scholarly journals Synaptic control of the shape of the motoneuron pool input-output function

2017 ◽  
Vol 117 (3) ◽  
pp. 1171-1184 ◽  
Author(s):  
Randall K. Powers ◽  
Charles J. Heckman
Keyword(s):  
Synaptic Input ◽  
Excitatory Input ◽  
Motor Output ◽  
Medial Gastrocnemius ◽  
Output Function ◽  
Input Output ◽  
Synaptic Inputs ◽  
Motoneuron Pool ◽  
Synaptic Control ◽  
Excitatory Drive

Although motoneurons have often been considered to be fairly linear transducers of synaptic input, recent evidence suggests that strong persistent inward currents (PICs) in motoneurons allow neuromodulatory and inhibitory synaptic inputs to induce large nonlinearities in the relation between the level of excitatory input and motor output. To try to estimate the possible extent of this nonlinearity, we developed a pool of model motoneurons designed to replicate the characteristics of motoneuron input-output properties measured in medial gastrocnemius motoneurons in the decerebrate cat with voltage-clamp and current-clamp techniques. We drove the model pool with a range of synaptic inputs consisting of various mixtures of excitation, inhibition, and neuromodulation. We then looked at the relation between excitatory drive and total pool output. Our results revealed that the PICs not only enhance gain but also induce a strong nonlinearity in the relation between the average firing rate of the motoneuron pool and the level of excitatory input. The relation between the total simulated force output and input was somewhat more linear because of higher force outputs in later-recruited units. We also found that the nonlinearity can be increased by increasing neuromodulatory input and/or balanced inhibitory input and minimized by a reciprocal, push-pull pattern of inhibition. We consider the possibility that a flexible input-output function may allow motor output to be tuned to match the widely varying demands of the normal motor repertoire. NEW & NOTEWORTHY Motoneuron activity is generally considered to reflect the level of excitatory drive. However, the activation of voltage-dependent intrinsic conductances can distort the relation between excitatory drive and the total output of a pool of motoneurons. Using a pool of realistic motoneuron models, we show that pool output can be a highly nonlinear function of synaptic input but linearity can be achieved through adjusting the time course of excitatory and inhibitory synaptic inputs.

Computer simulations of the effects of different synaptic input systems on motor unit recruitment

1993 ◽  
Vol 70 (5) ◽  
pp. 1827-1840 ◽  
Author(s):  
C. J. Heckman ◽  
M. D. Binder
Keyword(s):  
Motor Unit ◽  
Computer Simulations ◽  
Synaptic Input ◽  
Reciprocal Inhibition ◽  
Excitatory Input ◽  
Medial Gastrocnemius ◽  
Synaptic Inputs ◽  
Monte Carlo Techniques ◽  
Recruitment Order ◽  
Random Variance

1. The effects of four different synaptic input systems on the recruitment order within a mammalian motoneuron pool were investigated using computer simulations. The synaptic inputs and motor unit properties in the model were based as closely as possible on the available experimental data for the cat medial gastrocnemius pool and muscle. Monte Carlo techniques were employed to add random variance to the motor unit thresholds and forces and to sample the resulting recruitment orders. 2. The effects of the synaptic inputs on recruitment order depended on how they modified the range of recruitment thresholds established by differences in the intrinsic current thresholds of the motoneurons. Application of a uniform synaptic input to the pool (i.e., distributed equally to all motoneurons) resulted in a recruitment sequence that was quite stable even with the addition of large amounts of random variance. With 50% added random variance, the recruitment reversals did not exceed 8%. 3. The simulated monosynaptic input from homonymous Ia afferent fibers generated a twofold expansion of the range of recruitment thresholds beyond that attributed to the differences in the intrinsic current thresholds. The Ia input generated a small reduction in the number of recruitment reversals due to random variance (6% reversals at 50% random variance). The simulated monosynaptic vestibulospinal input generated a twofold compression of the range of recruitment thresholds that exerted a modest increase in the number of recruitment reversals (12% reversals at 50% random variance). 4. In comparison with the modest effects of the two monosynaptic inputs, the simulated oligosynpatic rubrospinal excitatory input exerted a nine-fold compression in the recruitment threshold range that resulted in a recruitment sequence that was highly sensitive to random variance. With 50% added random variance, the sequence became nearly random (40% reversals). 5. Reciprocal Ia inhibition was simulated by a uniform distribution within the pool, but its effects on recruitment order were highly dependent on the distribution of the excitatory input. Reciprocal inhibition exerted only minor effects on recruitment order when combined with the Ia or vestibulospinal inputs. However, when the excitatory drive was supplied by the rubrospinal input, even small amounts of reciprocal inhibition were sufficient to completely reverse the normal recruitment sequence. 6. The simulated monosynaptic Ia input was highly effective in compensating for the disruptive effects of rubrospinal excitation on recruitment order. Even a small Ia bias combined with the rubrospinal excitation was sufficient to halve the effects of random variance and to restore the normal recruitment sequence in the presence of rather large amounts of reciprocal inhibition.(ABSTRACT TRUNCATED AT 400 WORDS)

