, Cooper LN, Ebner FF (1987) A physiological basis for a theory of synapse modification. Science 237: 42-48.
Benusková L, Diamond ME, Ebner FF (1994) Dynamic synaptic modification threshold: A computational model of experience-dependent plasticity in adult rat barrel cortex. Proc. Natl Acad. Sci. USA 91: 4791-4795.
Benusková L, Rema V, Armstrong-James M, Ebner, FF (2001) Theory for a normal and impaired experience-dependent plasticity in neocortex of adult rats. Proc. Natl Acad. Sci. USA 98: 2797-2802.
Bienenstock EL, Cooper LN, Munro PW (1982) Theory for the development of neuron selectivity: Orientation specificity and binocular interaction in visual cortex. J. Neurosci. 2: 32-48.
Bloomfield SA, Hamos JE, Shernan SM (1987) Passive cable properties and morphological correlates of neurons in the lateral geniculate nucleus of the cat. J. Physiol. 383: 653-692.
Bower JM (1992) Modeling the nervous system. Trends Neurosci. 15: 411-412.
Bower JM, Beeman D (1998) The Book of GENESIS: Exploring Realistic Neural Models with General Neural Simulation System, 2nd edn. Telos, Santa Clara, CA.
Buonomano DV, Merzenich MM (1998) Cortical plasticity: From synapses to maps. Annu. Rev. Neurosci. 21: 149-186.
Calford MB, Tweedale R (1991) Immediate expansion of receptive fields of neurons in area 3b of macaque monkeys after digit denervation. Somatosens. Motor Res. 8: 249-260.
Calford MB (2002) Dynamic representational plasticity in sensory cortex. Neurosci. 111: 709-738.
Chen QX, Wong RKS (1995) Suppression of GABAA receptor responses by NMDA application in hippocampal neurons acutely isolated from the adult guinea-pig. J. Physiol. 482: 353-362.
Clark SA, Allard T, Jenkins WM, Merzenich MM (1988) Receptive fields in the body-surface map in adult cortex defined by temporally correlated inputs. Nature 332: 444-445.
Churchill JD, Muja N, Myers WA, Besheer J, Garraghty PE (1998) Somatotopic consolidation: A third phase of reorganization after peripheral nerve injury in adult squirrel monkeys. Exp. Brain Res. 118: 189-196.
Connors BW, Gutnick MJ, Prince DA (1982) Electrophysiological properties of neocortical neurons in vitro. J. Neurophysiol. 48: 1302-1320.
Cusick CG, Wall JT, Whiting JH, Wiley RG (1990) Temporal progression of cortical reorganization following nerve injury. Brain Res. 537: 355-358.
Das A (1997) Plasticity in adult sensory cortex: A review. Network 8: R33-R76.
Destexhe A, Mainen ZF, Sejnowski TJ (1998) Kinetic models of synaptic transmission. In: C Koch, I Segev, eds. Methods in Neural Modeling: From Synapses to Networks, 2nd, edn. MIT Press, Cambridge, MA, pp. 1-25.
Durand D, Carlen P (1985) Electrotonic parameters of neurons following chronic ethanol consumption. J. Neurophysiol. 54: 807-817.
Finnerty GT, Roberts LSE, Connors BW (1999) Sensory experience modifies the short-term dynamics of neocortical synapses. Nature 400: 367-371.
Fox K (1995) The critical period for long-term potentiation in primary sensory cortex. Neuron 15: 485-488.
Gardner EP, Palmer CI (1989) Simulation of motion skin. I. Receptive fields and temporal frequency coding by cutaneous mechanoreceptors of OPTA-CON pulses delivered to the hand. J. Neurophysiol. 62: 1410-1436.
Garraghty PE, Kaas JH (1991) Functional reorganization in adult monkey thalamus after peripheral nerve injury. Neurorep. 2: 747-750.
Garraghty PE, Kaas JH (1992) Dynamic features of sensory and motor maps. Current. Opin. Neurobiol. 2: 522-527.
Garraghty PE, Muja N (1996) NMDA receptors and plasticity in adult primate somatosensory cortex. J. Comp. Neurol. 367: 319-326.
Gibson JM, Beitel RE, Welker W (1975) Diversity of coding profiles of mechanoreceptors in glabrous skin kittens. Brain Res. 86: 181-203.
