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Dynamic Neural Network Models of the Premotoneuronal Circuitry Controlling Wrist Movements in Primates

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Abstract

Dynamic recurrent neural networks were derived to simulate neuronal populations generating bidirectional wrist movements in the monkey. The models incorporate anatomical connections of cortical and rubral neurons, muscle afferents, segmental interneurons and motoneurons; they also incorporate the response profiles of four populations of neurons observed in behaving monkeys. The networks were derived by gradient descent algorithms to generate the eight characteristic patterns of motor unit activations observed during alternating flexion-extension wrist movements. The resulting model generated the appropriate input-output transforms and developed connection strengths resembling those in physiological pathways. We found that this network could be further trained to simulate additional tasks, such as experimentally observed reflex responses to limb perturbations that stretched or shortened the active muscles, and scaling of response amplitudes in proportion to inputs. In the final comprehensive network, motor units are driven by the combined activity of cortical, rubral, spinal and afferent units during step tracking and perturbations.

The model displayed many emergent properties corresponding to physiological characteristics. The resulting neural network provides a working model of premotoneuronal circuitry and elucidates the neural mechanisms controlling motoneuron activity. It also predicts several features to be experimentally tested, for example the consequences of eliminating inhibitory connections in cortex and red nucleus. It also reveals that co-contraction can be achieved by simultaneous activation of the flexor and extensor circuits without invoking features specific to co-contraction.

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References

  • Baldissera F, Hultborn H, Illert M (1981) Integration in spinal neuronal systems. In: JM Brookhart and VB Mountcastle, eds. Handbook of Physiology—the Nervous System II. American Physiological Society, Bethesda, MD.

  • Baraduc P, Guigon E, Burnod Y (2001) Recoding arm position to learn visuomotor transformations. Cerebral Cortex 11: 906–917.

    Article  PubMed  Google Scholar 

  • Baraduc P, Guigon E (2002) Population computation of vectorial transformations. Neural Comput. 14: 845–871.

    Article  PubMed  Google Scholar 

  • Baranyi A, Szente MB, Woody CD (1993) Electrophysiological characterization of different types of neurons recorded in vivo in the motor cortex of the cat: I. Patterns of firing activity and synaptic responses. J. Neurophysiol. 69: 1850–1864.

    Google Scholar 

  • Berthier NE, Singh SP, Barto AG, Houk JC (1993) Distributed representation of limb motor programs in arrays of adjustable pattern generators. J. Cog. Neurosci. 5: 56–78.

    Google Scholar 

  • Bullock D, Contreras-Vidal JL (1993) How spinal neural networks reduce discrepancies between motor intention and motor realization. In: KM Newell and DM Corcos, eds. Variability and Motor Control. Human Kinetics Press, Champaign, IL, pp. 183–221.

  • Bullock D, Contreras-Vidal JL, Grossberg S (1993) Equilibria and dynamics of a neural network model for opponent muscle control. In: GA Bekey and KY Goldberg, eds. Neural Networks in Robotics. Kluwer Academic Publishers, Boston/Dordrecht/London, pp. 439–457.

  • Bullock D, Grossberg S (1992) Emergence of tri-phasic muscle activation from the nonlinear interactions of central and spinal neural network circuits. Human Movement Sci. 11: 157–167.

    Article  Google Scholar 

  • Bullock D, Grossberg S, Guenther FH (1993) A self-organizing neural model of motor equivalent reaching and tool use by a multijoint arm. J. Cog. Neurosci. 5: 408–435.

    Google Scholar 

  • Bullock D, Cisek P, Grossberg S (1998) Cortical networks for control of voluntary arm movements under variable force conditions. Cerebral Cortex 8: 48–62.

    Article  PubMed  Google Scholar 

  • Buys EJ, Lemon RN, Mantel GWH, Muir RB (1986) Selective facilitation of different hand muscles by single corticospinal neurones in the conscious monkey. J. Physiol. 381: 529–549.

    PubMed  Google Scholar 

  • Cheney PD, Fetz EE (1980) Functional classes of primate corticomotoneural cells and their relation to active force. J. Neurophysiol. 44: 773–791.

    PubMed  Google Scholar 

  • Cheney PD, Fetz EE (1984) Corticomotoneuronal cells contribute to long-latency stretch reflexes in the Rhesus monkey. J. Physiol. 349: 249–272.

    PubMed  Google Scholar 

  • Cheney PD, Fetz EE (1985) Comparable patterns of muscle facilitation evoked by individual corticomotoneuronal (CM) cells and by single intracortical microstimuli in primates: Evidence for functional groups of CM cells. J. Neurophysiol. 53: 786–804.

