Phantom reflexes: Muscle contractions at a frequency not physically present in the input stimuli

In the motor system, the periodic stimulation of one Ia-afferent input produces reflex muscle contractions at the input frequency. However, we observed that when two Ia monosynaptic reflex-afferent inputs are involved the periodic muscle contractions may occur at a frequency physically not present in the afferent inputs even when these inputs are sub-threshold. How can the muscles respond with such phantom reflex contractions at a frequency physically absent in the sub-threshold Ia-afferent input stimuli? Here we provide an explanation for this phenomenon in the cat spinal cord, that we termed "ghost motor response". We recorded monosynaptic reflexes in the L7 ventral root, intracellular potentials in the motoneurons, and the associated muscular contractions elicited by stimulation of the lateral and medial gastrocnemius nerves. By stimulating with periodic pulses of sub-threshold intensities and distinct frequencies of 2 and 3 Hz the lateral and medial gastrocnemius nerves, respectively, we observed monosynaptic responses and phantom reflex muscle contractions occurring at the fundamental frequency (1 Hz), which was absent in the input stimuli. Thus we observed a reflex ghost motor response at a frequency not physically present in the inputs. We additionally studied the inharmonic case for sub-threshold stimuli and observed muscular contractions occurring at much lower frequencies, which were also conspicuously absent in the inputs. This is the first experimental evidence of a phantom reflex response in the nervous system. The observed behavior was modeled by numerical simulations of a pool of neurons subjected to two different input pulses.

[1]  Dante R Chialvo How we hear what is not there: a neural mechanism for the missing fundamental illusion. , 2003, Chaos.

[2]  J. M. Sancho,et al.  Noise in spatially extended systems , 1999 .

[3]  Ramana Dodla,et al.  Subthreshold outward currents enhance temporal integration in auditory neurons , 2003, Biological Cybernetics.

[4]  S. Zhang,et al.  Neuronal circuits associated with the output of the dorsal cochlear nucleus through fusiform cells. , 1994, Journal of neurophysiology.

[5]  Dante R Chialvo,et al.  Ghost stochastic resonance with distributed inputs in pulse-coupled electronic neurons. , 2006, Physical review. E, Statistical, nonlinear, and soft matter physics.

[6]  J. Roll,et al.  Proprioceptive sensory codes mediating movement trajectory perception: human hand vibration-induced drawing illusions. , 1995, Canadian journal of physiology and pharmacology.

[7]  M. Kuno,et al.  Non‐linear summation of unit synaptic potentials in spinal motoneurones of the cat , 1969, The Journal of physiology.

[8]  D. Kernell,et al.  Algebraical summation in synaptic activation of motoneurones firing within the ‘primary range’ to injected currents , 1966, The Journal of physiology.

[9]  P J Cordo,et al.  Representation of wrist joint kinematics by the ensemble of muscle spindles from synergistic muscles. , 1998, Journal of neurophysiology.

[10]  H. Tamaki,et al.  Alternate activity in the synergistic muscles during prolonged low-level contractions. , 1998, Journal of applied physiology.

[11]  K. Zilles,et al.  Illusory Arm Movements Activate Cortical Motor Areas: A Positron Emission Tomography Study , 1999, The Journal of Neuroscience.

[12]  Mark Farrant,et al.  Maturation of EPSCs and Intrinsic Membrane Properties Enhances Precision at a Cerebellar Synapse , 2003, The Journal of Neuroscience.

[13]  C. Morris,et al.  Voltage oscillations in the barnacle giant muscle fiber. , 1981, Biophysical journal.

[14]  Laurence O Trussell,et al.  Cellular mechanisms for preservation of timing in central auditory pathways , 1997, Current Opinion in Neurobiology.

[15]  D. P. Lloyd,et al.  Facilitation and inhibition of spinal motoneurons. , 1946, Journal of neurophysiology.

[16]  Åke Vallbo,et al.  Basic patterns of muscle spindle discharge in man , 1981 .

[17]  Hiroyuki Kitajima,et al.  Bifurcations in Morris-Lecar neuron model , 2006, Neurocomputing.

[18]  E. Manjarrez,et al.  Spinal source for the synchronous fluctuations of bilateral monosynaptic reflexes in cats. , 2005, Journal of neurophysiology.

[19]  T. Sejnowski,et al.  The predictive brain: temporal coincidence and temporal order in synaptic learning mechanisms. , 1994, Learning & memory.

[20]  A. Prochazka,et al.  Muscle Receptors and Movement , 1981, Palgrave Macmillan UK.

[21]  Roll Jp,et al.  Proprioceptive sensory codes mediating movement trajectory perception: human hand vibration-induced drawing illusions. , 1995, Canadian journal of physiology and pharmacology.

[22]  Pablo Balenzuela,et al.  Neural mechanism for binaural pitch perception via ghost stochastic resonance. , 2004, Chaos.

[23]  Michael Rudolph,et al.  Tuning Neocortical Pyramidal Neurons between Integrators and Coincidence Detectors , 2003, Journal of Computational Neuroscience.

[24]  Nace L. Golding,et al.  Synaptic inputs to stellate cells in the ventral cochlear nucleus. , 1998, Journal of neurophysiology.

[25]  S. Gandevia,et al.  Cutaneous receptors contribute to kinesthesia at the index finger, elbow, and knee. , 2005, Journal of neurophysiology.

[26]  H. von Gersdorff,et al.  Fine-Tuning an Auditory Synapse for Speed and Fidelity: Developmental Changes in Presynaptic Waveform, EPSC Kinetics, and Synaptic Plasticity , 2000, The Journal of Neuroscience.

[27]  久場 博司 Development of membrane conductance improves coincidence detection in the nucleus laminaris of the chicken , 2003 .

[28]  D. Burke,et al.  Perceptual responses to microstimulation of single afferents innervating joints, muscles and skin of the human hand. , 1990, The Journal of physiology.

[29]  Gerardo Rojas-Piloni,et al.  Stochastic Resonance within the Somatosensory System: Effects of Noise on Evoked Field Potentials Elicited by Tactile Stimuli , 2003, The Journal of Neuroscience.

[30]  J. Rinzel,et al.  Sodium along with low-threshold potassium currents enhance coincidence detection of subthreshold noisy signals in MSO neurons. , 2004, Journal of neurophysiology.