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Jeanpierre Roll - One of the best experts on this subject based on the ideXlab platform.
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fusimotor drive may adjust Muscle Spindle feedback to task requirements in humans
Journal of Neurophysiology, 2009Co-Authors: Edith Ribotciscar, Valerie Hospod, Jeanpierre Roll, Jeanmarc AimonettiAbstract:The aim of the present study was to investigate whether the fusimotor control of Muscle Spindle sensitivity may depend on the movement parameter the task is focused on, either the velocity or the final position reached. The unitary activities of 18 Muscle Spindle afferents were recorded by microneurography at the common peroneal nerve. We compared in two situations the responses of Muscle Spindle afferents to ankle movements imposed while the subject was instructed not to pay attention to or to pay attention to the movement, both in the absence of visual cues. In the two situations, three ramp-and-hold movements were imposed in random order. In one situation, the three movements differed by their velocity and in the other by the final position reached. The task consisted in ranking the three movements according to the parameter under consideration (for example, slow, fast, and medium). The results showed that paying attention to movement velocity gave rise to a significant increase in the dynamic and static responses of Muscle afferents. In contrast, focusing attention on the final position reached made the Muscle Spindle feedback better discriminate the different positions and depressed its capacity to discriminate movement velocities. Changes are interpreted as reflecting dynamic and static gamma activation, respectively. The present results support the view that the fusimotor drive depends on the parameter the task is focused on, so that the Muscle afferent feedback is adjusted to the task requirements.
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changes in human Muscle Spindle sensitivity during a proprioceptive attention task
The Journal of Neuroscience, 2007Co-Authors: Valerie Hospod, Jeanpierre Roll, Jeanmarc Aimonetti, Edith RibotciscarAbstract:The aim of the present study was to test whether fusimotor control of human Muscle Spindle sensitivity changed when attention was selectively directed to the recognition of an imposed two-dimensional movement in the form of a written symbol. The unitary activities of 32 Muscle Spindle afferents (26 Ia, 6 II) were recorded by microneurography at the level of the common peroneal nerve. The patterns of firing rate in response to passive movements of the ankle, forming different letters or numbers, were compared in two conditions: control and recognition. No visual cues were given in either condition, but subjects had to recognize and name the character in one condition compared with not paying attention in the control condition. The results showed that 58% of the tested Ia afferents presented modified responses to movements when these had to be recognized. Changes in Ia afferent responses included decreased depth of modulation, increased variability of discharge, and changes in spontaneous activity. Not all changes were evident in the same afferent. Furthermore, the percentage of correctly recognized movements amounted to 63% when changes were observed, but it was only 48% when the primary ending sensitivity was unaltered. The responses of group II afferents were only weakly changed or unchanged. It is suggested that the altered Muscle Spindle sensitivity is because of selective changes in fusimotor control, the consequence of which might be to feed the brain movement trajectory information that is more accurate.
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the preferred sensory direction of Muscle Spindle primary endings influences the velocity coding of two dimensional limb movements in humans
Experimental Brain Research, 2002Co-Authors: Edith Ribotciscar, Mikael Bergenheim, Jeanpierre RollAbstract:The present study compares how accurately two different but close velocities of movement are discriminated by populations of Muscle Spindle primary afferents whether or not one takes into account the direction of the movement and the preferred sensory directions of the units (i.e., the direction of movement to which the afferents are the most sensitive). The activities of 26 Muscle Spindle primary endings originating from the tibialis anterior, the extensor digitorum longus, the extensor hallucis longus, and the peroneus lateralis Muscles were recorded in the lateral peroneal nerve. Their responses to movements imposed at two velocities (12.5 and 18 mm/s) were analyzed. These movements were straight-line movements imposed in eight directions and circular movements in both clockwise and anticlockwise directions. The encoding of the movement velocity was analyzed in two ways. First, the mean frequencies of discharge of the Muscle Spindle afferents were compared for the two velocities. Second, the data were analyzed using a “neuronal population vector model.” This model is based on the idea that such neuronal coding can be analyzed in terms of a series of population vectors (i.e., mean contribution of all the Muscle Spindle afferents within one directionally tuned Muscle) and by finally calculating a sum vector. The results showed no clear and consistent difference in the response frequency of the Muscle Spindle afferents for the two velocities of movement compared. Rather, the most consistently significant differences between the two velocities were in the lengths of the sum vectors. It is concluded that the encoding of two-dimensional movement velocity relies on populations of Muscle Spindle afferents coming from the whole set of Muscles surrounding a particular joint, each Muscle making an instantaneous, oriented, and weighted contribution to the sensory coding of the kinematics parameters.
