Intersegmental coordination of leech swimming: comparison of in situ and isolated nerve cord activity with body wall movement

Pearce, Robert A.; Wo, Friesen

doi:10.1016/0006-8993(84)90720-0

Cited by 40 publications

(36 citation statements)

References 3 publications

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“…Body shape was monitored with video recordings. The intersegmental phase lags of MN activity found in these independent experiments were 11.8 deg per segment (Pearce and Friesen, 1984) and 13.8 deg per segment (Yu et al, 1999). The ratio of wave propagation speed between body curvature and MN activation was about 0.77 (0.7411.8/16 in the former experiment and 0.8013.8/17.3 in the latter).…”

Section: Discussion Predicted Mn Activation and Muscle Tension In Commentioning

confidence: 59%

“…The relationship of MN output to the longitudinal muscles and swimming undulations was investigated in previous experiments on medicinal leeches. The occurrence of MN spikes (generated by dorsal excitatory MN cell DE-3) was recorded from electrodes implanted at two spatially separated points in the mid-body of nearly intact swimming leeches (Pearce and Friesen, 1984;Yu et al, 1999). In these experiments, the leeches were tethered by threads attached to the denervated head and tail suckers and suspended in a water tank.…”

Section: Discussion Predicted Mn Activation and Muscle Tension In Commentioning

confidence: 99%

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Mechanisms underlying rhythmic locomotion: interactions between activation, tension and body curvature waves

Friesen

Iwasaki

2012

Journal of Experimental Biology

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SUMMARYUndulatory animal locomotion arises from three closely related propagating waves that sweep rostrocaudally along the body: activation of segmental muscles by motoneurons (MNs), strain of the body wall, and muscle tension induced by activation and strain. Neuromechanical models that predict the relative propagation speeds of neural/muscle activation, muscle tension and body curvature can reveal crucial underlying control features of the central nervous system and the power-generating mechanisms of the muscle. We provide an analytical explanation of the relative speeds of these three waves based on a model of neuromuscular activation and a model of the body-fluid interactions for leech anguilliform-like swimming. First, we deduced the motoneuron spike frequencies that activate the muscle and the resulting muscle tension during swimming in intact leeches from muscle bending moments. Muscle bending moments were derived from our video-recorded kinematic motion data by our body-fluid interaction model. The phase relationships of neural activation and muscle tension in the strain cycle were then calculated. Our study predicts that the MN activation and body curvature waves have roughly the same speed (the ratio of curvature to MN activation speedϷ0.84), whereas the tension wave travels about twice as fast. The high speed of the tension wave resulting from slow MN activation is explained by the multiplicative effects of MN activation and muscle strain on tension development. That is, the product of two slower waves (activation and strain) with appropriate amplitude, bias and phase can generate a tension wave with twice the propagation speed of the factors. Our study predicts that (1) the bending moment required for swimming is achieved by minimal MN spike frequency, rather than by minimal muscle tension; (2) MN activity is greater in the mid-body than in the head and tail regions; (3) inhibitory MNs not only accelerate the muscle relaxation but also reduce the intrinsic tonus tension during one sector of the swim cycle; and (4) movements of the caudal end are passive during swimming. These predictions await verification or rejection through further experiments on swimming animals.

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Section: Discussion Predicted Mn Activation and Muscle Tension In Commentioning

confidence: 59%

Section: Discussion Predicted Mn Activation and Muscle Tension In Commentioning

confidence: 99%

Mechanisms underlying rhythmic locomotion: interactions between activation, tension and body curvature waves

Friesen

Iwasaki

2012

Journal of Experimental Biology

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“…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).…”

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confidence: 86%

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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“…The fundamental rhythmicity of rhythmic motor patterns such as undulatory crawling and swimming, swimmeret beating, and legged locomotion arises from the activity of rhythmic central neural networks [(central pattern generators (CPGs)] [lamprey (Wallén and Williams, 1984); leech (Pearce and Friesen, 1984); crayfish swimmerets (Skinner and Mulloney, 1998); Manduca crawling (Johnston and Levine, 1996b); mammals (Kiehn and Kjaerulff, 1998); turtle (Stein, 2008); stick insect (Büschges, 2005)]. However, production of these patterns requires not only rhythmicity but also coordination of the body segments or appendages that produce the movements, and the neural basis of this coordination shows great interspecies and interbehavior variation.…”

Section: Introductionmentioning

confidence: 99%

Sensory Feedback Induced by Front-Leg Stepping Entrains the Activity of Central Pattern Generators in Caudal Segments of the Stick Insect Walking System

Borgmann¹,

Hooper²,

Büschges³

2009

J. Neurosci.

106

157

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Legged locomotion results from a combination of central pattern generating network (CPG) activity and intralimb and interlimb sensory feedback. Data on the neural basis of interlimb coordination are very limited. We investigated here the influence of stepping in one leg on the activities of neighboring-leg thorax-coxa (TC) joint CPGs in the stick insect (Carausius morosus). We used a new approach combining single-leg stepping with pharmacological activation of segmental CPGs, sensory stimulation, and additional stepping legs. Stepping of a single front leg could activate the ipsilateral mesothoracic TC CPG. Activation of the metathoracic TC CPG required that both ipsilateral front and middle legs were present and that one of these legs was stepping. Unlike the situation in real walking, ipsilateral mesothoracic and metathoracic TC CPGs activated by front-leg stepping fired in phase with the front-leg stepping. Local (intralimb) sensory feedback from load sensors could override this intersegmental influence of front-leg stepping, shifting retractor motoneuron activity relative to the front-leg step cycle and thereby uncoupling them from front-leg stepping. These data suggest that front-leg stepping in isolation would result in in-phase activity of all ipsilateral legs, and functional stepping gaits (in which the three ipsilateral legs do not step in synchrony) emerge because of local load sensory feedback overriding this in-phase influence.

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Intersegmental coordination of leech swimming: comparison of in situ and isolated nerve cord activity with body wall movement

Cited by 40 publications

References 3 publications

Mechanisms underlying rhythmic locomotion: interactions between activation, tension and body curvature waves

Mechanisms underlying rhythmic locomotion: interactions between activation, tension and body curvature waves

Biological clockwork underlying adaptive rhythmic movements

Sensory Feedback Induced by Front-Leg Stepping Entrains the Activity of Central Pattern Generators in Caudal Segments of the Stick Insect Walking System

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