Motor Control of Aimed Limb Movements in an Insect

2008 ◽  
Vol 99 (2) ◽  
pp. 484-499 ◽  
Author(s):  
Keri L. Page ◽  
Jure Zakotnik ◽  
Volker Dürr ◽  
Thomas Matheson

Limb movements that are aimed toward tactile stimuli of the body provide a powerful paradigm with which to study the transformation of motor activity into context-dependent action. We relate the activity of excitatory motor neurons of the locust femoro-tibial joint to the consequent kinematics of hind leg movements made during aimed scratching. There is posture-dependence of motor neuron activity, which is stronger in large amplitude (putative fast) than in small (putative slow and intermediate) motor neurons. We relate this posture dependency to biomechanical aspects of the musculo-skeletal system and explain the occurrence of passive tibial movements that occur in the absence of agonistic motor activity. There is little recorded co-activation of antagonistic tibial extensor and flexor motor neurons, and there is differential recruitment of proximal and distal flexor motor neurons. Large-amplitude motor neurons are often recruited soon after a switch in joint movement direction. Motor bursts containing large-amplitude spikes exhibit high spike rates of small-amplitude motor neurons. The fast extensor tibiae neuron, when recruited, exhibits a pattern of activity quite different to that seen during kicking, jumping, or righting: there is no co-activation of flexor motor neurons and no full tibial flexion. Changes in femoro-tibial joint angle and angular velocity are most strongly dependent on variations in the number of motor neuron spikes and the duration of motor bursts rather than on firing frequency. Our data demonstrate how aimed scratching movements result from interactions between biomechanical features of the musculo-skeletal system and patterns of motor neuron recruitment.

Cells ◽  
2021 ◽  
Vol 10 (6) ◽  
pp. 1449
Author(s):  
Cyril Quessada ◽  
Alexandra Bouscary ◽  
Frédérique René ◽  
Cristiana Valle ◽  
Alberto Ferri ◽  
...  

Amyotrophic lateral sclerosis (ALS) is a fatal neurodegenerative disease characterized by progressive and selective loss of motor neurons, amyotrophy and skeletal muscle paralysis usually leading to death due to respiratory failure. While generally considered an intrinsic motor neuron disease, data obtained in recent years, including our own, suggest that motor neuron protection is not sufficient to counter the disease. The dismantling of the neuromuscular junction is closely linked to chronic energy deficit found throughout the body. Metabolic (hypermetabolism and dyslipidemia) and mitochondrial alterations described in patients and murine models of ALS are associated with the development and progression of disease pathology and they appear long before motor neurons die. It is clear that these metabolic changes participate in the pathology of the disease. In this review, we summarize these changes seen throughout the course of the disease, and the subsequent impact of glucose–fatty acid oxidation imbalance on disease progression. We also highlight studies that show that correcting this loss of metabolic flexibility should now be considered a major goal for the treatment of ALS.


1985 ◽  
Vol 54 (4) ◽  
pp. 887-899 ◽  
Author(s):  
W. Graf ◽  
R. Baker

The flatfish species constitute a natural paradigm for investigating adaptive changes in the vertebrate central nervous system. During metamorphosis all species of flatfish experience a 90 degree change in orientation between their vestibular and extraocular coordinate axes. As a result, the optic axes of both eyes maintain their orientation with respect to earth horizontal, but the horizontal semicircular canals become oriented vertically. Since the flatfish propels its body with the same swimming movements when referenced to the body as a normal fish, the horizontal canals are exposed to identical accelerations, but in the flatfish these accelerations occur in a vertical plane. The appropriate compensatory eye movements are simultaneous rotations of both eyes forward or backward (i.e., parallel), in contrast to the symmetric eye movements in upright fish (i.e., one eye moves forward, the other backward). Therefore, changes in the extraocular muscle arrangement and/or the neuronal connectivity are required. This study describes the peripheral and central oculomotor organization in the adult winter flounder, Pseudopleuronectes americanus. At the level of the peripheral oculomotor apparatus, the sizes of the horizontal extraocular muscles (lateral and medial rectus) were considerably smaller than those of the vertical eye muscles, as quantified by fiber counts and area measurements of cross sections of individual muscles. However, the spatial orientations and the kinematic characteristics of all six extraocular muscles were not different from those described in comparable lateral-eyed animals. There were no detectable asymmetries between the left and the right eye. Central oculomotor organization was investigated by extracellular horseradish peroxidase injections into individual eye muscles. Commonly described distributions of extraocular motor neurons in the oculomotor, trochlear, and abducens nuclei were found. These motor neuron pools consisted of two contralateral (superior rectus and superior oblique) and four ipsilateral populations (inferior oblique, inferior rectus, medial rectus, and lateral rectus). The labeled cells formed distinct motor neuron populations, which overlapped little. As expected, the numbers of labeled motoneurons differed in horizontal and vertical eye movers. The numerical difference was especially prominent in comparing the abducens nucleus with one of the vertical recti subdivisions. Nevertheless, there was bilateral symmetry between the motoneurons projecting to the left and right eyes.(ABSTRACT TRUNCATED AT 400 WORDS)


