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Adaptive plasticity in the spinal stretch reflex: An accessible substrate of memory?

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Summary

  1. 1.

    The study of the substrates of memory in higher vertebrates is one of the major problems of neurobiology. A simple and technically accessible experimental model is needed.

  2. 2.

    Recent studies have demonstrated long-term adaptive plasticity, a form of memory, in the spinal stretch reflex (SSR). The SSR is due largely to a two-neuron monosynaptic arc, the simplest, best-defined, and most accessible pathway in the primate central nervous system (CNS).

  3. 3.

    Monkeys can slowly change SSR amplitude without a change in initial muscle length or alpha motoneuron tone, when reward is made contingent on amplitude. Change occurs over weeks and months and persists for long periods. It is relatively specific to the agonist muscle and affects movement.

  4. 4.

    The salient features of SSR adaptive plasticity, combined with clinical and laboratory evidence indicating spinal cord capacity for intrinsic change, suggest that SSR change eventually involves persistent segmental alteration. If this is the case, SSR plasticity should be a powerful model for studying the neuronal and synaptic substrates of memory in a primate.

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References

  • Alkon, D. L. (1974). Associative training of Hermissenda.J. Gen. Physiol. 6470–84.

    Google Scholar 

  • Ashby, P., Verrier, M., Carleton, S., and Somerville, J. (1980). Vibratory inhibition of the monosynaptic reflex and presynaptic inhibition in man. InSpasticity: Disordered Motor Control (Feldman, R. G., Young, R. R., and Koella, W. P., Eds.), Year Book, Chicago, pp. 335–344.

    Google Scholar 

  • Baldissera, F., Hultborn, H., and Illert, M. (1981). Integration in spinal neuronal systems. InHandbook of Physiology. Sect. I. The Nervous System. Vol. II. Motor Control. Part I (Brooks, V. B., Ed.), Williams and Wilkins, Baltimore, pp. 509–595.

    Google Scholar 

  • Barker, D., and Saito, M. (1981). Autonomic innervation of receptors and muscle fibers in cat skeletal muscle.Proc. R. Soc. Lond. B 212317–332.

    Google Scholar 

  • Basmajian, J. V. (1978).Muscles Alive, Williams and Wilkins, Baltimore, pp. 32–36.

    Google Scholar 

  • Bliss, T. V. P., and Gardner-Medwin, A. (1973). Long-lasting potentiation of synaptic transmission in the dentate area of the unanesthetized rabbit following stimulation of the perforant path.J. Physiol. (Lond.)232331–356.

    Google Scholar 

  • Bliss, T. V. P., and Lomo, T. (1973). Long-lasting potentiation of synaptic transmission in the dentate area of the anesthetized rabbit following stimulation of the perforant path.J. Physiol. (Lond.)232357–374.

    Google Scholar 

  • Brown, A. G. (1981).Organization in the Spinal Cord, Springer Verlag, Berlin.

    Google Scholar 

  • Brown-Sequard, C. E. (1879). Recherches experimentales sur une nouvelle propriete du system nerveux.C.R. Hebd. Seances Acad. Sci. 89889–913.

    Google Scholar 

  • Burke, D. (1980). A reassessment of the muscle spindle contribution to muscle tone in normal and spastic man. InSpasticity: Disordered Motor Control (Feldman, R. G., Young, R. R., and Koella, W. P., Eds.), Year Book, Chicago, pp. 261–286.

    Google Scholar 

  • Burke, D., Gandevia, S. C., and McKeon, B. (1984). Monosynaptic and oligosynaptic contributions to human ankle jerk and H-reflex.J. Neurophysiol. 52435–448.

    Google Scholar 

  • Burke, R. E. (1981). Motor units: Anatomy, physiology, and functional organization. InHandbook of Physiology. Sect. I. The Nervous System. Vol. II. Motor Control. Part I (Brooks, V. B., Ed.), Williams and Wilkins, Baltimore, pp. 345–422.

    Google Scholar 

  • Burke, R. E., and Rudomin, P. (1978). Spinal neurons and synapses. InHandbook of Physiology. The Nervous System. Cellular Biology of Neurons (Kandel, E. R., Ed.), Williams and Wilkins, Baltimore, pp. 877–944.

    Google Scholar 

  • Bussel, B., Morin, C., and Pierrot-Deseilligny, E. (1978). Mechanism of monosynaptic reflex reinforcement during Jendrassik maneuver in man.J. Neurol. Neurosurg. Psychiat. 4140–44.

