Analysis of impulse adaptation in motoneurons

Tian, Jianghong; Iwasaki, Tetsuya; Friesen, W. Otto

doi:10.1007/s00359-009-0499-3

Cited by 9 publications

(10 citation statements)

References 21 publications

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“…The tension difference between the two sides gives rise to the muscle bending moment, which shapes body undulations. Each segmental CPG commands local muscle contraction through MN activation dynamics containing a time lag and impulse adaptation (13). CPG interneurons form a complex set of interactions with MNs to ensure that dorsal muscle is excited at 0°and inhibited at about 180°, and ventral muscle is driven in antiphase.…”

Section: Resultsmentioning

confidence: 99%

“…An obstacle in exploring the emergence of the functional properties from highly interconnected neuronal circuits through model-based analysis is the lack of biological realism (1). We, therefore, have focused on the individual components of the leech swimming system and developed dedicated models, with full experimental validations, for capturing essential dynamics of the CPG (12), motoneuron (MN) impulse adaptation (13), passive and active muscle dynamics (14,15), body-fluid interactions (16), and, finally, sensory feedback of body wall tension from peripheral receptors to the CPG (17).…”

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confidence: 99%

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Biological clockwork underlying adaptive rhythmic movements

Iwasaki

Friesen

2014

Proc. Natl. Acad. Sci. U.S.A.

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Owing to the complexity of neuronal circuits, precise mathematical descriptions of brain functions remain an elusive ambition. A more modest focus of many neuroscientists, central pattern generators, are more tractable neuronal circuits specialized to generate rhythmic movements, including locomotion. The relative simplicity and welldefined motor functions of these circuits provide an opportunity for uncovering fundamental principles of neuronal information processing. Here we present the culmination of mathematical analysis that captures the adaptive behaviors emerging from interactions between a central pattern generator, the body, and the physical environment during locomotion. The biologically realistic model describes the undulatory motions of swimming leeches with quantitative accuracy and, without further parameter tuning, predicts the sweeping changes in oscillation patterns of leeches undulating in air or swimming in high-viscosity fluid. The study demonstrates that central pattern generators are capable of adapting oscillations to the environment through sensory feedback, but without guidance from the brain.A long-term ambition in neuroscience is to generate a detailed, complete model of the human brain (1). Still ambitious, and certainly more realistic, is the aim to model components of vertebrate nervous systems. Most advanced in this arena are models based on the circuits underlying motor functions, such as rhythmic body movements during locomotion. These movements are generated by spinal neural oscillator circuits called central pattern generators (CPGs) (2, 3). The enormous number of neurons in the vertebrate central nervous system currently prevents analysis at the level of defined circuits between individual neurons. However, the simpler, accessible CPGs underlying locomotion in the invertebrates provide dynamically rich platforms amenable to detailed analysis that can lead to deep understanding of how neuronal circuits generate extremely robust and adaptive oscillatory behaviors. The leech CPG for undulatory swimming provides such a platform. The isolated nerve cord, with most (4, 5), a few (6, 7), or even a single segmental ganglion (8, 9), displays "fictive swimming," where the rhythmic motor pattern closely resembles that recorded in intact animals. Moreover, the leech continues to swim without the brain (10, 11), with the nerve cord severed in midbody (5), or with the body cut in half (7).Our study addresses the following question: How does the leech swimming system achieve its astonishing robustness and adaptability? A detailed explanation of the mechanisms underlying such complex phenomena requires mathematical modeling and analysis because a unidirectional sequence of cause-andeffect relationships alone cannot explain dynamical properties arising from multiple feedback loops. An obstacle in exploring the emergence of the functional properties from highly interconnected neuronal circuits through model-based analysis is the lack of biological realism (1). We, therefore, have focused on the...

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Section: Resultsmentioning

confidence: 99%

mentioning

confidence: 99%

Biological clockwork underlying adaptive rhythmic movements

Iwasaki

Friesen

2014

Proc. Natl. Acad. Sci. U.S.A.

