Orientation-Dependent Changes in Single Motor Neuron Activity during Adaptive Soft-Bodied Locomotion

2015 ◽  
Vol 85 (1) ◽  
pp. 47-62 ◽  
Author(s):  
Cinzia Metallo ◽  
Barry A. Trimmer

Recent major advances in understanding the organizational principles underlying motor control have focused on a small number of animal species with stiff articulated skeletons. These model systems have the advantage of easily quantifiable mechanics, but the neural codes underlying different movements are difficult to characterize because they typically involve a large population of neurons controlling each muscle. As a result, studying how neural codes drive adaptive changes in behavior is extremely challenging. This problem is highly simplified in the tobacco hawkmoth Manduca sexta, which, in its larval stage (caterpillar), is predominantly soft-bodied. Since each M. sexta muscle is innervated by one, occasionally two, excitatory motor neurons, the electrical activity generated by each muscle can be mapped to individual motor neurons. In the present study, muscle activation patterns were converted into motor neuron frequency patterns by identifying single excitatory junction potentials within recorded electromyographic traces. This conversion was carried out with single motor neuron resolution thanks to the high signal selectivity of newly developed flexible microelectrode arrays, which were specifically designed to record from M. sexta muscles. It was discovered that the timing of motor neuron activity and gait kinematics depend on the orientation of the plane of motion during locomotion. We report that, during climbing, the motor neurons monitored in the present study shift their activity to correlate with movements in the animal's more anterior segments. This orientation-dependent shift in motor activity is in agreement with the expected shift in the propulsive forces required for climbing. Our results suggest that, contrary to what has been previously hypothesized, M.sexta uses central command timing for adaptive load compensation.

1979 ◽  
Vol 42 (5) ◽  
pp. 1223-1232 ◽  
Author(s):  
E. Shapiro ◽  
J. Koester ◽  
J. H. Byrne

1. A behavioral and electrophysiological analysis of defensive ink release in Aplysia californica was performed to examine the response of this behavior and its underlying neural circuit to various-duration noxious stimuli. 2. Three separate behavioral protocols were employed using electrical shocks to the head as noxious stimuli to elicit ink release. Ink release was found to be selectively responsive to longer duration stimuli, and to increase in a steeply graded fashion as duration is increased. 3. Intracellular stimulation of ink motor neurons revealed that ink release is a linear function of motor neuron spike train duration, indicating that the selective sensitivity of the behavior to long-duration stimuli is not due to a nonlinearity in the glandular secretory process. 4. In contrast, electrophysiological examination of ink motor neuron activity in response to sustained head shock revealed an accelerating spike train. During the later part of the spike train, compound excitatory synaptic potentials show a positive shift in reversal potential. 5. Our results suggest a central locus for the mechanisms that determine sensitivity of inking behavior to stimulus duration. 6. In contrast to ink release, defensive gill withdrawal was found to be extremely sensitive to short-duration stimuli.


1984 ◽  
Vol 51 (6) ◽  
pp. 1375-1393 ◽  
Author(s):  
J. S. Eisen ◽  
E. Marder

During motor activity of the pyloric system of the lobster stomatogastric ganglion, there are rhythmic alternations between activity in the pyloric dilator (PD) and pyloric (PY) motor neurons. We studied the phase relations between PD motor neuron activity and PY motor neuron activity in preparations cycling at a wide range of frequencies and after altering the activity of the PD neurons. The PY neurons fall into two classes, early (PE) and late (PL) (21), distinguished by the different phases in the pyloric cycle at which they fire. The phase at which PE neurons fired and the phase at which PL neurons fired was independent of pyloric cycle frequency over a range of frequencies from 0.5 to 2.25 Hz. The anterior burster (AB) interneuron is electrically coupled to the PD motor neurons. Together the AB and PD neurons form the pacemaker for the pyloric system. Synchronous depolarization of the AB and PD neurons evokes a complex inhibitory post-synaptic potential (IPSP) in PY neurons. This IPSP has two components: an early, AB neuron-derived component and a late, PD neuron-derived component. Deletion of the PD neurons from the pyloric circuit by photoinactivation removed the PD-evoked component of the pacemaker-evoked IPSP. This resulted in a decrease in the duration of the IPSP evoked by pacemaker depolarization and a significant advance in the firing phase of PY neurons. Bath application of dopamine was used to hyperpolarize and inhibit the PD neurons (30), causing them to release less neurotransmitter. As a consequence, the duration of the IPSP evoked by pacemaker depolarization was decreased and the firing phase of the PY neurons was significantly advanced. Stimulation of the inferior ventricular nerve (IVN) produces a slow excitation of the PD neurons (30), causing them to release more neurotransmitter. Consequently, the duration of the IPSP evoked by pacemaker depolarization was increased and the firing phase of the PY neurons was significantly retarded for several cycles of pyloric activity following IVN stimulation. Thus, modulation of the strength of PD-evoked inhibition in PY neurons is responsible for altering the firing phase of the PY neurons with respect to the pyloric pacemaker. We suggest that frequency of the pyloric output and the phase relations of the elements within the pyloric cycle can be regulated independently. The potential implications of these data for modulation of synaptic efficacy in other preparations are discussed.