Gilbert CD, Wiesel TN (1985) Intrinsic connectivity and receptive field properties in visual cortex. Vision Res. 25: 365-374.
Goldreich D, Kyriazi H, Simons D (1999) Functional independence of layer IV barrels in rodent somatosensory cortex. J. Neurophysiol. 82: 1311-1316.
Grajski KA, Merzenich MM (1990) Hebb-type dynamics is sufficient to account for the inverse magnification rule in cortical somatotopy. Neural. Comput. 2: 71-84.
Grossberg S (2000) Linking mind to brain: The mathematics of biological intelligence. Not. Americ. Mathem. Soc. 47: 1361-1372.
Hebb DO (1949) The Organization of Behaviour. Wiley, New York.
Hille B (1984) Ionic Channels of Excitable Membranes. Sinauer, Sunderland, MA.
Hodgkin AL, Huxley AF (1952) A quantitative description of membrane current and its application of conduction and excitation in nerve. J. Physiol. Lond. 117: 500-544.
Jahr C, Stevens C (1990) A quantitative description of NMDA receptor-channel kinetic behavior. J. Neurosci. 10: 1830-1837.
Jenkins WM, Merzenich MM (1987) Reorganization of neocortical representations after brain injury: A neurophysiological model of the bases of recovery from stroke. Prog. Brain Res. 71: 249-266.
Johansson RS (1978) Tactile sensibilty in the human hand: Receptive field characteristics of mechanoreceptive units in the glabrous skin area. J. Neurophysiol. (London) 281: 101-123.
Jones EG (1985) The Thalamus. Plenum Press, New York.
Jones EG (1998) Viewpoint: The core and the matrix of thalamic organization. Neurosci. 85: 331-345.
Kaas JH, Nelson RJ, Sur M, Lin CS, Merzenich MM (1979) Multiple representations of the body within the primary somatosensory cortex of primates. Science 204: 521-523.
Kaas JH (1991) The reorganization of sensory and motor maps after injury in adult mammals. Annu. Rev. Neurosci. 14: 137-167.
Kaas JH (2000) Plasticity of sensory and motor maps in adult mammals. In Gazzaniga MS, The New Cognitive Neurosciences, 4th edition. MIT Press, Cambridge, pp. 223-236.
Kandel ER, Schwartz JH, Jessel TM (2000) Principles of Neural Science. McGraw Hill, New York.
Kawaguchi Y (1993) Groupings of nonpyramidal and pyramidal cells with specific physiological and morphological characteristics in rat frontal cortex. J. Neurophysiol. 69: 416-431.
Khinchin AI (1957) Mathematical Foundation of Information Theory. Dover, New York.
Koch C (1999) Biophysics of Computation: Information Processing in Single Neurons. Oxford University Press, New York.
Kolarik RC, Rasey SK, Wall JT (1994) The consistency, extent, and location of early-onset changes in cortical nerve dominance aggregates following injury of nerves to primate hands. J. Neurosci. 14: 4269-4288.
Larkman A, Mason A (1990) Correlations between morphology and electrophysiology of pyramidal neurons in slices of rat visual cortex. I. establishment of cell classes. J. Neurosci. 10: 1407-1414.
Lenz FA, Kwan HCV, Martín R, Tasker R, Richardson RT, Dostrovsky JO (1994) Characteristics of somatotopic organization and spontaneous neuronal activity in the region of the thalamic principal sensory nucleus in patients with spinal cord transection. J. Neurophysiol. 72: 1570-1587.
Lenz FA, Garonzik IM, Zihr TA, Dougherty PM (1998) Neuronal activity in the region of the thalamic principal sensory nucleus (ventralis caudalis) in patients with pain following amputations. Neurosci. 86: 1065-1081.
Lytton WW, Sejnowiski TJ (1991) Simulations of cortical pyramidal neurons synchronized to inhibitory interneurons. J. Neurophysiol. 66: 1059-1079.
Mazza MB, de Pinho M, Roque AC (1999) Biologically plausible models of topographic map formation in the somatosensory and auditory cortices. Int. J. Neural Syst. 9: 265-271.
Mazza M, de Pinho M, Piqueira JRC, Roque AC (2002) Using information theory for the analysis of cortical reorganization in a realistic computational model of the somatosensory system. Neurocomputing 44-46: 923-928.