1985 ◽  
Vol 53 (6) ◽  
pp. 1517-1534 ◽  
Author(s):  
G. A. Robertson ◽  
L. I. Mortin ◽  
J. Keifer ◽  
P. S. Stein

A turtle with a complete transection of the spinal cord, termed a spinal turtle, exhibits three types or “forms” of the scratch reflex: the rostral scratch, pocket scratch, and caudal scratch (21). Each scratch form is elicited by tactile stimulation of a site on the body surface innervated by afferents entering the spinal cord caudal to the transection. We recorded electromyographic (EMG) potentials from the hindlimb during each of the three forms of the scratch in the spinal turtle (see Fig. 1). Common to all scratch forms is the rhythmic alternation of the activity of the hip protractor muscle (VP-HP) and hip retractor muscle (HR-KF). Each form of the scratch displays a characteristic timing of the activity of the knee extensor muscle (FT-KE) with respect to the cycle of activity of the hip muscles VP-HP and HR-KF. In a rostral scratch, activation of FT-KE occurs during the latter portion of VP-HP activation. In a pocket scratch, activation of FT-KE occurs during HR-KF activation. In a caudal scratch, activation of FT-KE occurs after the cessation of HR-KF activation. The timing characteristics of these muscle activity patterns correspond to the timing characteristics of changes in the angles of the knee joint and the hip joint obtained with movement analyses (21). We recorded electroneurographic (ENG) potentials from peripheral nerves of the hindlimb during each of the three forms of the “fictive” scratch in the spinal turtle immobilized with neuromuscular blockade (see Fig. 4). Common to all forms of the fictive scratch is the rhythmic alternation of the activity of hip protractor motor neurons (VP-HP) and hip retractor motor neurons (HR-KF). Each form displays a characteristic timing of the activity of knee extensor motor neurons (FT-KE) with respect to the cycle of VP-HP and HR-KF motor neuron activity. The timing characteristics of these motor neuron activity patterns are similar to the timing characteristics of the muscle activity patterns obtained in the preparation with movement (cf. Figs. 1 and 4). The motor pattern for each scratch form is generated centrally within the spinal cord. In the spinal immobilized preparation, neuromuscular blockade prevents both limb movement and phasic sensory input, and complete spinal transection isolates the cord from supraspinal input.(ABSTRACT TRUNCATED AT 400 WORDS)


Author(s):  
Jacob A. Blum ◽  
Sandy Klemm ◽  
Lisa Nakayama ◽  
Arwa Kathiria ◽  
Kevin A. Guttenplan ◽  
...  

AbstractThe spinal cord is a fascinating structure responsible for coordinating all movement in vertebrates. Spinal motor neurons control the activity of virtually every organ and muscle throughout the body by transmitting signals that originate in the spinal cord. These neurons are remarkably heterogeneous in their activity and innervation targets. However, because motor neurons represent only a small fraction of cells within the spinal cord and are difficult to isolate, the full complement of motor neuron subtypes remains unknown. Here we comprehensively describe the molecular heterogeneity of motor neurons within the adult spinal cord. We profiled 43,890 single-nucleus transcriptomes using fluorescence-activated nuclei sorting to enrich for spinal motor neuron nuclei. These data reveal a transcriptional map of the adult mammalian spinal cord and the first unbiased characterization of all transcriptionally distinct autonomic and somatic spinal motor neuron subpopulations. We identify 16 sympathetic motor neuron subtypes that segregate spatially along the spinal cord. Many of these subtypes selectively express specific hormones and receptors, suggesting neuromodulatory signaling within the autonomic nervous system. We describe skeletal motor neuron heterogeneity in the adult spinal cord, revealing numerous novel markers that distinguish alpha and gamma motor neurons—cell populations that are specifically affected in neurodegenerative disease. We also provide evidence for a novel transcriptional subpopulation of skeletal motor neurons. Collectively, these data provide a single-cell transcriptional atlas for investigating motor neuron diversity as well as the cellular and molecular basis of motor neuron function in health and disease.