    Google Scholar 

  • Carew, T. J., Walters, E. T., and Kandel, E. R. (1981). Classical conditioning in a simple withdrawal reflex in Aplysia californica.J. Neurosci. 11426–1437.

    Google Scholar 

  • Cohen, D. H. (1969). Development of a vertebrate experimental model for cellular neurophysiologic studies of learning.Cond. Reflex. 461–80.

    Google Scholar 

  • Cohen, D. H. (1982). Central processing time for a conditioned response in a vertebrate model system. InConditioning: Representation of Involved Neural Functions (Woody, C. D., Ed.), Plenum, New York, pp. 517–534.

    Google Scholar 

  • Cooke, J. D., and Eastman, M. J. (1977). Long loop reflexes in the tranquilized monkey.Exp. Brain Res. 27491–500.

    Google Scholar 

  • Crago, P. E., Houk, J. C., and Hasan, Z. (1976). Regulatory actions of human stretch reflex.J. Neurophysiol. 39925–935.

    Google Scholar 

  • Crow, T. (1983). Conditioned modification of locomotion in Hermissenda crassicornis: Analysis of time-dependent associative and non-associative components.J. Neurosci. 32621–2628.

    Google Scholar 

  • DiGiorgio, A. M. (1929). Persistenza nell'animale spinale, di asymmetrie posturali e motorie di origine cerebellare.Arch. Fisiol. 27519–542.

    Google Scholar 

  • Dittmer, D. S. (Ed.) (1961).Biological Handbook: Blood and Other Body Fluids, Fed. Am. Soc. Exp. Biol., Washington, D.C., pp. 388–389.

    Google Scholar 

  • Eldred, E., Schnitzlain, H., and Buchwald, J. (1960). Response of muscle spindles to stimulation of sympathetic truck.Exp. Neurol. 213–25.

    Google Scholar 

  • Evarts, E. V., and Granit, R. (1976). Relations of reflexes and intended movements.Prog. Brain Res. 441–14.

    Google Scholar 

  • Evarts, E. V., and Tanji, J. (1974). Gating of motor cortex reflexes by prior instruction.Brain Res. 71479–494.

    Google Scholar 

  • Gerard, R. W. (1961). The fixation of experience. InBrain Mechanisms and Learning (Gerard, R. W., and Konorski, J., Eds.), Blackwell, Oxford, pp. 21–32.

    Google Scholar 

  • Gonshor, A., and Melvill Jones, G. (1971). Plasticity in the adult human vestibulo-ocular reflex arc.Proc. Can. Fed. Biol. Soc. 1411.

    Google Scholar 

  • Goode, D. J. (1982). Loss of patellar and Achilles tendon reflexes in classical ballet dancers.Arch. Neurol. 39323.

    Google Scholar 

  • Gormezano, I., Schniederman, N., Deaux, E., and Fuentes, I. (1962). Nictitating membrane: Classical conditioning and extinction in the albino rabbit.Science 13833–34.

    Google Scholar 

  • Gottlieb, G. L., and Agarwal, G. C. (1979). Responses to sudden torques about ankle in man: Myotatic reflex.J. Neurophysiol. 4291–106.

    Google Scholar 

  • Hagbarth, K.- E. (1967). EMG studies of stretch reflexes in man.Electroencephalogr. Clin. Neurophysiol. Suppl. 2574–79.

    Google Scholar 

  • Hammond, P. H. (1956). The influence of prior instruction to the subject on an apparently involuntary neuromuscular response.J. Physiol. 13217P-18P.

    Google Scholar 

  • Harris, D. A., and Henneman, E. (1980). Feedback signals from muscle and their efferent control. InMedical Physiology, Vol. 1 (Mountcastle, V. B., Ed.), Mosby, St. Louis, pp. 703–717.

    Google Scholar 

  • Henneman, E., and Mendell, L. M. (1981). Functional organization of motoneuron pool and inputs. InHandbook of Physiology. Sect. I. The Nervous System. Vol. II. Motor Control. Part I (Brooks, V. B., Ed.), Williams and Wilkins, Baltimore, pp. 423–507.

    Google Scholar 

  • Hill, W. C. O. (1974).Primates. Vol. VII. Cynopithecinae, Wiley, New York, pp. 551–552, 626-627, 672-673, et passim.

    Google Scholar 

  • Horowitz, B. (1981). Neuronal plasticity: How changes in dendritic architecture can affect spread of postsynaptic potentials.Brain Res. 224412–418.

    Google Scholar 

  • Houk, J. C., and Rymer, W. Z. (1981). Neural control of muscle length and tension. InHandbook of Physiology. Sect. I. The Nervous System. Vol. II. Motor Control. Part I (Brooks, V. B., Ed.), Williams and Wilkins, Baltimore, pp. 257–323.

