Firing Properties of Spinal Interneurons during Voluntary Movement. I. State-Dependent Regularity of Firing

The firing properties of single spinal interneurons (INs) were studied in five awake, behaving monkeys performing isometric or auxotonic flexion-extension torques at the wrist. INs tended to fire tonically at rest (mean rate, 14 spikes (sp)/sec) and during generation of static torque (mean rate, 19 sp/sec in flexion, 24 sp/sec in extension). INs exhibited regular firing, with autocorrelation functions showing clear periodic features and a mean coefficient of variation of interspike intervals (CV) of 0.55 during production of static torque. For the population, there was an inverse correlation between CV and mean rate. However, 46% of the INs had task-dependent changes in regularity that were not predicted by changes in firing rate, suggesting that their firing pattern is determined not only by the intrinsic properties of the neurons but also by the properties of its synaptic inputs. INs showed two main response types to passive wrist displacement: biphasic and coactivation. Cells with these sensory responses had different, stereotypical temporal activity profiles and firing regularity during active movement. However, INs having correlational linkages with forearm muscles, identified as features in spike-triggered averages of electromyographic activity, did not exhibit unique responses or firing properties, although they tended to fire more regularly than other INs. This suggests the lack of a precise mapping of inputs to outputs for the spinal premotor network.

[1]  P. Alstrøm,et al.  Characterization of reliability of spike timing in spinal interneurons during oscillating inputs. , 2001, Journal of neurophysiology.

[2]  J. Vedel,et al.  Firing pattern of type‐identified wrist extensor motor units during wrist extension and hand clenching in humans , 1997, The Journal of physiology.

[3]  F. Plum Handbook of Physiology. , 1960 .

[4]  J. Tanji,et al.  Discharges of single motor units at voluntary contraction of abductor digiti minimi muscle in man. , 1972, Brain research.

[5]  R N Lemon,et al.  Synchronization in monkey motor cortex during a precision grip task. I. Task-dependent modulation in single-unit synchrony. , 2001, Journal of neurophysiology.

[6]  G. P. Moore,et al.  Input-output relations in computer-simulated nerve cells , 1968, Kybernetik.

[7]  C. Stevens,et al.  Synaptic noise and other sources of randomness in motoneuron interspike intervals. , 1968, Journal of neurophysiology.

[8]  O. Kiehn,et al.  Bistability of alpha‐motoneurones in the decerebrate cat and in the acute spinal cat after intravenous 5‐hydroxytryptophan. , 1988, The Journal of physiology.

[9]  E. Fetz,et al.  Activity of spinal interneurons and their effects on forearm muscles during voluntary wrist movements in the monkey. , 1998, Journal of neurophysiology.

[10]  K. Pearson Proprioceptive regulation of locomotion , 1995, Current Opinion in Neurobiology.

[11]  R R Young,et al.  Discharge properties of single motor units in patients with spinal cord injuries , 1993, Muscle & nerve.

[12]  A. Schmied,et al.  Delayed and prolonged effects of a near threshold EPSP on the firing time of human α‐motoneurones , 2002, The Journal of physiology.

[13]  G. P. Moore,et al.  SENSITIVITY OF NEURONES IN APLYSIA TO TEMPORAL PATTERN OF ARRIVING IMPULSES. , 1963, The Journal of experimental biology.

[14]  A. Pastor,et al.  Reversible deafferentation of abducens motoneurons and internuclear neurons with tetanus neurotoxin , 2001, Neuroreport.

[15]  R K Powers,et al.  Relationship between the time course of the afterhyperpolarization and discharge variability in cat spinal motoneurones , 2000, The Journal of physiology.

[16]  William R. Softky,et al.  The highly irregular firing of cortical cells is inconsistent with temporal integration of random EPSPs , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[17]  O. Prospero-Garcia,et al.  Reliability of Spike Timing in Neocortical Neurons , 1995 .

[18]  E. Fetz,et al.  Functional classes of primate corticomotoneuronal cells and their relation to active force. , 1980, Journal of neurophysiology.

[19]  W Wolf,et al.  Discharge pattern of single motor units in basal ganglia disorders , 1986, Neurology.

[20]  A. Aertsen,et al.  Spike synchronization and rate modulation differentially involved in motor cortical function. , 1997, Science.

[21]  R. Person,et al.  Discharge frequency and discharge pattern of human motor units during voluntary contraction of muscle. , 1972, Electroencephalography and clinical neurophysiology.

[22]  E. Fetz,et al.  Responses of identified cells in postcentral cortex of awake monkeys during comparable active and passive joint movements. , 1980, Journal of neurophysiology.