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proprioceptive population coding of two dimensional limb movements in humans i Muscle Spindle feedback during spatially oriented movements
Experimental Brain Research, 2000Co-Authors: Mikael Bergenheim, Edith Ribotciscar, Jeanpierre RollAbstract:The proprioceptive coding of multidirectional ankle joint movements was investigated, focusing in particular on the question as to how accurately the direction of a movement is encoded when all the proprioceptive information from all the Muscles involved in the actual movement is taken into account. During ankle movements imposed on human subjects, the activity of 30 Muscle Spindle afferents originating in the extensor digitorum longus, tibialis anterior, extensor hallucis longus and peroneus lateralis Muscles was recorded from the lateral peroneal nerve using the microneurographic technique. In the first part of the study, it was proposed to investigate whether Muscle Spindle afferents have a preferred direction, as previously found to occur in the case of cortical cells, and to analyze the neural coding of the movement trajectories using a "population vector model." This model is based on the idea that neuronal coding can be analyzed in terms of a series of vectors, each based on specific movement parameters. In the present case, each vector gives the mean contribution of a population of Muscle Spindle afferents within one directionally tuned Muscle. A given population vector points in the "preferred sensory direction" of the Muscle to which it corresponds, and its length is the mean frequency of all the afferents within that Muscle. Our working hypothesis was that the sum of these weighted vectors points in the same direction as the ongoing movement. The results show that each Muscle Spindle afferent, and likewise each Muscle, has a specific preferred sensory direction, as well as a preferred sensory sector within which it is capable of sending sensory information to the central nervous system. Interestingly, the results also demonstrate that the preferred directions are the same as the directions of vibration-induced illusions. In addition, the results show that the neuronal population vector model describes the multipopulation proprioceptive coding of spatially oriented 2D limb movements, even at the peripheral sensory level, based on the sum vectors calculated from all the Muscles involved in the movement. In an accompanying paper, the coding of more complex 2D movements such as those involved in drawing rectilinear and curvilinear geometrical shapes was investigated.
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increased Muscle Spindle sensitivity to movement during reinforcement manoeuvres in relaxed human subjects
The Journal of Physiology, 2000Co-Authors: Edith Ribotciscar, Christiane Rossidurand, Jeanpierre RollAbstract:The effects of reinforcement manoeuvres, such as mental computation and the Jendrassik manoeuvre, on Muscle Spindle sensitivity to passively imposed sinusoidal stretching (1.5 deg, 2 Hz) in relaxed subjects were analysed. The unitary activity of 26 Muscle Spindle afferents (23 Ia, 3 II) originating from ankle Muscles was recorded using the microneurographic method. Particular care was paid to the subjects' state of physical and mental relaxation. The results showed that the activity of 54 % of the Ia afferents was modified during mental computation. The modifications took the form of either an increase in the number of spikes (mean, 26 % among 11 Ia fibres) or a shortening in the latency of the response to sinusoidal stretching (mean, 13 ms among 3 Ia fibres), or both. They were sometimes accompanied by an enhanced variability in the instantaneous discharge frequency. The three secondary endings tested exhibited no change in their sensitivity to stretch during mental computation. The increased sensitivity to passive movements sometimes began as soon as the instructions were given to the subjects and sometimes increased during mental computation. In addition, the increased sensitivity either stopped after the subjects gave the right answer or continued for several minutes. During the performance of a Jendrassik manoeuvre, the Ia units underwent changes similar to those described above for mental computation. It was concluded that Muscle Spindle sensitivity to movement can be modified in relaxed human subjects. The results reinforce the idea that the fusimotor system plays a role in arousal and expectancy, and contribute to narrowing the gap between human and behaving animal data. Whereas in amphibia, terminal branches of α-motoneurones provide motor innervation to Muscle Spindles, in mammals, a separate fusimotor supply has evolved, namely γ-motoneurones. These are morphologically different from α-motoneurones, they receive different reflex connections, and they innervate Muscle Spindles separately and more extensively. Together this suggests that the fusimotor system might, to some extent, act independently of the skeletomotor system and could modify Muscle Spindle sensitivity selectively in order to make the receptors extract more accurate information about movement. The fusimotor system is indeed better thought of as allowing state-dependent parametric adjustment of length and velocity feedback rather than as simply compensating automatically for Muscle shortening, a role devoted to the pre-existing skeleto-fusimotor system (see Prochazka, 1989). Muscle Spindle afferent recordings from behaving animals support this notion of adjustment. Indeed, it has been reported that demanding motor tasks are associated with higher levels of γ-drive than are routine movements, without concomitant changes in skeletomotor activity (Prochazka et al. 1985, 1988; Hulliger et al. 1989; Prochazka, 1989; Gorassini et al. 1993). Some microneurographic studies on Muscle afferents have reported that independent control of fusimotor activity may also occur in humans (Burg et al. 1973, 1974, 1975, 1976; Hagbarth et al. 1975; Burke et al. 1980a, b; Vallbo & Hulliger, 1981; Gandevia & Burke, 1985; Aniss et al. 1990; Gandevia et al. 1994), although this is controversial (see reviews by Vallbo et al. 1979; Prochazka, 1996). We previously revealed a fusimotor drive in human relaxed Muscles more directly by recording γ-efferents that exhibited substantial changes in activity during various reinforcement manoeuvres (Ribot et al. 1986). An increase in the fusimotor activity was induced (1) by cognitive factors, such as listening