Computer simulation of the steady-state input-output function of the cat medial gastrocnemius motoneuron pool

1991 ◽  
Vol 65 (4) ◽  
pp. 952-967 ◽  
Author(s):  
C. J. Heckman ◽  
M. D. Binder
Keyword(s):  
Experimental Data ◽  
Steady State ◽  
Motor Unit ◽  
Frequency Modulation ◽  
Motor Units ◽  
Medial Gastrocnemius ◽  
Output Function ◽  
Input Output ◽  
Motoneuron Pool ◽  
Random Variance

1. A pool of 100 simulated motor units was constructed in which the steady-state neural and mechanical properties of the units were very closely matched to the available experimental data for the cat medial gastrocnemius motoneuron pool and muscle. The resulting neural network generated quantitative predictions of whole system input-output functions based on the single unit data. The results of the simulations were compared with experimental data on normal motor system behavior in humans and animals. 2. We considered only steady-state, isometric conditions. All motoneurons received equal proportions of the synaptic input, and no feedback loops were operative. Thus the intrinsic properties of the motor unit population alone determined the form of the system input-output function. Expressing the synaptic input in terms of effective synaptic current allowed the simulated motoneuron input-output functions to be specified by well-known firing rate-injected current relations. The motor unit forces were determined from standard motor unit force-frequency relations, and the system output at any input level was assumed to be the linear sum of the forces of the active motor units. 3. The steady-state input-output function of the simulated motoneuron pool had a roughly sigmoidal shape that was quite different from those derived from previous recruitment models, which did not incorporate frequency modulation. Frequency modulation in combination with the skewed distribution of thresholds (low values much more frequent than high) restricted upward curvature to low input levels, whereas frequency modulation alone was responsible for the final gradual approach to the maximum force output. 4. Sensitivity analyses were performed to assess the importance of several assumptions that were required to deal with gaps and uncertainties in the available experimental data. The shape of the input-output function was not critically dependent on any of these assumptions, including those specifying linear summation of inputs and outputs. 5. A key assumption of the model was that systematic variance in motor unit properties was much more important than random variance for determining the input-output function. Addition of random variance via Monte Carlo techniques showed that this assumption was correct. These results suggest that the output of a motoneuron pool should be quite tolerant of random variance in the distribution of synaptic inputs and yet substantially altered by any systematic differences, such as unequal distribution of inputs among different motor unit types.(ABSTRACT TRUNCATED AT 400 WORDS)

Computer simulations of the effects of different synaptic input systems on the steady-state input-output structure of the motoneuron pool

1994 ◽  
Vol 71 (5) ◽  
pp. 1727-1739 ◽  
Author(s):  
C. J. Heckman
Keyword(s):  
Steady State ◽  
Motor Unit ◽  
Fatigue Resistance ◽  
Synaptic Input ◽  
Motor Units ◽  
Output Function ◽  
Input Output ◽  
Unit Type ◽  
Motoneuron Pool ◽  
Output Structure