2019 ◽  
Vol 20 (16) ◽  
pp. 3848 ◽  
Author(s):  
Baris Genc ◽  
Oge Gozutok ◽  
P. Hande Ozdinler

Motor neuron circuitry is one of the most elaborate circuitries in our body, which ensures voluntary and skilled movement that requires cognitive input. Therefore, both the cortex and the spinal cord are involved. The cortex has special importance for motor neuron diseases, in which initiation and modulation of voluntary movement is affected. Amyotrophic lateral sclerosis (ALS) is defined by the progressive degeneration of both the upper and lower motor neurons, whereas hereditary spastic paraplegia (HSP) and primary lateral sclerosis (PLS) are characterized mainly by the loss of upper motor neurons. In an effort to reveal the cellular and molecular basis of neuronal degeneration, numerous model systems are generated, and mouse models are no exception. However, there are many different levels of complexities that need to be considered when developing mouse models. Here, we focus our attention to the upper motor neurons, which are one of the most challenging neuron populations to study. Since mice and human differ greatly at a species level, but the cells/neurons in mice and human share many common aspects of cell biology, we offer a solution by focusing our attention to the affected neurons to reveal the complexities of diseases at a cellular level and to improve translational efforts.


Author(s):  
Jens Peter Gabriel ◽  
Ansgar Büschges

In the single middle leg preparation of the stick insect walking on a treadmill, the activity of flexor and extensor tibiae motor neurons and muscles, which are responsible for the movement of the tibia in stance and swing phases, respectively, was investigated with respect to changes in stepping velocity. Changes in stepping velocity were correlated with cycle period. There was a close correlation of flexor motor neuron activity (stance phase) with stepping velocity, but the duration and activation of extensor motor neurons (swing phase) was not altered. The depolarization of flexor motor neurons showed two components. At all step velocities, a stereotypic initial depolarization was generated at the beginning of stance phase activity. A subsequent larger depolarization and activation was tightly linked to belt velocity, i.e. it occurred earlier and with larger amplitude during fast steps compared with slow steps. Alterations in a tonic background excitation appear not to play a role in controlling the motor neuron activity for changes in stepping velocity. Our results indicate that in the single insect leg during walking, mechanisms for altering stepping velocity become effective only during an already ongoing stance phase motor output. We discuss the putative mechanisms involved.


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)


2019 ◽  
Vol 11 (523) ◽  
pp. eaav5264 ◽  
Author(s):  
Irit Reichenstein ◽  
Chen Eitan ◽  
Sandra Diaz-Garcia ◽  
Guy Haim ◽  
Iddo Magen ◽  
...  

Motor neuron–specific microRNA-218 (miR-218) has recently received attention because of its roles in mouse development. However, miR-218 relevance to human motor neuron disease was not yet explored. Here, we demonstrate by neuropathology that miR-218 is abundant in healthy human motor neurons. However, in amyotrophic lateral sclerosis (ALS) motor neurons, miR-218 is down-regulated and its mRNA targets are reciprocally up-regulated (derepressed). We further identify the potassium channel Kv10.1 as a new miR-218 direct target that controls neuronal activity. In addition, we screened thousands of ALS genomes and identified six rare variants in the human miR-218-2 sequence. miR-218 gene variants fail to regulate neuron activity, suggesting the importance of this small endogenous RNA for neuronal robustness. The underlying mechanisms involve inhibition of miR-218 biogenesis and reduced processing by DICER. Therefore, miR-218 activity in motor neurons may be susceptible to failure in human ALS, suggesting that miR-218 may be a potential therapeutic target in motor neuron disease.