to instructions about mental computation tasks, performing computations, or focusing attention on the experimental situation; (2) by behavioural factors, such as laughing or talking; (3) by environmental factors, such as hearing or seeing somebody enter the room in which the experiment was taking place or hearing a short auditory stimulus; and (4) by clinical neurophysiological manoeuvres, such as clenching both fists (the Jendrassik manoeuvre). However, these four types of manoeuvre failed to change the Muscle Spindle response to Muscle stretching. Indeed, the Muscle Spindle responses to ramp and hold stretches recorded with (‘test response’) and without (‘control response’) concomitant manoeuvres did not differ (Ribot et al. 1986). This lack of change in the Muscle Spindles' stretch sensitivity may be due to at least two factors. First, any fusimotor discharge, whether spontaneous or induced, was found to be difficult to suppress: only some subjects succeeded in entering a state of deep mental and somatic relaxation that is apparently required to minimise fusimotor activity. Second, the firing rate of the fusimotor neurones that was induced by each of the reinforcement manoeuvres was never greater than the firing rate of their spontaneous discharges. These points suggest that what we had been calling the ‘control response’, when analysing Muscle Spindle sensitivity to stretch (Ribot et al. 1986), may have been obtained while the γ-system was already discharging and that the performance of any additional manoeuvre may not in fact have increased the fusimotor drive relative to the control situation. In the present study, we reinvestigated this issue by taking particular care to ensure that the subject was always as physically and mentally relaxed as possible in the control situation. These conditions were fulfilled by using only subjects accustomed to participating in microneurographic experiments. They were helped to relax by listening to a relaxation audiotape, and their level of arousal was monitored throughout the experiments by recording electrodermal activities (Ohman et al. 1993). Furthermore, since the fusimotor tone might be of the dynamic type (Burg et al. 1976; Ribot et al. 1986; Gandevia et al. 1994), ramp and hold stretches may not be the most appropriate stimulus for investigating whether any corresponding changes occur in the Muscle Spindle response. We therefore used continuously repeated sinusoidal movements to show up any intermittent or delayed effects. The results show that reinforcement manoeuvres, such as mental computation and fist clenching, can increase the primary Muscle Spindle sensitivity to passive movements. This increase indicates that a fusimotor outflow operates on the Muscle Spindle endings in non-contracting Muscles in awake subjects and plays a role in arousal and expectancy, as for behaving animals (see review by Prochazka, 1989).
Edith Ribotciscar - One of the best experts on this subject based on the ideXlab platform.
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fusimotor drive may adjust Muscle Spindle feedback to task requirements in humans
Journal of Neurophysiology, 2009Co-Authors: Edith Ribotciscar, Valerie Hospod, Jeanpierre Roll, Jeanmarc AimonettiAbstract:The aim of the present study was to investigate whether the fusimotor control of Muscle Spindle sensitivity may depend on the movement parameter the task is focused on, either the velocity or the final position reached. The unitary activities of 18 Muscle Spindle afferents were recorded by microneurography at the common peroneal nerve. We compared in two situations the responses of Muscle Spindle afferents to ankle movements imposed while the subject was instructed not to pay attention to or to pay attention to the movement, both in the absence of visual cues. In the two situations, three ramp-and-hold movements were imposed in random order. In one situation, the three movements differed by their velocity and in the other by the final position reached. The task consisted in ranking the three movements according to the parameter under consideration (for example, slow, fast, and medium). The results showed that paying attention to movement velocity gave rise to a significant increase in the dynamic and static responses of Muscle afferents. In contrast, focusing attention on the final position reached made the Muscle Spindle feedback better discriminate the different positions and depressed its capacity to discriminate movement velocities. Changes are interpreted as reflecting dynamic and static gamma activation, respectively. The present results support the view that the fusimotor drive depends on the parameter the task is focused on, so that the Muscle afferent feedback is adjusted to the task requirements.
-
changes in human Muscle Spindle sensitivity during a proprioceptive attention task
The Journal of Neuroscience, 2007Co-Authors: Valerie Hospod, Jeanpierre Roll, Jeanmarc Aimonetti, Edith RibotciscarAbstract:The aim of the present study was to test whether fusimotor control of human Muscle Spindle sensitivity changed when attention was selectively directed to the recognition of an imposed two-dimensional movement in the form of a written symbol. The unitary activities of 32 Muscle Spindle afferents (26 Ia, 6 II) were recorded by microneurography at the level of the common peroneal nerve. The patterns of firing rate in response to passive movements of the ankle, forming different letters or numbers, were compared in two conditions: control and recognition. No visual cues were given in either condition, but subjects had to recognize and name the character in one condition compared with not paying attention in the control condition. The results showed that 58% of the tested Ia afferents presented modified responses to movements when these had to be recognized. Changes in Ia afferent responses included decreased depth of modulation, increased variability of discharge, and changes in spontaneous activity. Not all changes were evident in the same afferent. Furthermore, the percentage of correctly recognized movements amounted to 63% when changes were observed, but it was only 48% when the primary ending sensitivity was unaltered. The responses of group II afferents were only weakly changed or unchanged. It is suggested that the altered Muscle Spindle sensitivity is because of selective changes in fusimotor control, the consequence of which might be to feed the brain movement trajectory information that is more accurate.