    Google Scholar 

  • Hunt, C. (1960). The effect of sympathetic stimulation on mammalian muscle spindles.J. Physiol. (Lond.)151332–341.

    Google Scholar 

  • Iles, J. F. (1977). Responses in human pretibial muscles to sudden stretch and nerve stimulation.Exp. Brain Res. 30451–470.

    Google Scholar 

  • Ito, M. (1982). Cerebellar control of the vestibulo-ocular reflex: Around the flocculus hypothesis.Annu. Rev. Neurosci. 5275–296.

    Google Scholar 

  • Jendrassik, E. (1883). Beitrage zur lehre von den sehnenreflexen.Deut. Arch. Klin. Med. 33177–199.

    Google Scholar 

  • Kandel, E. R., and Schwartz, J. H. (1982). Molecular biology of learning: Modulation of transmitter release.Science 218433–443.

    Google Scholar 

  • Kandel, E. R., and Spencer, W. A. (1968). Cellular neurophysiological approaches in the study of learning.Physiol. Rev. 4865–134.

    Google Scholar 

  • Lee, R. G., and Tatton, W. G. (1975). Motor responses to sudden limb displacements in primates with specific CNS lesions and in human patients with motor system disorders.Can. J. Neurol. Sci. 2285–293.

    Google Scholar 

  • Lloyd, D. P. C. (1949). Post-tetanic potentiation of response in monosynaptic reflex pathways of the spinal cord.J. Gen. Physiol. 33147–170.

    Google Scholar 

  • Lundberg, A. (1967). The supraspinal control of transmission in spinal reflex pathways.Electroencephalogr. Clin. Neurophysiol. 2535–46.

    Google Scholar 

  • Lynch, G., and Baudry, M. (1984). The biochemistry of memory: A new and specific hypothesis.Science 2241057–1063.

    Google Scholar 

  • Mandl, G., Melvill Jones, G., and Cynader, M. (1981). Adaptability of the vestibulo-ocular reflex to vision reversal in strobe reared cats.Brain Res. 20935–45.

    Google Scholar 

  • Manni, E. (1950). Localizzazoni cerebellari corticali nella cavia. Nota 1: Il “corpus cerebelli.”Arch. Fisiol. 49213–237.

    Google Scholar 

  • Matthews, P. B. C. (1972).Mammalian Muscle Receptors and Their Central Actions, Williams and Wilkins, Baltimore, pp. 319–409 et passim.

    Google Scholar 

  • Matthews, P. B. C. (1981). Muscle spindles: Their messages and their fusimotor supply. InHandbook of Physiology, Sect. II. The Nervous System. Vol. II. Motor Control. Part I (Brooks, V. B., Ed.), Williams and Wilkins, Baltimore, pp. 43–106.

    Google Scholar 

  • McGough, G. P. (1924). The relation of the pyramidal tract to spinal shock.Am. J. Physiol. 71137–152.

    Google Scholar 

  • Mendell, L. M. (1984). Modifiability of spinal synapses.Physiol. Rev. 64260–324.

    Google Scholar 

  • Miles, F. A., and Lisberger, S. C. (1981). Plasticity in the vestibulo-ocular reflex: A new hypothesis.Annu. Rev. Neurosci. 4273–299.

    Google Scholar 

  • Mountcastle, V. B. (1980). Effects of spinal cord transection. InMedical Physiology, Vol. 1 (Mountcastle, V. B., Ed.), Mosby, St. Louis, pp. 781–786.

    Google Scholar 

  • Myklebust, B. (1983). Development of stretch reflexes. Am. Acad. Cerebr. Palsy Dev. Med. Annu. Mtg., Chicago.

    Google Scholar 

  • Myklebust, B. M., Gottlieb, G. L., Penn, R. L., and Agarwal, G. C. (1982). Reciprocal excitation of antagonistic muscles as a differentiating feature in spasticity.Ann. Neurol. 12367–374.

    Google Scholar 

  • Naftchi, N. E. (Ed.) (1979).Spinal Cord Injury, Spectrum, New York, 1982.

    Google Scholar 

  • Nelson, S. G., and Mendell, L. M. (1979). Enhancement in Ia-motoneuron synaptic transmission caudal to chronic spinal cord transection.J. Neurophysiol. 42642–654.

    Google Scholar 

  • Passatore, M., and Filippi, G. M. (1981). On whether there is a direct sympathetic influence on jaw muscle spindles.Brain Res. 219162–165.