2017 ◽  
Author(s):  
Tianqi Xu ◽  
Jing Huo ◽  
Shuai Shao ◽  
Michelle Po ◽  
Taizo Kawano ◽  
...  

Descending signals from the brain play critical roles in controlling and modulating locomotion kinematics. In the Caenorhabditis elegans nervous system, descending AVB premotor interneurons exclusively form gap junctions with B-type motor neurons that drive forward locomotion. We combined genetic analysis, optogenetic manipulation, and computational modeling to elucidate the function of AVB-B gap junctions during forward locomotion. First, we found that some B-type motor neurons generated intrinsic rhythmic activity, constituting distributed central pattern generators. Second, AVB premotor interneurons drove bifurcation of B-type motor neuron dynamics, triggering their transition from stationary to oscillatory activity. Third, proprioceptive couplings between neighboring B-type motor neurons entrained the frequency of body oscillators, forcing coherent propagation of bending waves. Despite substantial anatomical differences between the worm motor circuit and those in higher model organisms, we uncovered converging principles that govern coordinated locomotion.Significance StatementA deep understanding of the neural basis of motor behavior must integrate neuromuscular dynamics, mechanosensory feedback, as well as global command signals, to predict behavioral dynamics. Here, we report on an integrative approach to defining the circuit logic underlying coordinated locomotion in C. elegans. Our combined experimental and computational analysis revealed that (1) motor neurons in C. elegans could function as intrinsic oscillators; (2) Descending inputs and proprioceptive couplings work synergistically to facilitate the sequential activation of motor neuron activities, allowing bending waves to propagate efficiently along the body. Our work thus represents a key step towards an integrative view of animal locomotion.


2001 ◽  
Vol 204 (7) ◽  
pp. 1307-1317 ◽  
Author(s):  
D.L. McLean ◽  
J.R. McDearmid ◽  
K.T. Sillar

Nitric oxide (NO) is a ubiquitous neuromodulator with a diverse array of functions in a variety of brain regions, but a role for NO in the generation of locomotor activity has yet to be demonstrated. The possibility that NO is involved in the generation of motor activity in embryos of the frog Rana temporaria was investigated using the NO donors S-nitroso-n-acetylpenicillamine (SNAP; 100--500 micromol l(−1)) and diethylamine nitric oxide complex sodium (DEANO; 25--100 micromol l(−1)). Immobilised Rana temporaria embryos generate a non-rhythmic ‘lashing’ motor pattern either spontaneously or in response to dimming of the experimental bath illumination. Bath-applied NO donors triggered a qualitatively similar motor pattern in which non-rhythmic motor bursts were generated contra- and ipsilaterally down the length of the body. The inactive precursor of SNAP, n-acetyl-penicillamine (NAP), at equivalent concentrations did not trigger motor activity. NO donors failed to initiate swimming and had no measurable effects on the parameters of swimming induced by electrical stimulation. Intracellular recordings with potassium-acetate-filled electrodes revealed that the bursts of ventral root discharge induced by NO donors were accompanied by phasic depolarisations in motor neurons. During the inter-burst intervals, periods of substantial membrane hyperpolarization below the normal resting potential were observed, presumably coincident with contralateral ventral root activity. With KCl-filled electrodes, inhibitory potentials were strongly depolarising, suggesting that inhibition was Cl(−)-dependent. The synaptic drive seen in motor neurons after dimming of the illumination was very similar to that induced by the NO donors. NADPH-diaphorase histochemistry identified putative endogenous sources of NO in the central nervous system and the skin. Three populations of bilaterally symmetrical neurons were identified within the brainstem. Some of these neurons had contralateral projections and many had axonal processes that projected to and entered the marginal zones of the spinal cord, suggesting that they were reticulospinal.