-
the preferred sensory direction of Muscle Spindle primary endings influences the velocity coding of two dimensional limb movements in humans
Experimental Brain Research, 2002Co-Authors: Edith Ribotciscar, Mikael Bergenheim, Jeanpierre RollAbstract:The present study compares how accurately two different but close velocities of movement are discriminated by populations of Muscle Spindle primary afferents whether or not one takes into account the direction of the movement and the preferred sensory directions of the units (i.e., the direction of movement to which the afferents are the most sensitive). The activities of 26 Muscle Spindle primary endings originating from the tibialis anterior, the extensor digitorum longus, the extensor hallucis longus, and the peroneus lateralis Muscles were recorded in the lateral peroneal nerve. Their responses to movements imposed at two velocities (12.5 and 18 mm/s) were analyzed. These movements were straight-line movements imposed in eight directions and circular movements in both clockwise and anticlockwise directions. The encoding of the movement velocity was analyzed in two ways. First, the mean frequencies of discharge of the Muscle Spindle afferents were compared for the two velocities. Second, the data were analyzed using a “neuronal population vector model.” This model is based on the idea that such neuronal coding can be analyzed in terms of a series of population vectors (i.e., mean contribution of all the Muscle Spindle afferents within one directionally tuned Muscle) and by finally calculating a sum vector. The results showed no clear and consistent difference in the response frequency of the Muscle Spindle afferents for the two velocities of movement compared. Rather, the most consistently significant differences between the two velocities were in the lengths of the sum vectors. It is concluded that the encoding of two-dimensional movement velocity relies on populations of Muscle Spindle afferents coming from the whole set of Muscles surrounding a particular joint, each Muscle making an instantaneous, oriented, and weighted contribution to the sensory coding of the kinematics parameters.
-
proprioceptive population coding of two dimensional limb movements in humans i Muscle Spindle feedback during spatially oriented movements
Experimental Brain Research, 2000Co-Authors: Mikael Bergenheim, Edith Ribotciscar, Jeanpierre RollAbstract:The proprioceptive coding of multidirectional ankle joint movements was investigated, focusing in particular on the question as to how accurately the direction of a movement is encoded when all the proprioceptive information from all the Muscles involved in the actual movement is taken into account. During ankle movements imposed on human subjects, the activity of 30 Muscle Spindle afferents originating in the extensor digitorum longus, tibialis anterior, extensor hallucis longus and peroneus lateralis Muscles was recorded from the lateral peroneal nerve using the microneurographic technique. In the first part of the study, it was proposed to investigate whether Muscle Spindle afferents have a preferred direction, as previously found to occur in the case of cortical cells, and to analyze the neural coding of the movement trajectories using a "population vector model." This model is based on the idea that neuronal coding can be analyzed in terms of a series of vectors, each based on specific movement parameters. In the present case, each vector gives the mean contribution of a population of Muscle Spindle afferents within one directionally tuned Muscle. A given population vector points in the "preferred sensory direction" of the Muscle to which it corresponds, and its length is the mean frequency of all the afferents within that Muscle. Our working hypothesis was that the sum of these weighted vectors points in the same direction as the ongoing movement. The results show that each Muscle Spindle afferent, and likewise each Muscle, has a specific preferred sensory direction, as well as a preferred sensory sector within which it is capable of sending sensory information to the central nervous system. Interestingly, the results also demonstrate that the preferred directions are the same as the directions of vibration-induced illusions. In addition, the results show that the neuronal population vector model describes the multipopulation proprioceptive coding of spatially oriented 2D limb movements, even at the peripheral sensory level, based on the sum vectors calculated from all the Muscles involved in the movement. In an accompanying paper, the coding of more complex 2D movements such as those involved in drawing rectilinear and curvilinear geometrical shapes was investigated.