    PubMed  Google Scholar 

  • Cheney PD, Fetz EE, Mewes K (1991) Neural mechanisms underlying corticospinal and rubrospinal control of limb movements. Prog. Brain Res. 87: 213–252.

    PubMed  Google Scholar 

  • Clough JFM, Phillips CG, Sheridan JD (1971) The short-latency projection from the baboons’ motor cortex to fusimotor neurones of the forearm and hand. J. Physiol. 216: 257–279.

    PubMed  Google Scholar 

  • Corradini ML, Gentilucci M, Leo T, Rizzolatti G (1992) Motor control of voluntary arm movements. Kinematic and modelling study. Biological Cybernetics 67: 347–360.

    Google Scholar 

  • Dornay M, Mussa-Ivaldi FA, McIntyre J, Bizzi E (1993) Stability constraints for the distributed control of motor behavior. Neural Networks 6: 1045–1059.

    Google Scholar 

  • Evarts EV (1981) Role of motor cortex in voluntary movements in primates. In: JM Brookhart, VB Mountcastle, eds. Handbook of Physiology—The Nervous System II. American Physiological Society, Bethesda, Maryland, pp. 1083–1120.

  • Edin BB, Vallbo AB (1990) Dynamic response of human muscle spindle afferents to stretch. J. Neurophysiol. 63: 1297–1306.

    PubMed  Google Scholar 

  • Fetz EE (1992) Are movement parameters recognizably coded in the activity of single neurons? Behav. Brain Sci. 15: 679– 690.

    Google Scholar 

  • Fetz EE (1993) Dynamic recurrent neural network models of sensorimotor behavior. In: D Gardner, ed. The Neurobiology of Neural Networks. MIT Press, Cambridge MA. pp. 165–190.

    Google Scholar 

  • Fetz EE, Cheney PD (1980) Postspike facilitation of forelimb muscle activity by primate corticomotoneuronal cells. J. Neurophysiol. 44: 751–772.

    PubMed  Google Scholar 

  • Fetz EE, Cheney PD, Mewes K, Palmer S (1989) Control of forelimb muscle activity by populations of corticomotoneuronal and rubromotoneuronal cells. Prog. Brain Res. 80: 437–449.

    PubMed  Google Scholar 

  • Fetz EE, Shupe LE (1990) Neural network models of the primate motor system. In: R Eckmiller, ed. Advanced Neural Computers. Elsevier Science Publishers B.V., North-Holland, pp. 43–50.

    Google Scholar 

  • Fetz EE, Shupe LE, Murthy VN (1990) Neural networks controlling wrist movement. PIJCNN 2: 675–679.

    Google Scholar 

  • Fetz EE, Toyama K, Smith WS (1991) Synaptic interactions between cortical neurons. In: A Peters, EG Joness, eds. Cerebral Cortex, Vol IX. Plenum Publishing Corporation. pp. 1–47.

  • Fetz EE, Perlmutter SI, Maier MA, Flament D, Fortier PA (1996) Response patterns and post-spike effects of premotor neurons in cervical spinal cord of behaving monkeys. Can. J. Physiol. and Pharm. 74: 531–546.

    Article  Google Scholar 

  • Flament D, Fortier PA, Fetz EE (1992) Response patterns and post-spike effects of peripheral afferents in dorsal root ganglia of behaving monkeys. J. Neurophysiol. 67: 875–889.

    PubMed  Google Scholar 

  • Fromm C (1983) Contrasting properties of pyramidal tract neurons located in the precentral or postcentral areas and of corticorubral neurons in the behaving monkey. Adv. Neurol. 39: 329– 345.

    PubMed  Google Scholar 

  • Georgopoulos AP (1991) Higher order motor control. Annual Review of Neuroscience 14: 361–377.

    Article  PubMed  Google Scholar 

  • Gomi H, Kawato M (1997) Human arm stiffness and equilibrium-point trajectory during multi-joint movement. Biolological Cybernetics 76: 163–171.

    Article  Google Scholar 

  • Graham BP, Redman SJ (1993) Dynamic behavior of a model of the muscle stretch reflex. Neural Net. 6: 947–962.

    Google Scholar 

  • Gribble PL, Ostry DJ, Sanguineti V, Laboissière R (1998) Are complex control signals required for human arm movement? J. Neurophysiol. 79: 1409–24.

    Google Scholar 

  • Guigon E, Burnod Y (1995) Modelling the acquisition of goal-directed behaviors by population of neurons. Int. J. Psychophysiol. 19: 103–113.

    Article  PubMed  Google Scholar 

  • Hoff B, Arbib MA (1992) A model of the effects of speed, accuracy, and perturbation of visually guided reaching. In: R Caminiti, P Johnson, Y Burnod, eds. Control of Arm Movement in Space: Neurophysiological and Computational Approaches. Springer, Berlin, New York. pp. 285–306.