1. The effects of different types of synaptic input on the steady-state input-output relations of the mammalian motoneuron pool were investigated by the use of computer simulations. The properties of the simulated motor units and their synaptic inputs were based as closely as possible on the experimental data from studies in the cat hindlimb. 2. Three basic types of synaptic input systems were simulated: postsynaptic, presynaptic, and neuromodulatory. The effects of these inputs on three aspects of the system input-output structure were studied: gain, precision, and motor-unit type utilization. 3. The gain analyses were based on a simulation of the steady-state homonymous Ia input. The gain of this steady-state Ia “reflex” was found to be determined largely by the slope of the pool input-output function. Precision was evaluated in two ways, from the amplitudes of the quantal steps due to motor-unit recruitment and from the sensitivity of the input-output function to noise. The pattern of motor-unit type utilization allowed indirect assessment of fatigue resistance: the larger the percentage of force generated by FF units, the lower the fatigue resistance. 4. A uniformly distributed input (i.e., one that generates equal input in all motoneurons) generates outputs that are solely determined by the intrinsic properties of the motor units. Thus the gain, precision, and motor-unit type patterns generated by a uniform input were used as the basis with which the effects of all other input systems were compared. 5. Postsynaptic excitatory inputs with nonuniform distributions within the pool did influence gain. The greatest effect was the increase mediated by the rubrospinal excitatory input (27% increase at 30% of maximal force). However, this input also greatly decreased both fatigue resistance and precision, due to increased activation of FF units at low force levels. In contrast, the Ia input slightly decreased gain (12% decrease at 30% of maximum force) while slightly increasing fatigue resistance and precision. 6. The simulated neuromodulatory input was based on the monoaminergic reticulospinal effect on motoneurons. Gain was generally increased by the monoaminergic input. However, the magnitude of the increase strongly depended on whether the monoaminergic effects were largest on S units (giving a 20% increase at 30% of maximum force), equal on all types (52%), or largest on FF units (102%). Presynaptic inhibition reduced gain with no effect whatsoever on fatigue resistance or precision. 7. Therefore Ia reflex gain was modifiable by all three types of input: postsynaptic, presynaptic, and neuromodulatory.(ABSTRACT TRUNCATED AT 400 WORDS)

Analysis of effective synaptic currents generated by homonymous Ia afferent fibers in motoneurons of the cat

1988 ◽  
Vol 60 (6) ◽  
pp. 1946-1966 ◽  
Author(s):  
C. J. Heckman ◽  
M. D. Binder
Keyword(s):  
Steady State ◽  
Synaptic Input ◽  
Input Resistance ◽  
Firing Frequency ◽  
Medial Gastrocnemius ◽  
Synaptic Current ◽  
Synaptic Inputs ◽  
Input System ◽  
Synaptic Potentials ◽  
Ia Epsp

1. We have developed a technique to measure the total amount of current from a synaptic input system that reaches the soma of a motoneuron under steady-state conditions. We refer to this quantity as the effective synaptic current (IN) because only that fraction of the synaptic current that actually reaches the soma and initial segment of the cell affects its recruitment threshold and firing frequency. 2. The advantage of this technique for analysis of synaptic inputs in comparison to the standard measurements of synaptic potentials is apparent from Ohm's law. Steady-state synaptic potentials recorded at the soma of a cell are the product of IN and input resistance (RN), which is determined by intrinsic cellular properties such as cell size and membrane resistivity. Measuring IN avoids the confounding effect of RN on the amplitudes of synaptic potentials and thus provides a more direct assessment of the magnitude of a synaptic input. 3. Steady-state synaptic inputs were generated in cat medial gastrocnemius (MG) motoneurons by using tendon vibration to activate homonymous Ia afferents. We found that the magnitude of the Ia effective synaptic current (Ia IN) was not the same in all MG cells. Instead, Ia IN covaried with RN (r = 0.64; P less than 0.001), being about twice as large on average in motoneurons with high RN values as in those with low RN values. Ia IN was also correlated with motoneuron rheobase, afterhyperpolarization duration, and axonal conduction velocity. 4. A comparison of transient Ia EPSPs with steady-state Ia EPSPs (Ia EPSPSS) evoked in the same cells suggested that the effective synaptic current that produces the transient Ia EPSP was also greater in motoneurons with high RN values than in those with low RN values. 5. The factors responsible for the Ia IN-RN covariance are uncertain. However, our finding greater values of Ia IN in high RN motoneurons is consistent with other evidence suggesting that Ia boutons on these motoneurons have a higher probability for neurotransmitter release than those on low RN motoneurons (19). 6. The neural mechanisms underlying orderly recruitment are discussed. The effect of the Ia input is to produce an approximately twofold expansion of the differences in motoneuron recruitment thresholds that are generated by intrinsic cellular properties. It is suggested that the higher efficacy of Ia input in low-threshold motoneurons confers particular importance on this input system in the control of vernier movements (7).