-
increased Muscle Spindle sensitivity to movement during reinforcement manoeuvres in relaxed human subjects
The Journal of Physiology, 2000Co-Authors: Edith Ribotciscar, Christiane Rossidurand, Jeanpierre RollAbstract:The effects of reinforcement manoeuvres, such as mental computation and the Jendrassik manoeuvre, on Muscle Spindle sensitivity to passively imposed sinusoidal stretching (1.5 deg, 2 Hz) in relaxed subjects were analysed. The unitary activity of 26 Muscle Spindle afferents (23 Ia, 3 II) originating from ankle Muscles was recorded using the microneurographic method. Particular care was paid to the subjects' state of physical and mental relaxation. The results showed that the activity of 54 % of the Ia afferents was modified during mental computation. The modifications took the form of either an increase in the number of spikes (mean, 26 % among 11 Ia fibres) or a shortening in the latency of the response to sinusoidal stretching (mean, 13 ms among 3 Ia fibres), or both. They were sometimes accompanied by an enhanced variability in the instantaneous discharge frequency. The three secondary endings tested exhibited no change in their sensitivity to stretch during mental computation. The increased sensitivity to passive movements sometimes began as soon as the instructions were given to the subjects and sometimes increased during mental computation. In addition, the increased sensitivity either stopped after the subjects gave the right answer or continued for several minutes. During the performance of a Jendrassik manoeuvre, the Ia units underwent changes similar to those described above for mental computation. It was concluded that Muscle Spindle sensitivity to movement can be modified in relaxed human subjects. The results reinforce the idea that the fusimotor system plays a role in arousal and expectancy, and contribute to narrowing the gap between human and behaving animal data. Whereas in amphibia, terminal branches of α-motoneurones provide motor innervation to Muscle Spindles, in mammals, a separate fusimotor supply has evolved, namely γ-motoneurones. These are morphologically different from α-motoneurones, they receive different reflex connections, and they innervate Muscle Spindles separately and more extensively. Together this suggests that the fusimotor system might, to some extent, act independently of the skeletomotor system and could modify Muscle Spindle sensitivity selectively in order to make the receptors extract more accurate information about movement. The fusimotor system is indeed better thought of as allowing state-dependent parametric adjustment of length and velocity feedback rather than as simply compensating automatically for Muscle shortening, a role devoted to the pre-existing skeleto-fusimotor system (see Prochazka, 1989). Muscle Spindle afferent recordings from behaving animals support this notion of adjustment. Indeed, it has been reported that demanding motor tasks are associated with higher levels of γ-drive than are routine movements, without concomitant changes in skeletomotor activity (Prochazka et al. 1985, 1988; Hulliger et al. 1989; Prochazka, 1989; Gorassini et al. 1993). Some microneurographic studies on Muscle afferents have reported that independent control of fusimotor activity may also occur in humans (Burg et al. 1973, 1974, 1975, 1976; Hagbarth et al. 1975; Burke et al. 1980a, b; Vallbo & Hulliger, 1981; Gandevia & Burke, 1985; Aniss et al. 1990; Gandevia et al. 1994), although this is controversial (see reviews by Vallbo et al. 1979; Prochazka, 1996). We previously revealed a fusimotor drive in human relaxed Muscles more directly by recording γ-efferents that exhibited substantial changes in activity during various reinforcement manoeuvres (Ribot et al. 1986). An increase in the fusimotor activity was induced (1) by cognitive factors, such as listening to instructions about mental computation tasks, performing computations, or focusing attention on the experimental situation; (2) by behavioural factors, such as laughing or talking; (3) by environmental factors, such as hearing or seeing somebody enter the room in which the experiment was taking place or hearing a short auditory stimulus; and (4) by clinical neurophysiological manoeuvres, such as clenching both fists (the Jendrassik manoeuvre). However, these four types of manoeuvre failed to change the Muscle Spindle response to Muscle stretching. Indeed, the Muscle Spindle responses to ramp and hold stretches recorded with (‘test response’) and without (‘control response’) concomitant manoeuvres did not differ (Ribot et al. 1986). This lack of change in the Muscle Spindles' stretch sensitivity may be due to at least two factors. First, any fusimotor discharge, whether spontaneous or induced, was found to be difficult to suppress: only some subjects succeeded in entering a state of deep mental and somatic relaxation that is apparently required to minimise fusimotor activity. Second, the firing rate of the fusimotor neurones that was induced by each of the reinforcement manoeuvres was never greater than the firing rate of their spontaneous discharges. These points suggest that what we had been calling the ‘control response’, when analysing Muscle Spindle sensitivity to stretch (Ribot et al. 1986), may have been obtained while the γ-system was already discharging and that the performance of any additional manoeuvre may not in fact have increased the fusimotor drive relative to the control situation. In the present study, we reinvestigated this issue by taking particular care to ensure that the subject was always as physically and mentally relaxed as possible in the control situation. These conditions were fulfilled by using only subjects accustomed to participating in microneurographic experiments. They were helped to relax by listening to a relaxation audiotape, and their level of arousal was monitored throughout the experiments by recording electrodermal activities (Ohman et al. 1993). Furthermore, since the fusimotor tone might be of the dynamic type (Burg et al. 1976; Ribot et al. 1986; Gandevia et al. 1994), ramp and hold stretches may not be the most appropriate stimulus for investigating whether any corresponding changes occur in the Muscle Spindle response. We therefore used continuously repeated sinusoidal movements to show up any intermittent or delayed effects. The results show that reinforcement manoeuvres, such as mental computation and fist clenching, can increase the primary Muscle Spindle sensitivity to passive movements. This increase indicates that a fusimotor outflow operates on the Muscle Spindle endings in non-contracting Muscles in awake subjects and plays a role in arousal and expectancy, as for behaving animals (see review by Prochazka, 1989).
Lena H Ting - One of the best experts on this subject based on the ideXlab platform.