  • Hörner M, Illert M, Kümmel H (1991) Absence of recurrent axon collaterals in motoneurones to the extrinsic digit extensor muscles of the cat forelimb. Neurosci. Let. 122: 183–186.

    Article  Google Scholar 

  • Houk JC, Keifer J, Barto AG (1993) Distributed motor commands in the limb premotor network. Trends Neurosci. 16: 27–33.

    Article  PubMed  Google Scholar 

  • Hultborn H, Jankowska H, Lindstrom S (1971) Recurrent inhibition of interneurons monosynaptically activated from group Ia afferents. J. Physiol. 215: 613–636.

    PubMed  Google Scholar 

  • Hultborn H, Lindstrom S, Wigstrom H (1979) On the function of recurrent inhibition in the spinal cord. Exp. Brain Res. 37: 399–403.

    Article  PubMed  Google Scholar 

  • Humphrey DR, Reed DJ (1983) Separate cortical systems for control of joint movement and joint stiffness: reciprocal activation and coactivation of antagonist muscles. In: JE Desmedt, ed. Motor Control Mechanisms in Health and Disease: Advances in Neurology 39. Raven Press, New York, pp. 347–372.

    Google Scholar 

  • Humphrey DR, Gold R, Reed DJ (1984) Sizes, laminar and topographic origins of cortical projections to the major divisions of the red nucleus in the monkey. J. Comp. Neurol. 225: 75–94.

    Article  PubMed  Google Scholar 

  • Imamizu H, Uno Y, Kawato M (1998) Adaptive internal model of intrinsic kinematics involved in learning an aiming task. J. Exp. Psychol. and Human Perceptual Performance 3: 812–829.

    Google Scholar 

  • Jankowska E (1992) Interneuronal relay in spinal pathways from proprioceptors. Prog. Neurobiol. 38: 335–378.

    Article  PubMed  Google Scholar 

  • Kang Y, Endo K, Araki T (1988) Excitarory synaptic actions between pairs of neighboring pyramidal tract cells in the motor cortex. J. Neurophysiol. 59: 636–647.

    PubMed  Google Scholar 

  • Kang Y, Endo K, Araki T (1991) Differential connections by intracortical axon collaterals among pyramidal tract cells in the cat motor cortex. J. Physiol. 435: 243–256.

    PubMed  Google Scholar 

  • Kawato M, Maeda Y, Uno Y, Suzuki R (1990) Trajectory formation of arm movement by cascade neural network model based on minimum torque-change criterion. Biological Cybernetics 62: 275–288.

    Article  PubMed  Google Scholar 

  • Kettner R, Marcario J, Port N (1993) A neural network model of ortical activity during reaching. J. Cog. Neurosci. 5: 14–33.

    Google Scholar 

  • Lukashin AV, Georgopoulos AP (1993) A dynamical neural network model for motor cortical activity during movement: population coding of movement trajectories. Biological Cybernetics 69: 517–524.

    Article  PubMed  Google Scholar 

  • Lukashin AV, Wilcox GL, Georgopoulos AP (1994) Overlapping neural networks for multiple motor engrams. Proc. Natl. Acad. Sci. 91: 8651–8654.

    PubMed  Google Scholar 

  • Lukashin AV, Amirikian BR, Georgopoulos AP (1996) A simulated actuator driven by motor cortical signals. NeuroReport 7: 2597–2601.

    PubMed  Google Scholar 

  • Lukashin AV, Wilcox GL, Georgopoulos AP (1996) Modeling of directional operations in the motor cortex: a noisy network of spiking neurons is trained to generate a neural-vector trajectory. Neural Net. 9: 937–410.

    Article  Google Scholar 

  • Maier MA, Shupe LE, Fetz EE (2004) Recurrent neural networks of integrate-and-fire cells simulating short-term memory and wrist movement tasks derived from continuous dynamic networks. J. Physiol. (Paris) 97: 601–612.

    Article  Google Scholar 

  • Maier MA, Perlmutter SI, Fetz EE (1998) Response patterns and force relations of monkey spinal interneurons during active wrist movement. J. Neurophysiol. 80: 2495–2513.

    PubMed  Google Scholar 

  • Mantel GWH, Lemon RN (1987) Cross-correlation reveals facilitation of single motor units in thenar muscles by single corticospinal neurones in the conscious monkey. Neurosci. Let. 77: 113–118.

    Article  Google Scholar 

  • Marsden CD, Merton PA, Morton HB (1976) Stretch reflex and servo action in a variety of human muscles. J. Physiol. 259: 531–560.

    PubMed  Google Scholar 

  • Massone L, Bizzi E (1989) A neural network model for limb trajectory formation. Biological Cybernetics 61: 417–425.