Modes of activation of motoneurons controlling ventilatory movements of the locust abdomen

1974 ◽  
Vol 269 (896) ◽  
pp. 29-48 ◽  
Keyword(s):  
Synaptic Input ◽  
Ventral Surface ◽  
Excitatory Input ◽  
The Other ◽  
Intracellular Recordings ◽  
Phase 3 ◽  
Synaptic Inputs ◽  
Frequency Code ◽  
Metathoracic Ganglion ◽  
Stimulation Of

1. Intracellular recordings have been made from tonic and phasic expiratory, inspiratory and spiracular motoneurons and presumed sensory integrating neurons of the metathoracic ganglion in a locust during rhythmic ventilatory movements of the abdomen. The neurons have somata with diameters of no more than 30 μm situated on the ventral surface of the ganglion. 2. No motoneurons showed an intrinsic rhythmicity, all being driven in the ventilatory rhythm by complex patterns of synaptic inputs in one of the following ways: ( a ) excitation alone during the phase when spikes are produced (spiracle closer and some tonic expiratory motoneurons); ( b ) excitation during one phase and inhibition during the other (some tonic expiratory motoneurons); ( c ) excitation and inhibition during both phases (most motoneurons) in which one type of input dominates a particular phase. 3. The burst of spikes by a particular motoneuron may end because of a lack of excitatory input (spiracle closer motoneurons) or be terminated rapidly by inhibition (inspiratory motoneurons). Inhibition may also precede the main burst of spikes (inspiratory motoneurons) so that any spikes during the opposite phase are abolished. The pattern of synaptic input determines the frequency code of spikes within a burst. 4. Phasic expiratory motoneurons receive an underlying pattern of synaptic inputs in phase with ventilation even when they do not spike. Non-specific excitation (for example, a d.c. depolarization of the soma) is able to produce bursts of spikes in the correct phase of ventilation. 5. No direct pathway between any groups of motoneurons was found. Driving by common antecedent interneurons is inferred for those motoneurons which show similar patterns of spikes (inspiratory and spiracle closer motoneurons). 6. Stimulation of descending fibres in the pro-mesothoracic connectives evokes e.p.s.ps in some motoneurons, perhaps monosynaptically. In inspiratory motoneurons these fibres cause e.p.s.ps but will abolish the inspiratory burst of spikes and reset the ventilatory rhythm. All observations imply that the mechanism of the ventilatory rhythm lies among interneurons.

scholarly journals Frequency-dependent amplification of stretch-evoked excitatory input in spinal motoneurons

2012 ◽  
Vol 108 (3) ◽  
pp. 753-759 ◽  
Author(s):  
Randall K. Powers ◽  
Paul Nardelli ◽  
T. C. Cope
Keyword(s):  
Membrane Potential ◽  
Low Frequency ◽  
Excitatory Input ◽  
Medial Gastrocnemius ◽  
Frequency Dependent ◽  
Fast Kinetics ◽  
Synaptic Inputs ◽  
Slow Kinetics ◽  
Voltage Dependent ◽  
Inward Currents