McCormick DA, Connors BW, Lighthall JW (1985) Comparative electrophysiology of pyramidal and sparsely spiny stellate neurons of the neocortex. J. Neurophysiol. 54: 782-806.
McCowan B, Hanser SF, Doyle LR (1999) Quantitative tools for comparing animal communication systems: Information theory applied to bottlenose dolphin whistle repertoires. Anim. Behav. 57: 409-419.
Mel BW (1993) Synaptic integration in an excitable dendritic tree. J. Neurophysiol. 70: 1086-1101.
Merzenich MM, Kaas JH, Wall JT, Nelson RJ, Sur M, Felleman DJ (1983a) Topographic reorganization of somatosensory cortical areas 3b and 1 in adult monkeys following restricted deafferentation. Neurosci. 8: 33-55.
Merzenich MM, Kaas JH, Wall JT, Sur M, Nelson RJ, Sur M, Felleman DJ (1983b) Progression of change following median nerve section in the cortical representation of the hand in areas 3b and 1 in adult owl and squirrel monkeys. Neurosci. 10: 639-665.
Merzenich MM, Nelson, Stryker MP, Cynader MS, Schopmann A, Zook JM (1984) Somatosensory map changes following digit amputation in adult monkeys. J. Comp. Neurology 244: 591-605.
Merzenich MM, Nelson RJ, Kaas JH, Stryker MP, Jenkins WM (1987) Variability in hand surface representations in areas 3b and 1 in adult owl and squirrel monkeys. J. Comp. Neurology 258: 281-296.
Merzenich MM, Sameshima K (1993) Cortical plasticity and memory. Curr. Opin. Neurobiol. 3: 187-196.
Miller KD, Keller JB, Stryker MP (1989) Ocular dominance column development: Analysis and simulation. Science. 245: 605-615.
Myers WA, Churchill JD, Muja N, Garraghty PE (2000) Role of NMDA receptors in adult primate cortical somatosensory plasticity. J. Comp. Neurol. 418: 373-382.
Nolte J (1993) The Human Brain: An Introduction to its Functional Anatomy. Mosby-Year Book, Saint Louis, MO.
Nowak L, Bregestovski P, Ascher P, Herbet A, Prochiantz A (1984) Magnesium gates glutamate-activated channels in mouse central neurones. Nature 307: 462-465.
Oliveira RF, Roque AC (2002) A biologically plausible neural network model of the primate primary visual system. Neurocomput. 44-46: 957-963.
Panzeri S, Treves A, Schultz S, Rolls ET (1999) On decoding the responses of a population of neurons from short time windows. Neural Comput. 11: 1553-1577.
Pape HC, McCormick DA (1995) Electrophysiological and pharmacological properties of interneurons in the cat dorsal lateral nucleus. Neurosci. 68: 1105-1125.
Pearson JC, Finkel LM, Edelman GM (1987) Plasticity in the organization of adult cerebral cortical maps: A computer simulation based on neuronal group selection. J. Neurosci. 7: 4209-4223.
Piqueira JRC (1994) Structural and functional complexity: An informational approach. Proceedings of IEEE Conference on Systems, Man and Cybernetics, San Antonio-TX, pp. 1974-1978.
Pongrácz F, Nicholas PP, Kocsis JD, Shepherd GM (1992) A model of NMDA receptor-mediated activity in dendrites of hippocampal CA1 pyramidal neurons. J. Neurophysiol. 68: 2248-2259.
Rall W (1989) Cable theory for dendritic neurons. In: Koch C, Segev I, eds. Methods in Neural Modeling: From Synapses to Networks. MIT Press, Cambridge, MA, pp. 9-62.
Rasmusson DD (1996) Changes in the response properties of neurons in the ventroposterior lateral thalamic nucleus of the racoon after peripheral deafferentation. J. Neurophysiol. 75: 2441-2450.
Rieke F, Warland D, Steveninck RR, Bialek W (1997) Spikes: Exploring the Neural Code. MIT Press, Cambridge, MA.
Roque da Silva AC (1992) Analysis of equilibrium properties of a continuous neural network made of excitatory and inhibitory neurons. Network 3: 303-321.