1992 ◽  
Vol 67 (3) ◽  
pp. 648-663 ◽  
Author(s):  
P. Skorupski ◽  
B. M. Rawat ◽  
B. M. Bush

1. Movement of the crayfish thoracocoxal leg joint is monitored by a muscle receptor organ (TCMRO) and a chordotonal organ (TCCO). Both receptors span the joint in parallel but signal opposite directions of leg movement. The TCMRO is innervated by afferents responsive to lengthening, which corresponds to leg remotion, whereas TCCO afferents are responsive to shortening of the chordotonal strand, which corresponds to leg promotion. 2. When both receptors are stimulated in parallel, in an otherwise isolated preparation, reflex responses of coxal promoter and remotor motor neurons occur on both stretch and release. By comparison with experiments where one or the other of these receptors is stimulated selectively, we conclude that reflexes evoked by stretch of the two receptors are due to the TCMRO and reflexes evoked by release are due to the TCCO. 3. Reflexes mediated by these receptors are both state dependent and phase dependent. In preparations that produce patterns of reciprocal motor activity in promotor and remotor motor neurons (the active state), the reflex effect depends on the phase of this centrally generated activity. In preparations that are quiescent, or that produce only tonic motor output (the inactive state), the reflex effect is stable, corresponding to a typical resistance (negative feedback) reflex for both directions of receptor movement. 4. In the active state, coxal promotor motor neurons are both excited and inhibited in a phase-dependent manner by stretching the TCMRO. A subgroup of promotor motor neurons is excited by shortening the TCCO. One subgroup of the antagonistic coxal remotor motor neurons receives phase-dependent excitation from stretch of the TCMRO, whereas a second subgroup receives phase-dependent excitation from shortening the TCCO. 5. There are, therefore, at least two ways in which reflex effects can be modulated. At the level of a single motor neuron, the reflex response can vary in gain, and in some cases in sign, in a manner depending on centrally generated motor activity. In addition, at the level of a pool of synergistic motor neurons, the reflex effect is not uniform; instead, different subgroups of motor neurons display different reflex effects, so that the relative levels of excitability of different motor neuron reflex subgroups can also determine the net reflex effect. 6. Excitation of promotor motor neurons by TCCO shortening and of remotor motor neurons by TCMRO lengthening are positive feedback reflexes. The subgroups of motor neurons in which positive feedback reflexes can be evoked in both promotor and remotor pools are termed group 1.(ABSTRACT TRUNCATED AT 400 WORDS)


1996 ◽  
Vol 75 (2) ◽  
pp. 561-574 ◽  
Author(s):  
E. M. Quinlan ◽  
A. D. Murphy

1. The mechanism for generating diverse patterns of buccal motor neuron activity was explored in the multifunctional central pattern generator (CPG) of Helisoma. The standard pattern of motor neuron activity, which results in typical feeding behavior, consists of three distinct phases of buccal motor neuron activity. We have previously identified CPG interneurons that control the motor neuron activity during phases 1 and 2 of the standard pattern. Here we identify a pair of interneurons responsible for buccal motor neuron activity during phase 3, and examine the variability in the interactions between this third subunit and other subunits of the CPG. 2. During the production of the standard pattern, phase 3 excitation in many buccal motor neurons follows a prominent phase 2 inhibitory postsynaptic potential. Therefore phase 3 excitation was previously attributed to postinhibitory rebound (PIR) in these motor neurons. Two classes of observations indicated that PIR was insufficient to account for phase 3 activity, necessitating phase 3 interneurons. 1) A subset of identified buccal neurons is inhibited during phase 3 by discrete synaptic input. 2) Other identified buccal neurons display discrete excitation during both phases 2 and 3. 3. A bilaterally symmetrical pair of CPG interneurons, named N3a, was identified and characterized as the source of phase 3 postsynaptic potentials in motor neurons. During phase 3 of the standard motor pattern, interneuron N3a generated bursts of action potentials. Stimulation of N3a, in quiescent preparations, evoked a depolarization in motor neurons that are excited during phase 3 and a hyperpolarization in motor neurons that are inhibited during phase 3. Hyperpolarization of N3a during patterned motor activity eliminated both phase 3 excitation and inhibition. Physiological and morphological characterization of interneuron N3a is provided to invite comparisons with possible homologues in other gastropod feeding CPGs. 4. These data support a model proposed for the organization of the tripartite buccal CPG. According to the model, each of the three phases of buccal motor neuron activity is controlled by discrete subsets of pattern-generating interneurons called subunit 1 (S1), subunit 2 (S2), and subunit 3 (S3). The standard pattern of buccal motor neuron activity underlying feeding is mediated by an S1-S2-S3 sequence of CPG subunit activity. However, a number of "nonstandard" patterns of buccal motor activity were observed. In particular, S2 and S3 activity can occur independently or be linked sequentially in rhythmic patterns other than the standard feeding pattern. Simultaneous recordings of S3 interneuron N3a with effector neurons indicated that N3a can account for phase-3-like postsynaptic potentials (PSPs) in nonstandard patterns. The variety of patterns of buccal motor neuron activity indicates that each CPG subunit can be active in the absence of, or in concert with, activity in any other subunit. 5. To explore how CPG activity may be regulated to generate a particular motor pattern from the CPG's full repertoire, we applied the neuromodulator serotonin. Serotonin initiated and sustained the production of an S2-S3 pattern of activity, in part by enhancing PIR in S3 interneuron N3a after the termination of phase 2 inhibition.