    Google Scholar 

  • Patterson, M. M. (1980). Mechanisms of classical conditioning of spinal reflexes. InNeural Mechanisms of Goal-Directed Behavior and Learning (Thompson, R. F., Hicks, L. H., and Shvyrkov, V. B., Eds.), Academic, New York, pp. 263–272.

    Google Scholar 

  • Rall, W. (1974). Dendritic spines, synaptic potency and neuronal plasticity. InCellular Mechanisms Subserving Changes in Neuronal Activity (Woody, C. D., Brown, K. A., Crow, T. J., Jr., and Knispel, J. D., Eds.), Brain Information Service, Los Angeles, pp. 13–22.

    Google Scholar 

  • Rothwell, J. C., Traub, M. M., and Marsden, C. D. (1980). Influence of voluntary intent on the human long-latency stretch reflex.Nature 286496–498.

    Google Scholar 

  • Stein, R. B. (1983). What variable(s) does the nervous system control in limb movements?Behav. Brain Sci. 5535–577.

    Google Scholar 

  • Sypert, G. W., Fleshman, J. W., and Munson, J. B. (1980). Comparison of monosynaptic actions of medial gastrocnemius group Ia and group II muscle spindle afferents on triceps surae motoneurons.J. Neurophysiol. 44726–738.

    Google Scholar 

  • Taylor, A., and Prochazka, A. (Eds.) (1981).Muscle Receptors and Movement, Oxford University Press, New York, pp. 83–294.

    Google Scholar 

  • Teyler, T. J., and Discenna, P. (1984). Long-term potentiation as a candidate mnemonic device.Brain Res. Rev. 715–28.

    Google Scholar 

  • Thompson, R. F. (1983). Neuronal substrates of simple associative learning: Classical conditioning.Trends Neurosci. 6270–275.

    Google Scholar 

  • Thompson, R. F., Berger, T. W., and Madden, J., IV (1983).Annu. Rev. Neurosci. 6447–491.

    Google Scholar 

  • Vallbo, Å. B. (1974). Human muscle spindle discharge during isometric voluntary contractions. Amplitude relationships between spindle frequency and torque.Acta Physiol. Scand. 90319–336.

    Google Scholar 

  • Wolpaw, J. R. (1982). Reflexes capable of change: Models for the study of memory.Fed. Proc. 412146.

    Google Scholar 

  • Wolpaw, J. R. (1983). Adaptive plasticity in the primate spinal stretch reflex: Reversal and re-development.Brain Res. 278299–304.

    Google Scholar 

  • Wolpaw, J. R., and O'Keefe, J. A. (1984). Adaptive plasticity in the primate spinal stretch reflex: Evidence for a two-phase process.J. Neurosci. 42718–2724.

    Google Scholar 

  • Wolpaw, J. R., and Seegal, R. F. (1982). Diurnal rhythm in the spinal stretch reflex.Brain Res. 244365–369.

    Google Scholar 

  • Wolpaw, J. R., Kieffer, V. A., Seegal, R. F., Braitman, D. J., and Sanders, M. G. (1983a). Adaptive plasticity in the spinal stretch reflex.Brain Res. 267196–200.

    Google Scholar 

  • Wolpaw, J. R., Braitman, D. J., and Seegal, R. F. (1983b). Adaptive plasticity in the primate spinal stretch reflex: Initial development.J. Neurophysiol. 501296–1311.

    Google Scholar 

  • Wolpaw, J. R., Seegal, R. F., and O'Keefe, J. A. (1983c). Adaptive plasticity in the primate spinal stretch reflex: Behavior of synergist and antagonist muscles.J. Neurophysiol. 501312–1319.

    Google Scholar 

  • Wolpaw, J. R., Noonan, P. A., and O'Keefe, J. A. (1984). Adaptive plasticity and diurnal rhythm in the primate spinal stretch reflex are independent phenomena.Brain Res. 300385–391.

    Google Scholar 

  • Woody, C. D. (1982). Neurophysiologic correlates of latent facilitation. InConditioning: Representation of Involved Neural Function (Woody, C. D., Ed.), Plenum, New York, pp. 233–248.

    Google Scholar 

  • Woody, C. D., and Black-Cleworth, P. (1973). Differences in excitability of cortical neurons as a function of motor projection in conditioned cats.J. Neurophysiol. 361104–1116.

    Google Scholar 

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Wolpaw, J.R. Adaptive plasticity in the spinal stretch reflex: An accessible substrate of memory?. Cell Mol Neurobiol 5, 147–165 (1985). https://doi.org/10.1007/BF00711090

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