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diverse Muscle Spindle firing properties emerge from multiscale Muscle mechanics
bioRxiv, 2019Co-Authors: Kyle P Blum, Kenneth S Campbell, Brian C Horslen, Paul Nardelli, Stephen N Housley, Timothy C Cope, Lena H TingAbstract:Sensory information about the body and its mechanical interactions with the environment are critical for neural control of movement. Muscle Spindle sensory neurons richly innervate Muscles in vertebrates; their firing patterns as Muscles stretch have been well characterized experimentally, but have not been fully explained mechanistically. Here, we show that a diverse range of Muscle Spindle firing characteristics are emergent from first principles of Muscle contractile mechanics. We develop a mechanistic Muscle Spindle model that predicts well-known phenomena such as variations in Muscle Spindle sensitivity due to prior movement history and nonlinear scaling with Muscle stretch velocity. The model further predicts how central commands to Muscle Spindles, fusimotor drive, alters their firing responses, and shows how seemingly paradoxical Muscle Spindle firing during voluntary force production in humans can arise. Our multiscale Muscle Spindle model provides a unifying biophysical framework that may broadly explain and predict movement-related sensory signals in health and disease.
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elastic tissue forces mask Muscle fiber forces underlying Muscle Spindle ia afferent firing rates in stretch of relaxed rat Muscle
The Journal of Experimental Biology, 2019Co-Authors: Kyle P Blum, Paul Nardelli, Timothy C Cope, Lena H TingAbstract:ABSTRACT Stretches of relaxed cat and rat Muscle elicit similar history-dependent Muscle Spindle Ia firing rates that resemble history-dependent forces seen in single activated Muscle fibers ( Nichols and Cope, 2004). Owing to thixotropy, whole musculotendon forces and Muscle Spindle firing rates are history dependent during stretch of relaxed cat Muscle, where both Muscle force and Muscle Spindle firing rates are elevated in the first stretch in a series of stretch–shorten cycles ( Blum et al., 2017). By contrast, rat musculotendon exhibits only mild thixotropy, such that the measured forces when stretched cannot explain history-dependent Muscle Spindle firing rates in the same way ( Haftel et al., 2004). We hypothesized that history-dependent Muscle Spindle firing rates elicited in stretch of relaxed rat Muscle mirror history-dependent Muscle fiber forces, which are masked at the level of whole musculotendon force by extracellular tissue force. We removed estimated extracellular tissue force contributions from recorded musculotendon force using an exponentially elastic tissue model. We then showed that the remaining estimated Muscle fiber force resembles history-dependent Muscle Spindle firing rates recorded simultaneously. These forces also resemble history-dependent forces recorded in stretch of single activated fibers that are attributed to Muscle cross-bridge mechanisms ( Campbell and Moss, 2000). Our results suggest that history-dependent Muscle Spindle firing in both rats and cats arise from history-dependent forces owing to thixotropy in Muscle fibers.
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noncontractile tissue forces mask Muscle fiber forces underlying Muscle Spindle ia afferent firing rates in stretch of relaxed rat Muscle
bioRxiv, 2018Co-Authors: Kyle P Blum, Paul Nardelli, Timothy C Cope, Lena H TingAbstract:Stretches of relaxed cat and rat Muscle elicit similar history-dependent Muscle Spindle Ia firing rates that resemble history-dependent forces seen in single activated Muscle fibers (Nichols and Cope, 2004). During stretch of relaxed cat Muscle, whole musculotendon forces exhibit history-dependence that mirror history-dependent Muscle Spindle firing rates, where both Muscle force and Muscle Spindle firing rates are elevated in the first stretch in a series of stretch-shorten cycles (Blum et al 2017). By contrast, rat musculotendon are only mildly history-dependent and do not mirror history-dependent Muscle Spindle firing rates in the same way (Haftel et al., 2004). We hypothesized that history-dependent Muscle Spindle firing rates elicited in stretch of relaxed rat Muscle would mirror history-dependent Muscle fiber forces, which are masked by noncontractile tissue at the level of whole musculotendon force. We removed noncontractile tissue force contributions from the recorded musculotendon force using an exponentially-elastic tissue model. We then show that the remaining estimated Muscle fiber force resembles history-dependent Muscle Spindle firing rates recorded simultaneously. These forces also resemble history-dependent forces recorded in stretch of single activated fibers and attributed to Muscle cross-bridge mechanisms (Campbell and Moss 2000). Our results suggest that history-dependent Muscle Spindle firing in both rats and cats arise from stretch of cross-bridges in Muscle fibers.
Timothy C Cope - One of the best experts on this subject based on the ideXlab platform.
