Subthreshold activation of spinal motoneurones in the stretch reflex: experimental data and modeling

Responses of gastrocnemius–soleus motoneurones to stretches of the homonymous muscles were recorded intrasomatically in decerebrate cats; changes of membrane potential (MP) were evoked by smoothed trapezoid stretches of the muscles. Amplitudes of separate excitatory postsynaptic potentials (EPSPs) were defined via differences between values of MP at the end and beginning of the positive derivative waves, which were also used as basic elements in the model of the excitatory postsynaptic currents (EPSCs). EPSCs were assumed to be transformed into EPSPs by low-pass filtering properties of the somatic membrane; parameters of the filtering were firstly defined from analysis of Ia EPSP in the same cell and then were applied in model Pm0. The model showed unsatisfactory quality in tracking slow components of MP; to overcome the disadvantage there was proposed model Pm1 based on addition to Pm0 the difference between two low-pass filtered signals MP and Pm0 (the cutoff frequency 10 or 20 Hz). An overestimation of EPSPs’ amplitudes was corrected in model Pm2. The mismatch in tracking slow changes of MP was assumed to be connected with summation of a great number of low-amplitude EPSPs generated at distal dendrites; information about waveform of separate EPSPs could disappear in this process. One can speculate that slow components of membrane depolarization at least partly are linked with the persistent inward currents in dendrites; variable and, sometimes, too fast decays in EPSPs seem to reflect inhibitory synaptic influences.

[1]  C. Heckman,et al.  Influence of active dendritic currents on input-output processing in spinal motoneurons in vivo. , 2003, Journal of neurophysiology.

[2]  Michael Rudolph,et al.  Note on “ Characterization of subthreshold voltage fluctuations in neuronal membranes ” , 2008 .

[3]  W. Rall Distinguishing theoretical synaptic potentials computed for different soma-dendritic distributions of synaptic input. , 1967, Journal of neurophysiology.

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

[5]  T. Sejnowski,et al.  Synaptic background noise controls the input/output characteristics of single cells in an in vitro model of in vivo activity , 2003, Neuroscience.

[6]  H. Hultborn,et al.  Voltage-dependent excitation of motoneurones from spinal locomotor centres in the cat , 2004, Experimental Brain Research.

[7]  Ole Petter Ottersen,et al.  Distribution of glutamate-, glycine- and GABA-immunoreactive nerve terminals on dendrites in the cat spinal motor nucleus , 1998, Experimental Brain Research.

[8]  J. Eccles Membrane time constants of cat motoneurons and time courses of synptic action. , 1961, Experimental neurology.

[9]  R K Powers,et al.  Amplification and linear summation of synaptic effects on motoneuron firing rate. , 2001, Journal of neurophysiology.

[10]  R E Burke,et al.  Composite nature of the monosynaptic excitatory postsynaptic potential. , 1967, Journal of neurophysiology.

[11]  U. Windhorst,et al.  Renshaw cell responses to intra-arterial injection of muscle metabolites into cat calf muscles , 1997, Neuroscience Research.

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

[13]  A. I. Kostyukov,et al.  Muscle hysteresis and movement control: A theoretical study , 1998, Neuroscience.

[14]  W. Rall Membrane potential transients and membrane time constant of motoneurons. , 1960, Experimental neurology.

[15]  R. Brownstone,et al.  Characterization of calcium currents in functionally mature mouse spinal motoneurons , 2000, The European journal of neuroscience.

[16]  L. Jami,et al.  Contraction-induced excitation in cat peroneal motoneurons. , 1995, Journal of neurophysiology.

[17]  Z. Siwy,et al.  Origin of 1/f(alpha) noise in membrane channel currents. , 2002, Physical review letters.

[18]  Louis J. DeFelice,et al.  Introduction to membrane noise , 1981 .

[19]  M. Binder Integration of synaptic and intrinsic dendritic currents in cat spinal motoneurons , 2002, Brain Research Reviews.

[20]  N. Spruston,et al.  Diversity and dynamics of dendritic signaling. , 2000, Science.

[21]  U. Windhorst,et al.  Effects in feline gastrocnemius-soleus motoneurones induced by muscle fatigue , 2005, Experimental Brain Research.

[22]  M. Binder,et al.  Summation of effective synaptic currents and firing rate modulation in cat spinal motoneurons. , 2000, Journal of neurophysiology.

[23]  D. Kernell,et al.  Size and remoteness: two relatively independent parameters of dendrites, as studied for spinal motoneurones of the cat. , 1989, The Journal of physiology.

[24]  A. Destexhe,et al.  The high-conductance state of neocortical neurons in vivo , 2003, Nature Reviews Neuroscience.

[25]  C. Heckman,et al.  Active properties of motoneurone dendrites: diffuse descending neuromodulation, focused local inhibition , 2008, The Journal of physiology.

[26]  L. Jami,et al.  Effects on peroneal motoneurons of cutaneous afferents activated by mechanical or electrical stimulations. , 2000, Journal of neurophysiology.

[27]  J. Storm-Mathisen,et al.  Ia boutons to CCN neurones and motoneurones are enriched with glutamate-like immunoreactivity. , 1995, Neuroreport.

[28]  S. Gandevia Spinal and supraspinal factors in human muscle fatigue. , 2001, Physiological reviews.

[29]  I. B. Kulagina,et al.  Activity‐dependent reconfiguration of the effective dendritic field of motoneurons , 2000, The Journal of comparative neurology.

[30]  A. G. Brown,et al.  Direct observations on the contacts made between Ia afferent fibres and alpha‐motoneurones in the cat's lumbosacral spinal cord. , 1981, The Journal of physiology.

[31]  W Rall,et al.  Dendritic location of synapses and possible mechanisms for the monosynaptic EPSP in motoneurons. , 1967, Journal of neurophysiology.

[32]  L. Ting,et al.  Positive proprioceptive feedback elicited by isometric contractions of ankle flexors on pretibial motoneurons in cats. , 2002, Journal of neurophysiology.

[33]  E. Schomburg Spinal sensorimotor systems and their supraspinal control , 1990, Neuroscience Research.

[34]  A. Lundberg,et al.  Spatial synaptic distribution of recurrent and group Ia inhibitory systems in cat spinal motoneurones , 1971, The Journal of physiology.

[35]  M. Binder,et al.  Synaptic integration in spinal motoneurones , 1999, Journal of Physiology-Paris.

[36]  M. Taussig The Nervous System , 1991 .

[37]  W. Rall Core Conductor Theory and Cable Properties of Neurons , 2011 .

[38]  W. Webb,et al.  Conductivity noise in transmembrane ion channels due to ion concentration fluctuations via diffusion. , 1997, Biophysical journal.

[39]  S. Bezrukov,et al.  Noise in Biological Membranes and Relevant Ionic Systems , 1994 .

[40]  J. Jack,et al.  Electric current flow in excitable cells , 1975 .

[41]  M D Binder,et al.  Analysis of effective synaptic currents generated by homonymous Ia afferent fibers in motoneurons of the cat. , 1988, Journal of neurophysiology.

[42]  Idan Segev,et al.  Synaptic integration mechanisms. Theoretical and experimental investigation of temporal postsynaptic interactions between excitatory and inhibitory inputs. , 1983, Biophysical journal.

[43]  J. Eccles,et al.  The time courses of excitatory and inhibitory synaptic actions , 1959, The Journal of physiology.