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“…The evoked impulse frequencies of the stimulated MNs were estimated from spikes recorded by extracellular suction electrodes in peripheral nerves that carry the axons of contralateral MNs. It had previously been shown that, because of electrical coupling between homologs, impulse frequency in one MN can be estimated by multiplying the impulse frequency in its homolog by a factor of 3 (Tian, 2008;Tian et al, 2010). The amplitude of the injected current ranged from 2 to 3 nA to evoke MN impulse bursts with impulse frequencies similar to those recorded in swimming leeches (Yu et al, 1999).…”

Section: Methodsmentioning

confidence: 99%

“…Impulse frequency was calculated as the reciprocal of interspike intervals. The impulse frequency of the target MN DE-3 was estimated to be three times that computed from extracellular recordings of impulses generated by the contralateral MN (Tian et al, 2010). The bottom trace is the tension resulting from the strain and MN input to the longitudinal muscles; maximum tension is ~3 gram force (0.02958 N).…”

Section: Validation Of the Multiplicative Model Structurementioning

confidence: 99%

“…We have developed mathematical models of the central pattern generator (CPG) Zheng, 2007), impulse adaptation in MNs (Tian et al, 2010), passive properties of longitudinal muscles of the body wall (Tian et al, 2007;Tian, 2008) and body-fluid interactions during undulatory swimming (Chen et al, 2011). The muscle model with MN activation developed here will be integrated with these component models later to study the feedback control mechanisms underlying animal locomotion.…”

Section: Introductionmentioning

confidence: 99%

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Mechanisms underlying rhythmic locomotion: dynamics of muscle activation

Chen

Tian

Iwasaki

et al. 2011

Journal of Experimental Biology

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SUMMARYWe have studied the dynamical properties of tension development in leech longitudinal muscle during swimming. A new method is proposed for modeling muscle properties under functionally relevant conditions where the muscle is subjected to both periodic activation and rhythmic length changes. The 'dual-sinusoid' experiments were conducted on preparations of leech nerve cord and body wall. The longitudinal muscle was activated periodically by injection of sinusoidal currents into an identified motoneuron. Simultaneously, sinusoidal length changes were imposed on the body wall with prescribed phase differences (12 values equally spaced over 2 radians) with respect to the current injection. Through the singular value decomposition of appropriately constructed tension data matrices, the leech muscle was found to have a multiplicative structure in which the tension was expressed as the product of activation and length factors. The time courses of activation and length factors were determined from the tension data and were used to develop component models. The proposed modeling method is a general one and is applicable to contractile elements for which the effects of series elasticity are negligible.

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The activity of leech motoneurons during motor patterns is regulated by intrinsic properties and synaptic inputs

et al. 2011

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The activity of motoneurons during motor patterns depends on their intrinsic properties and on synaptic inputs. This study analyzed the properties of two leech motoneurons: the excitors of dorsal longitudinal muscles (DE-3) and of dorsal and ventral longitudinal muscles (MN-L) in basal conditions (normal and high Mg²⁺ saline) and during crawling. The voltage-current relationships in DE-3 and MN-L were similar. The curves exhibited the largest slope around resting potential, showed marked inward and outward rectification, and were not affected by high Mg²⁺. In response to 5-s pulses, DE-3 exhibited a fast initial adaptation, a slow recovery and a very slow late adaptation. High Mg²⁺ abolished the initial high frequency. The frequency-voltage relationship for the rest of the response was highly similar in normal and in high Mg²⁺ saline. MN-L exhibited a minor initial adaptation and then fired steadily. High Mg²⁺ diminished the frequency-voltage relationship. During crawling DE-3 and MN-L fired in phase and their frequency-voltage curves overlapped with the lower end of the curves obtained in basal conditions. The results suggest that the activity of these motoneurons during crawling was regulated, to a large extent, by synaptic inputs.

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Analysis of impulse adaptation in motoneurons

Cited by 9 publications

References 21 publications

Biological clockwork underlying adaptive rhythmic movements

Biological clockwork underlying adaptive rhythmic movements

Mechanisms underlying rhythmic locomotion: dynamics of muscle activation

The activity of leech motoneurons during motor patterns is regulated by intrinsic properties and synaptic inputs

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