Voltage-dependent calcium and sodium channels mediating persistent inward currents (PICs) amplify the effects of synaptic inputs on the membrane potential and firing rate of motoneurons. CaPIC channels are thought to be relatively slow, whereas the NaPIC channels have fast kinetics. These different characteristics influence how synaptic inputs with different frequency content are amplified; the slow kinetics of Ca channels suggest that they can only contribute to amplification of low frequency inputs (<5 Hz). To characterize frequency-dependent amplification of excitatory postsynaptic potentials (EPSPs), we measured the averaged stretch-evoked EPSPs in cat medial gastrocnemius motoneurons in decerebrate cats at different subthreshold levels of membrane potential. EPSPs were produced by muscle spindle afferents activated by stretching the homonymous and synergist muscles at frequencies of 5–50 Hz. We adjusted the stretch amplitudes at different frequencies to produce approximately the same peak-to-peak EPSP amplitude and quantified the amount of amplification by expressing the EPSP integral at different levels of depolarization as a percentage of that measured with the membrane hyperpolarized. Amplification was observed at all stretch frequencies but generally decreased with increasing stretch frequency. However, in many cells the amount of amplification was greater at 10 Hz than at 5 Hz. Fast amplification was generally reduced or absent when the lidocaine derivative QX-314 was included in the electrode solution, supporting a strong contribution from Na channels. These results suggest that NaPICs can combine with CaPICs to enhance motoneuron responses to modulations of synaptic drive over a physiologically significant range of frequencies.

scholarly journals Amplification and Linear Summation of Synaptic Effects on Motoneuron Firing Rate

2001 ◽  
Vol 85 (1) ◽  
pp. 43-53 ◽  
Author(s):  
Jonathan F. Prather ◽  
Randall K. Powers ◽  
Timothy C. Cope
Keyword(s):  
Firing Rate ◽  
Synaptic Input ◽  
Synaptic Integration ◽  
Medial Gastrocnemius ◽  
Resting Potential ◽  
Repetitive Firing ◽  
Linear Summation ◽  
Decerebrate Cat ◽  
Inward Current ◽  
Synaptic Inputs

The aim of this study was to measure the effects of synaptic input on motoneuron firing rate in an unanesthetized cat preparation, where activation of voltage-sensitive dendritic conductances may influence synaptic integration and repetitive firing. In anesthetized cats, the change in firing rate produced by a steady synaptic input is approximately equal to the product of the effective synaptic current measured at the resting potential ( I N) and the slope of the linear relation between somatically injected current and motoneuron discharge rate ( f-I slope). However, previous studies in the unanesthetized decerebrate cat indicate that firing rate modulation may be strongly influenced by voltage-dependent dendritic conductances. To quantify the effects of these conductances on motoneuron firing behavior, we injected suprathreshold current steps into medial gastrocnemius motoneurons of decerebrate cats and measured the changes in firing rate produced by superimposed excitatory synaptic input. In the same cells, we measured I N and the f-I slope to determine the predicted change in firing rate (Δ F = I N * f-I slope). In contrast to previous results in anesthetized cats, synaptically induced changes in motoneuron firing rate were greater-than-predicted. This enhanced effect indicates that additional inward current was present during repetitive firing. This additional inward current amplified the effective synaptic currents produced by two different excitatory sources, group Ia muscle spindle afferents and caudal cutaneous sural nerve afferents. There was a trend toward more prevalent amplification of the Ia input (14/16 cells) than the sural input (11/16 cells). However, in those cells where both inputs were amplified (10/16 cells), amplification was similar in magnitude for each source. When these two synaptic inputs were simultaneously activated, their combined effect was generally very close to the linear sum of their amplified individual effects. Linear summation is also observed in medial gastrocnemius motoneurons of anesthetized cats, where amplification is not present. This similarity suggests that amplification does not disturb the processes of synaptic integration. Linear summation of amplified input was evident for the two segmental inputs studied here. If these phenomena also hold for other synaptic sources, then the presence of active dendritic conductances underlying amplification might enable motoneurons to integrate multiple synaptic inputs and drive motoneuron firing rates throughout the entire physiological range in a relatively simple fashion.