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diverse Muscle Spindle firing properties emerge from multiscale Muscle mechanics
bioRxiv, 2019Co-Authors: Kyle P Blum, Kenneth S Campbell, Brian C Horslen, Paul Nardelli, Stephen N Housley, Timothy C Cope, Lena H TingAbstract:Sensory information about the body and its mechanical interactions with the environment are critical for neural control of movement. Muscle Spindle sensory neurons richly innervate Muscles in vertebrates; their firing patterns as Muscles stretch have been well characterized experimentally, but have not been fully explained mechanistically. Here, we show that a diverse range of Muscle Spindle firing characteristics are emergent from first principles of Muscle contractile mechanics. We develop a mechanistic Muscle Spindle model that predicts well-known phenomena such as variations in Muscle Spindle sensitivity due to prior movement history and nonlinear scaling with Muscle stretch velocity. The model further predicts how central commands to Muscle Spindles, fusimotor drive, alters their firing responses, and shows how seemingly paradoxical Muscle Spindle firing during voluntary force production in humans can arise. Our multiscale Muscle Spindle model provides a unifying biophysical framework that may broadly explain and predict movement-related sensory signals in health and disease.
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elastic tissue forces mask Muscle fiber forces underlying Muscle Spindle ia afferent firing rates in stretch of relaxed rat Muscle
The Journal of Experimental Biology, 2019Co-Authors: Kyle P Blum, Paul Nardelli, Timothy C Cope, Lena H TingAbstract:ABSTRACT Stretches of relaxed cat and rat Muscle elicit similar history-dependent Muscle Spindle Ia firing rates that resemble history-dependent forces seen in single activated Muscle fibers ( Nichols and Cope, 2004). Owing to thixotropy, whole musculotendon forces and Muscle Spindle firing rates are history dependent during stretch of relaxed cat Muscle, where both Muscle force and Muscle Spindle firing rates are elevated in the first stretch in a series of stretch–shorten cycles ( Blum et al., 2017). By contrast, rat musculotendon exhibits only mild thixotropy, such that the measured forces when stretched cannot explain history-dependent Muscle Spindle firing rates in the same way ( Haftel et al., 2004). We hypothesized that history-dependent Muscle Spindle firing rates elicited in stretch of relaxed rat Muscle mirror history-dependent Muscle fiber forces, which are masked at the level of whole musculotendon force by extracellular tissue force. We removed estimated extracellular tissue force contributions from recorded musculotendon force using an exponentially elastic tissue model. We then showed that the remaining estimated Muscle fiber force resembles history-dependent Muscle Spindle firing rates recorded simultaneously. These forces also resemble history-dependent forces recorded in stretch of single activated fibers that are attributed to Muscle cross-bridge mechanisms ( Campbell and Moss, 2000). Our results suggest that history-dependent Muscle Spindle firing in both rats and cats arise from history-dependent forces owing to thixotropy in Muscle fibers.
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noncontractile tissue forces mask Muscle fiber forces underlying Muscle Spindle ia afferent firing rates in stretch of relaxed rat Muscle
bioRxiv, 2018Co-Authors: Kyle P Blum, Paul Nardelli, Timothy C Cope, Lena H TingAbstract:Stretches of relaxed cat and rat Muscle elicit similar history-dependent Muscle Spindle Ia firing rates that resemble history-dependent forces seen in single activated Muscle fibers (Nichols and Cope, 2004). During stretch of relaxed cat Muscle, whole musculotendon forces exhibit history-dependence that mirror history-dependent Muscle Spindle firing rates, where both Muscle force and Muscle Spindle firing rates are elevated in the first stretch in a series of stretch-shorten cycles (Blum et al 2017). By contrast, rat musculotendon are only mildly history-dependent and do not mirror history-dependent Muscle Spindle firing rates in the same way (Haftel et al., 2004). We hypothesized that history-dependent Muscle Spindle firing rates elicited in stretch of relaxed rat Muscle would mirror history-dependent Muscle fiber forces, which are masked by noncontractile tissue at the level of whole musculotendon force. We removed noncontractile tissue force contributions from the recorded musculotendon force using an exponentially-elastic tissue model. We then show that the remaining estimated Muscle fiber force resembles history-dependent Muscle Spindle firing rates recorded simultaneously. These forces also resemble history-dependent forces recorded in stretch of single activated fibers and attributed to Muscle cross-bridge mechanisms (Campbell and Moss 2000). Our results suggest that history-dependent Muscle Spindle firing in both rats and cats arise from stretch of cross-bridges in Muscle fibers.
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Muscle Spindle responses to horizontal support surface perturbation in the anesthetized cat insights into the role of autogenic feedback in whole body postural control
Journal of Neurophysiology, 2012Co-Authors: Claire F Honeycutt, Paul Nardelli, Timothy C Cope, Richard T NicholsAbstract:Intact cats and humans respond to support surface perturbations with broadly tuned, directionally sensitive Muscle activation. These Muscle responses are further sensitive to initial stance widths (distance between feet) and perturbation velocity. The sensory origins driving these responses are not known, and conflicting hypotheses are prevalent in the literature. We hypothesize that the direction-, stance-width-, and velocity-sensitive Muscle response during support surface perturbations is driven largely by rapid autogenic proprioceptive pathways. The primary objective of this study was to obtain direct evidence for our hypothesis by establishing that Muscle Spindle receptors in the intact limb can provide appropriate information to drive the Muscle response to whole body postural perturbations. Our second objective was to determine if Spindle recordings from the intact limb generate the heightened sensitivity to small perturbations that has been reported in isolated Muscle experiments. Maintenance of this heightened sensitivity would indicate that Muscle Spindles are highly proficient at detecting even small disturbances, suggesting they can provide efficient feedback about changing postural conditions. We performed intraaxonal recordings from Muscle Spindles in anesthetized cats during horizontal, hindlimb perturbations. We indeed found that Muscle Spindle afferents in the intact limb generate broadly tuned but directionally sensitive activation patterns. These afferents were also sensitive to initial stance widths and perturbation velocities. Finally, we found that afferents in the intact limb have heightened sensitivity to small perturbations. We conclude that Muscle Spindle afferents provide an array of important information about biomechanics and perturbation characteristics highlighting their potential importance in generating appropriate muscular response during a postural disturbance.