[23]  E. Fetz,et al.  Primate spinal interneurons show pre-movement instructed delay activity , 1999, Nature.

[24]  M. Piotrkiewicz An influence of afterhyperpolarization on the pattern of motoneuronal rhythmic activity , 1999, Journal of Physiology-Paris.

[25]  Charles J. Wilson,et al.  Spontaneous Activity of Neostriatal Cholinergic Interneurons In Vitro , 1999, The Journal of Neuroscience.

[26]  C. Stevens,et al.  Input synchrony and the irregular firing of cortical neurons , 1998, Nature Neuroscience.

[27]  A. Rees,et al.  Regularity of firing of neurons in the inferior colliculus. , 1997, Journal of neurophysiology.

[28]  S. Fung,et al.  Serotonin, norepinephrine and associated neuropeptides: effects on somatic motoneuron excitability. , 1996, Progress in brain research.

[29]  P. Harrison,et al.  Organization of input to the interneurones mediating group I non‐reciprocal inhibition of motoneurones in the cat. , 1985, The Journal of physiology.

[30]  '. B.Vallbo Properties of cutaneous mechanoreceptors in the human hand-related to touch sensation , 1999 .

[31]  O Kiehn,et al.  Population reconstruction of the locomotor cycle from interneuron activity in the mammalian spinal cord. , 2000, Journal of neurophysiology.

[32]  B. Jacobs,et al.  Activity of medullary serotonergic neurons in freely moving animals , 2002, Brain Research Reviews.

[33]  Ole Kiehn,et al.  Firing Properties of Identified Interneuron Populations in the Mammalian Hindlimb Central Pattern Generator , 2002, The Journal of Neuroscience.

[34]  J. Feldman,et al.  Synaptic control of motoneuronal excitability. , 2000, Physiological reviews.

[35]  W. Shofner,et al.  Regularity and latency of units in ventral cochlear nucleus: implications for unit classification and generation of response properties. , 1988, Journal of neurophysiology.

[36]  J Rinzel,et al.  Influence of temporal correlation of synaptic input on the rate and variability of firing in neurons. , 2000, Biophysical journal.

[37]  E. Jankowska,et al.  Effects of monoamines on interneurons in four spinal reflex pathways from group I and/or group II muscle afferents , 2000, The European journal of neuroscience.

[38]  Serge Rossignol,et al.  Low-threshold, short-latency cutaneous reflexes during fictive locomotion in the “semi-chronic” spinal cat , 2004, Experimental Brain Research.

[39]  Yifat Prut,et al.  Firing Properties of Spinal Interneurons during Voluntary Movement. II. Interactions between Spinal Neurons , 2003, The Journal of Neuroscience.

[40]  P. Matthews,et al.  The regularity of primary and secondary muscle spindle afferent discharges , 1969, The Journal of physiology.

[41]  J. Goldberg,et al.  RESPONSE OF NEURONS OF THE SUPERIOR OLIVARY COMPLEX OF THE CAT TO ACOUSTIC STIMULI OF LONG DURATION. , 1964, Journal of neurophysiology.

[42]  C. Heckman,et al.  Synaptic integration in bistable motoneurons. , 1999, Progress in brain research.

[43]  T. Sejnowski,et al.  Impact of Correlated Synaptic Input on Output Firing Rate and Variability in Simple Neuronal Models , 2000, The Journal of Neuroscience.

[44]  J. Boudreau,et al.  WAVE ACTIVITY IN THE SUPERIOR OLIVARY COMPLEX OF THE CAT. , 1964, Journal of neurophysiology.

[45]  E. Fetz,et al.  Response patterns and force relations of monkey spinal interneurons during active wrist movement. , 1998, Journal of neurophysiology.

[46]  S. Edgley,et al.  Inputs to group II‐activated midlumbar interneurones from descending motor pathways in the cat. , 1994, The Journal of physiology.

[47]  J. Abbs,et al.  Finger movement responses of cutaneous mechanoreceptors in the dorsal skin of the human hand. , 1991, Journal of neurophysiology.

[48]  R. Burke,et al.  Disynaptic excitation from the medial longitudinal fasciculus to lumbosacral motoneurons: modulation by repetitive activation, descending pathways, and locomotion , 2004, Experimental Brain Research.

[49]  M. Abeles,et al.  Transmission of information by the axon: II. The channel capacity , 2004, Biological Cybernetics.

[50]  A. P. Georgopoulos,et al.  Variability and Correlated Noise in the Discharge of Neurons in Motor and Parietal Areas of the Primate Cortex , 1998, The Journal of Neuroscience.