Sanger TD, Merzenich MM (2000) Computational model of the role of sensory disorganization in focal task-specific dystonia. J. Neurophysiol. 84: 2458-2464.
Segev I (1995) Dendritic processing. In: Arbib MA, ed. The Handbook of Brain Theory and Neural Networks. MIT Press, Cambridge, MA, pp. 282-289.
Sherman RA, Koch C (1998) Thalamus. In RA Sherman, ed. The Synaptic Organization of the Brain. Oxford University Press, pp. 289-328.
Shannnon C, Weaver W (1949) The Mathematical Theory of Communication. University of Illinois Press, Chicago.
Shiryayev AN (1993) Selected Works of A.N. Kolmogorov. Kluwer Academic Publishers, Amsterdam.
Silva MLD, Piqueira JRC, Vielliard JME (2000) Using Shannon Entropy on Measuring the Individual Variability in the Rufous-Bellied Trush Turdus Rufiventris Vocal Communication. J. Theor. Biol. 207: 57-64.
Sirosh J, Miikkulainen R (1997) Topographic receptive fields and patterned lateral interaction in a self-organizing model of the primary visual cortex. Neural. Comput. 9: 577-594.
Sur M, Merzenich MM, Kaas JH (1980) Magnification, receptive-field area and hypercolumn size in owl monkeys. J. Neurophys. 44: 295-311.
Takeuchi A, Amari S (1979) Formation of topographic maps and columnar microstructures in nerve fields. Biol. Cybern. 35: 63-72.
Toma S, Nakajima Y (1995) Response characteristics of cutaneous mechanoreceptors to vibratory stimuli in human glabrous skin. Neurosci. Letters 195: 61-63.
Traub RD, Miles R (1991) Model of the origin of rhythmic population oscillations in the hippocampal slice. Science 243: 1319-1325.
Traub RD, Wong RK, Miles R, Michelson H (1991) A model of CA3 hippocampal pyramidal neuron incorporating voltage-clamp data on intrinsic conductances. J. Neurophysiol. 66: 635-650.
von der Malsburg C (1973) Self-organization of orientation sensitive cells in the striata cortex. Kybernetik, 14: 84-100.
Xing J, Gerstein GL (1996) Networks with lateral connectivity. III. plasticity and reorganization of somatosensory cortex. J. Neurophysiol. 75: 217-232.
Xerri C, Merzenich MM, Petersen BE, Jenkins WM (1998) Plasticity of primary somatosensory cortex paralleling sensorimotor skill recovery from stroke in adult monkeys. J. Neurophysiol. 79: 2119-2148.
Yuen GLF, Durand D (1991) Reconstruction of the hippocampal granule cell electrophysiology by computer simulation. Neurosci. 41: 411-425.
Wall JT, Xu J, Wang X (2002) Human brain plasticity: An emerging view of the multiple substrates and mechanisms that cause cortical changes and related sensory dysfunction after injuries of sensoryinputs from the body. Brain Res. Rev. 39: 181-215.
Wang X, Rinzel J, Ragawski MA (1991) A model of the t-type calcium current and the low threshold spike in thalamic neurons. J. Neurophysiol. 66: 839-850.
Watanabe O (1992) Kolmogorov Complexity and Computational Complexity. Springer-Verlag, Berlin.
White EL (1989) Cortical Circuits: Synaptic Organization of the Cerebral Cortex, Structure, Function and Theory. Birkhauser, Boston.
Willshaw DJ, von der Malsburg C (1976) How patterned neural connections can be set up by self-organization. Proc. R. Soc. Lond. B 194: 431-445.
Woolsey C, Marshall WH, Bard P (1942) Representation of cutaneous tactile sensibility in the cerebral cortex of the monkey as indicated by evoked potentials. Bull. Johns Hopkins Hosp. 70: 399-441.
Zador A, Koch C, Brown TH (1990) Biophysical model of a Hebbian receptor channel kinetic behavior. Proc. Natl. Acad. Sci. USA 10: 97-133.
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Mazza, M., de Pinho, M., Piqueira, J.R.C. et al. A Dynamical Model of Fast Cortical Reorganization. J Comput Neurosci 16, 177–201 (2004). https://doi.org/10.1023/B:JCNS.0000014109.83574.78
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DOI: https://doi.org/10.1023/B:JCNS.0000014109.83574.78