1993 ◽  
Vol 70 (5) ◽  
pp. 2136-2147 ◽  
Author(s):  
R. L. Sainburg ◽  
H. Poizner ◽  
C. Ghez

1. We analyzed the performance of a simple pantomimed gesture in 2 patients with large-fiber sensory neuropathy and 11 control subjects to determine how proprioceptive deafferentation disrupts unconstrained multijoint movements. Both patients had near-total loss of joint position, vibration, and discriminative touch sensation in the upper extremities. Muscle strength remained intact. 2. Subjects performed a gesture similar to slicing a loaf of bread. In this gesture, the hand first moves outward from the body, reverses direction sharply, and then moves back toward the body. Accurate performance requires precise coordination between the shoulder and elbow joints during movement reversals. Movements were performed under two conditions: with eyes open and with eyes closed. Three dimensional shoulder, elbow, wrist, and hand trajectories were recorded on a WATSMART system. 3. When control subjects performed the gesture with their eyes closed, their wrist trajectories were relatively straight and individual cycles of motion were planar. Movements reversed direction sharply, such that outward and inward portions of the wrist path were closely aligned. Corresponding to this spatial profile, the reversals in movement direction at the shoulder joint, from flexion to extension, and at the elbow joint, from extension to flexion, were synchronous. 4. In contrast, when deafferented patients performed the gesture with their eyes closed, their wrist trajectories were highly curved and individual cycles were severely nonplanar. The wrist paths showed a characteristic anomaly during the reversal in movement direction, when elbow joint movement became transiently locked. Correspondingly, the movement reversals at the shoulder and elbow joints were severely temporally decoupled. 5. When patients were able to view their limbs during performance of this gesture there was significant improvement in the linearity and planarity of movements. However, the patients remained unable to synchronize the movements at the shoulder and elbow joints to produce spatially precise wrist paths. 6. We conclude that loss of proprioception disrupts interjoint coordination and discuss the hypothesis that this interjoint coordination deficit results from a failure to control the interaction forces that arise between limb segments during multijoint movements.


2012 ◽  
Vol 107 (10) ◽  
pp. 2756-2768 ◽  
Author(s):  
Jan M. Ache ◽  
Thomas Matheson

Limb movements can be driven by muscle contractions, external forces, or intrinsic passive forces. For lightweight limbs like those of insects or small vertebrates, passive forces can be large enough to overcome the effects of gravity and may even generate limb movements in the absence of active muscle contractions. Understanding the sources and actions of such forces is therefore important in understanding motor control. We describe passive properties of the femur-tibia joint of the locust hind leg. The resting angle is determined primarily by passive properties of the relatively large extensor tibiae muscle and is influenced by the history of activation of the fast extensor tibiae motor neuron. The resting angle is therefore better described as a history-dependent resting state. We selectively stimulated different flexor tibiae motor neurons to generate a range of isometric contractions of the flexor tibiae muscle and then stimulated the fast extensor tibiae motor neuron to elicit active tibial extensions. Residual forces in the flexor muscle have only a small effect on subsequent active extensions, but the effect is larger for distal than for proximal flexor motor neurons and varies with the strength of flexor activation. We conclude that passive properties of a lightweight limb make substantial and complex contributions to the resting state of the limb that must be taken into account in the patterning of neuronal control signals driving its active movements. Low variability in the effects of the passive forces may permit the nervous system to accurately predict their contributions to behavior.


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