1984 ◽  
Vol 52 (3) ◽  
pp. 389-409 ◽  
Author(s):  
M. Peters ◽  
U. Altrup

Identified motor neurons in the buccal ganglia of Helix pomatia and pharynx muscles innervated by them were studied with intracellular recording and cobalt staining. Retrograde cobalt staining via the buccal nerves indicated that neurons occupy relatively constant positions within the ganglia. With intracellular cobalt staining it was shown that the shape of a representative motor neuron (B4) is similar in different preparations. In some cases, however, deviations from the normal pattern of axon distribution were found. Presumed motor endings of neuron B4 in the muscle were also visualized with intracellular staining. Recordings from individual motor neurons show typical phase relationships of spontaneous spike activity. Most motor neurons are active in the retraction phase of the radula. Only excitatory motor neurons were found. Most neurons directly supply more than one muscle. Amplitude of excitatory junction potentials (EJP) and plasticity at neuromuscular junctions from one neuron are similar in different muscles. Single muscle fibers receive polyneuronal innervation. Activity of single motor neurons already leads to muscle contraction even without spiking of the muscle cells. Muscle tension depends on integrated EJP size. Most motor neurons supply typical combinations of a set of muscles. Thus, several muscles can be activated synchronously by activity of a single motor neuron. In this way muscle combinations are predetermined morphologically by the peripheral branching patterns of the respective neurons.


2000 ◽  
Vol 83 (6) ◽  
pp. 3337-3350 ◽  
Author(s):  
Andrew K. Tryba ◽  
Roy E. Ritzmann

In a previous study, we combined joint kinematics and electromyograms (EMGs) to examine the change in the phase relationship of two principal leg joints during walking and searching. In this study, we recorded intracellularly from motor neurons in semi-intact behaving animals to examine mechanisms coordinating extension at these leg joints. In particular, we examined the change in the phase of the coxa-trochanter (CTr) and femur-tibia (FT) joint extension during walking and searching. In doing so, we discovered marked similarities in the activity of CTr and FT joint extensor motor neurons at the onset of extension during searching and at the end of stance during walking. The data suggest that the same interneurons may be involved in coordinating the CTr and FT extensor motor neurons during walking and searching. Previous studies in stick insects have suggested that extensor motor neuron activity during the stance phase of walking results from an increase in tonic excitation of the neuron leading to spiking that is periodically interrupted by centrally generated inhibition. However, the CTr and FT extensor motor neuron activity during walking consists of characteristic phasic modulations in motor neuron frequency within each step cycle. The phasic increases and decreases in extensor EMG frequency during stance are associated with kinematic events (i.e., foot set-down and joint cycle transitions) during walking. Sensory feedback associated with these events might be responsible for phasic modulation of the extensor motor neuron frequency. However, our data rule out the possibility that sensory cues resulting from foot set-down are responsible for a decline in CTr extensor activity that is characteristic of the Blaberusstep cycle. Our data also suggest that both phasic excitation and inhibition contribute to extensor motor neuron activity during the stance phase of walking.


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.


2021 ◽  
Vol 104 (2) ◽  
pp. 003685042110080
Author(s):  
Jeffrey W Keller ◽  
Annina Fahr ◽  
Julia Balzer ◽  
Jan Lieber ◽  
Hubertus JA van Hedel

Current clinical assessments evaluating selective voluntary motor control are measured on an ordinal scale. We combined the Selective Control of the Upper Extremity Scale (SCUES) with surface electromyography to develop a more objective and interval-scaled assessment of selective voluntary motor control. The resulting Similarity Index (SI) quantifies the similarity of muscle activation patterns. We aimed to evaluate the validity and reliability of this new assessment named SISCUES (Similarity Index of the SCUES) in children with upper motor neuron lesions. Thirty-three patients (12.2 years [8.8;14.9]) affected by upper motor neuron lesions with mild to moderate impairments and 31 typically developing children (11.6 years [8.5;13.9]) participated. We calculated reference muscle activation patterns for the SISCUES using data of 33 neurologically healthy adults (median [1st; 3rd quantile]: 32.5 [27.9; 38.3]). We calculated Spearman correlations (ρ) between the SISCUES and the SCUES and the Manual Ability Classification System (MACS) to establish concurrent validity. Discriminative validity was tested by comparing scores of patients and healthy peers with a robust ANCOVA. Intraclass correlation coefficients2,1 and minimal detectable changes indicated relative and absolute reliability. The SISCUES correlates strongly with SCUES (ρ = 0.76, p < 0.001) and moderately with the MACS (ρ = −0.58, p < 0.001). The average SISCUES can discriminate between patients and peers. The intraclass correlation coefficient2,1 was 0.90 and the minimal detectable change was 0.07 (8% of patients’ median score). Concurrent validity, discriminative validity, and reliability of the SISCUES were established. Further studies are needed to evaluate whether it is responsive enough to detect changes from therapeutic interventions.


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