Masayuki Moritani - One of the best experts on this subject based on the ideXlab platform.
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jaw Muscle Spindle afferent pathways to the trigeminal motor nucleus in the rat
The Journal of Comparative Neurology, 2001Co-Authors: Masayuki Moritani, Dean DessemAbstract:Neural pathways conveying proprioceptive feedback from the jaw Muscles were studied in rats by combining retrograde and intracellular neuronal labeling. Initially, horseradish peroxidase was iontophoresed unilaterally into the trigeminal motor nucleus (Vmo). Two days later, 1–5 jaw-Muscle Spindle afferent axons located in the mesencephalic trigeminal nucleus were physiologically identified and intracellularly stained with biotinamide. Stained mesencephalic trigeminal jaw-Muscle Spindle afferent axon collaterals and boutons were predominantly distributed in the supratrigeminal region (Vsup), Vmo, dorsomedial trigeminal principal sensory nucleus (Vpdm), parvicellular reticular formation (PCRt), alpha division of the parvicellular reticular formation (PCRtA), and dorsomedial portions of the spinal trigeminal subnuclei oralis (Vodm), and interpolaris (Vidm). Numerous neurons retrogradely labeled with horseradish peroxidase from the trigeminal motor nucleus were found bilaterally in the PCRt, PCRtA, Vodm, and Vidm. Retrogradely labeled neurons were also present contralaterally in the Vsup, Vpdm, Vmo, peritrigeminal zone, and bilaterally in the dorsal medullary reticular field. Putative contacts between intracellularly stained mesencephalic trigeminal jaw-Muscle Spindle afferent boutons and trigeminal premotor neurons retrogradely labeled with horseradish peroxidase were found in the ipsilateral Vodm, PCRtA, and PCRt, as well as the contralateral Vsup, Vmo, Vodm, PCRt, and PCRtA. Thus, multiple disynaptic jaw-Muscle Spindle afferent-motoneuron circuits exist. These pathways are likely to convey long-latency jaw-Muscle stretch reflexes and may contribute to stiffness regulation of the masticatory Muscles. J. Comp. Neurol. 435:341–353, 2001. © 2001 Wiley-Liss, Inc.
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central distribution of synaptic contacts of primary and secondary jaw Muscle Spindle afferents in the trigeminal motor nucleus of the cat
The Journal of Comparative Neurology, 1998Co-Authors: Hiroto Kishimoto, Masayuki Moritani, Atsushi Yoshida, Motohide Takemura, Shinji Nakagawa, Yoshitaka Nagase, Takeshi Wada, Barry J Sessle, Yoshio ShigenagaAbstract:Little is known about the differences of the terminations of group Ia and group II afferents within the brainstem or spinal cord. The present study was performed to classify cat jaw Muscle Spindle afferents by the use of succinylcholine (SCh) and to examine the morphological characteristics of the physiologically classified afferents at the light and electron microscopic levels through the use of the intra-axonal horseradish peroxidase (HRP) injection technique. The effects of SCh on stretch responses of 119 jaw Muscle Spindle afferents from the masseter were examined. The SCh converted the single skew distribution of the values for dynamic index (DI) into a bimodal one. Fifty-eight and 61 afferents were classified as group Ia and group II afferents, respectively. The central projections of 17 intra-axonally stained afferents (10 group Ia and 7 group II afferents) were examined. The Spindle afferents terminated mainly in the supratrigeminal nucleus (Vsup), region h, and the dorsolateral subdivision of trigeminal motor nucleus (Vmo.dl) but differed in the pattern of projections of group Ia and group II afferents. The proportion of group Ia afferent terminals was higher in Vmo.dl but lower in Vsup than that of group II afferents. In Vmo.dl, the proportion of group Ia afferent terminals was higher in the central region but lower in the more outer regions than that of group II afferents. The ultrastructure of serially sectioned afferent boutons (63 group Ia and 72 group II boutons) also was examined. The boutons from the two groups were distributed widely from the soma to small-diameter dendrites, but the frequency of synaptic contacts on proximal dendrites was higher in group Ia than group II afferents. The present study provides evidence that the two groups of jaw Muscle Spindle afferents differ in their central projection and the spatial distribution of their synaptic contacts on Vmo.dl neurons. J. Comp. Neurol. 391:50–63, 1998. © 1998 Wiley-Liss, Inc.