scholarly journals Identification of Brain Electrical Activity Related to Head Yaw Rotations

Sensors ◽  
2021 ◽  
Vol 21 (10) ◽  
pp. 3345
Author(s):  
Enrico Zero ◽  
Chiara Bersani ◽  
Roberto Sacile
Keyword(s):  
Electrical Activity ◽  
Electrical Stimulus ◽  
Head Movements ◽  
Brain Electrical Activity ◽  
Output Function ◽  
Input Output ◽  
Eeg Signals ◽  
Head Turning ◽  
Identification Technique ◽  
The Brain

Automatizing the identification of human brain stimuli during head movements could lead towards a significant step forward for human computer interaction (HCI), with important applications for severely impaired people and for robotics. In this paper, a neural network-based identification technique is presented to recognize, by EEG signals, the participant’s head yaw rotations when they are subjected to visual stimulus. The goal is to identify an input-output function between the brain electrical activity and the head movement triggered by switching on/off a light on the participant’s left/right hand side. This identification process is based on “Levenberg–Marquardt” backpropagation algorithm. The results obtained on ten participants, spanning more than two hours of experiments, show the ability of the proposed approach in identifying the brain electrical stimulus associate with head turning. A first analysis is computed to the EEG signals associated to each experiment for each participant. The accuracy of prediction is demonstrated by a significant correlation between training and test trials of the same file, which, in the best case, reaches value r = 0.98 with MSE = 0.02. In a second analysis, the input output function trained on the EEG signals of one participant is tested on the EEG signals by other participants. In this case, the low correlation coefficient values demonstrated that the classifier performances decreases when it is trained and tested on different subjects.

scholarly journals Circuit contributions to sensory-driven glutamatergic drive of olfactory bulb mitral and tufted cells during odorant inhalation

2021 ◽  
Author(s):  
Andrew K. Moran ◽  
Thomas P. Eiting ◽  
Matt Wachowiak
Keyword(s):  
Olfactory Bulb ◽  
Gabab Receptor ◽  
Glutamate Release ◽  
Excitatory Input ◽  
Slight Reduction ◽  
Receptor Antagonists ◽  
Glutamate Signaling ◽  
Inhibitory Circuits ◽  
Primary Determinant ◽  
Excitatory Drive

In the mammalian olfactory bulb (OB), mitral/tufted (MT) cells respond to odorant inhalation with diverse temporal patterns that are thought to encode odor information. Much of this diversity is already apparent at the level of glutamatergic input to MT cells, which receive direct, monosynaptic excitatory input from olfactory sensory neurons (OSNs) as well as multisynaptic excitatory drive via glutamatergic interneurons. Both pathways are also subject to modulation by inhibitory circuits in the glomerular layer of the OB. To understand the role of direct OSN input versus postsynaptic OB circuit mechanisms in shaping diverse dynamics of glutamatergic drive to MT cells, we imaged glutamate signaling onto MT cell dendrites in anesthetized mice while blocking multisynaptic excitatory drive with ionotropic glutamate receptor antagonists and blocking presynaptic modulation of glutamate release from OSNs with GABAB receptor antagonists. GABAB receptor blockade increased the magnitude of inhalation-linked glutamate transients onto MT cell apical dendrites without altering their inhalation-linked dynamics, confirming that presynaptic inhibition impacts the gain of OSN inputs to the OB. Surprisingly, blockade of multisynaptic excitation only modestly impacted glutamatergic input to MT cells, causing a slight reduction in the amplitude of inhalation-linked glutamate transients in response to low odorant concentrations and no change in the dynamics of each transient. Postsynaptic blockade also modestly impacted glutamate dynamics over a slower timescale, mainly by reducing adaptation of the glutamate response across multiple inhalations of odorant. These results suggest that direct glutamatergic input from OSNs provides the bulk of excitatory drive to MT cells, and that diversity in the dynamics of this input may be a primary determinant of the temporal diversity in MT cell responses that underlies odor representations at this stage.

Sign in / Sign up

Export Citation Format

Share Document