    PubMed  Google Scholar 

  • Matsumura M, Sawaguchi T, Oishi T, Ueki K, Kubota K (1991) Behavioral deficits induced by local injection of bicuculline and muscimol into the primate motor and premotor cortex. J. Neurophysiol. 65: 1542–1553.

    PubMed  Google Scholar 

  • Matsumura M, Sawaguchi T, Kubota K (1992) GABAergic inhibition of neuronal activity in the primate motor and premotor cortex during voluntary movement. J. Neurophysiol. 68: 692–702.

    PubMed  Google Scholar 

  • Mewes K, Cheney PD (1994) Primate rubromotoneuronal cells: parametric relations and contribution to wrist movement. J. Neurophysiol. 72: 14–30.

    PubMed  Google Scholar 

  • Nielsen JB (1998) Co-contraction of antagonistic muscles in man. Danish Medical Bulletin, 45: 423–435.

    PubMed  Google Scholar 

  • Nieoullon A, Vuillon-Cacciuttolo G, Dusticier N, Kerkerian L, Andre D, Bosler O (1988) Putative neurotransmitters in the red nucleus and their involvement in postlesion adaptive mechanisms. Behav. Brain Res. 28: 163–174.

    Article  PubMed  Google Scholar 

  • Palmer SS, Fetz EE (1985) Discharge proprties of primate forearm motor units during isometric muscle activity. J. Neurophysiol. 54: 1178–1193.

    PubMed  Google Scholar 

  • Perlmutter SI, Maier MA, Fetz EE (1998) Activity of spinal interneurons their effects on forearm muscles during voluntary wrist movements in the monkey. J. Neurophysiol. 80: 2475–2494.

    PubMed  Google Scholar 

  • Pompeiano O (1984) Recurrent inhibition. In: RA Davidoff, ed. Handbook of the Spinal Cord. Marcel Dekker, New York. pp. 461–557.

    Google Scholar 

  • Porter LL, Sakamoto T, Asanuma H (1990) Morphological and physiological identification of neurons in the cat motor cortex which receive direct input from the somatic sensory cortex. Exp. Brain Res. 80: 209–212.

    Article  PubMed  Google Scholar 

  • Porter R, Lemon RN (1993) Corticospinal Functiona and Voluntary Movement. Oxford University Press, Oxford.

    Google Scholar 

  • Prut Y, Perlmutter SI (2003) Firing properties of spinal interneurons during voluntary movement. I. State-dependent regularity of firing. J. Neurosci. 23: 9600–9610.

    Google Scholar 

  • Schmied A, Amalric M, Dormont JF, Farin D (1991) GABAergic control of rubral single unit activity during a reaction time task. Exp. Brain Res. 84: 285–296.

    Article  PubMed  Google Scholar 

  • Schmied A, Farin D, Amalric M, Dormont JF (1991) Changes in motor performance and rubral single unit activity in cats after microinjections of serotonin into the red nucleus area. Brain Res. 567: 91–100.

    Article  PubMed  Google Scholar 

  • Tatton WG, Bawa P (1979) Input-output properties of motor unit responses in muscles stretched by imposed displacements of the monkey wrist. Exp Brain Res. 37: 439–457.

    Article  PubMed  Google Scholar 

  • Todorov E, Jordan MI (2002) Optimal feedback control as a theory of motor coordination. Nature Neurosci. 5: 1226–35.

    Article  PubMed  Google Scholar 

  • Uno Y, Kawato M, Suzuki R (1989) Formation and control of optimal trajectory in human multijoint arm movements. Biological Cybernetics 61: 89–101.

    Article  PubMed  Google Scholar 

  • Wada Y, Kawato M (1993) A neural network model for arm trajectory formation using forward and inverse dynamics models. Neural Net. 6: 919–932.

    Google Scholar 

  • Watrous RL, Shastri L (1986) Learning phonetic features using connectionist networks: an experiment in speech recognition. Technical Report MS-CIS-86-78, Linc Lab 44, University of Pensylvania.

  • Williams RJ, Zipser D (1989) A learning algorithm for continually running fully recurrent neural networks. Neural Comp. 1: 270–280.

    Google Scholar 

  • Windhorst U (1990) Activation of renshaw cells. Prog. Neurobiol. 35: 135–179.

    Article  PubMed  Google Scholar 

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Maier, M.A., Shupe, L.E. & Fetz, E.E. Dynamic Neural Network Models of the Premotoneuronal Circuitry Controlling Wrist Movements in Primates. J Comput Neurosci 19, 125–146 (2005). https://doi.org/10.1007/s10827-005-0899-5

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  • DOI: https://doi.org/10.1007/s10827-005-0899-5

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