The neurophysiological bases of undulatory locomotion in vertebrates

Grillner, Sten; Matsushima, Toshiya; Wadden, Tom; Tegnér, Jesper; Manira, Abdeljabbar El; Wallén, Peter

doi:10.1016/s1044-5765(05)80021-1

Cited by 30 publications

(16 citation statements)

References 37 publications

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“…For such fictive preparations of lampreys (Cohen and Wallan 1980;Wall6n and Williams 1984), sharks (Bone 1966), and teleost fish (Fetcho and Svoboda 1993), the motor output consists of a rhythmic pattern of alternating, unilateral activity that is propagated posteriorly. These experiments suggest that spinal motor pattern generators are sufficient to produce most features of the rhythmic motor patterns used during locomotion (McClellan 1988;Grillner et al 1991;Grillner et al 1993).…”

Section: Introductionmentioning

confidence: 79%

“…For in vitro preparations of lamprey spinal cords, Matsushima and Grillner (1992) were able to produce both a rostro-caudal and caudo-rostral propagation of activity depending on which spinal segment was excited with the application of an amino acid. These experiments collectively suggest that motor pattern generators within each segment of the spinal cord are sufficient to produce the rhythmic motor patterns of locomotion (McClellan 1988;Grillner et al 1991;Grillner et al 1993). Furthermore, the relative excitability and interactions of adjacent spinal segments play a major role in determining how motor activity propagates along the length of the animal (McClellan 1988;Grillner et al 1991;Grillner et al 1993).…”

Section: Motor Patternmentioning

confidence: 90%

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Muscle activity in autotomized tails of a lizard (Gekko gecko): a naturally occurring spinal preparation

Rumping

Jayne

1996

J Comp Physiol A

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We quantified muscle activity in tails of lizards (Gekko gecko) during running and after autotomy of the tail. We chose different animals and varied where we broke the tails in order to obtain three experimental preparations having: no regenerated tissue or prior tail loss (non-regenerated), a large regenerated portion and a few original caudal vertebrae (partially regenerated), and only regenerated tissue (fully regenerated). All observed axial motor patterns were rhythmic. During running of intact animals, muscles in non-regenerated tails were activated in an alternating, unilateral pattern that was propagated posteriorly. After autotomy, non-regenerated tails had unilateral muscle activity that alternated between the left and right sides and propagated anteriorly. Autotomized, partially regenerated tails had unilateral, alternating muscle activity that lacked any longitudinal propagation. Autotomized, fully regenerated tails had periodic muscle activity that occurred simultaneously for both left and right sides and all longitudinal positions. Neither tactile stimulation nor removal of the tail tip prior to autotomizing the tail affected the motor pattern. Several features of the motor pattern of autotomized tails changed significantly with increased time after autotomy. Autotomized tails with one or more spinal segments moved longer and more vigorously than autotomized tails consisting entirely of regenerated (unsegmented) tissue.

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Section: Introductionmentioning

confidence: 79%

Section: Motor Patternmentioning

confidence: 90%

Muscle activity in autotomized tails of a lizard (Gekko gecko): a naturally occurring spinal preparation

Rumping

Jayne

1996

J Comp Physiol A

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“…This connectivity now facilitated waves travelling rostrally in the rostral part of the body, whereas the caudal part -as in the lamprey -favored downward waves. From both modeling studies and in vitro experiments, it is known that the propagation of activity along the spinal cord in the lamprey can be reversed by manipulating the excitatory gradients (Ekeberg 1993;Grillner et al 1993). Similarly, as shown in Fig.…”

Section: Simulation Of Swimmingmentioning

confidence: 95%

“…On the other hand, EMG data indicate that both swimming and walking patterns of epaxial muscle activity in the newt are different from the swimming pattern in lamprey . Whereas the latter consists of a single wave of activity propagating continuously down the body (Grillner et al 1993), the swimming pattern in the newt is characterized by two discontinuities in the rostrocaudal propagation of activity, occurring near the limb girdles. During walking, the girdle regions exhibit two distinct bursts of activity per step cycle, whereas other parts of the trunk express a single burst.…”

Section: Aquatic and Terrestrial Locomotionmentioning

confidence: 99%

From swimming to walking: a single basic network for two different behaviors

Bem

Cabelguen

Ekeberg

et al. 2003

Biological Cybernetics

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In this paper we consider the hypothesis that the spinal locomotor network controlling trunk movements has remained essentially unchanged during the evolutionary transition from aquatic to terrestrial locomotion. The wider repertoire of axial motor patterns expressed by amphibians would then be explained by the influence from separate limb pattern generators, added during this evolution. This study is based on EMG data recorded in vivo from epaxial musculature in the newt Pleurodeles waltl during unrestrained swimming and walking, and on a simplified model of the lamprey spinal pattern generator for swimming. Using computer simulations, we have examined the output generated by the lamprey model network for different input drives. Two distinct inputs were identified which reproduced the main features of the swimming and walking motor patterns in the newt. The swimming pattern is generated when the network receives tonic excitation with local intensity gradients near the neck and girdle regions. To produce the walking pattern, the network must receive (in addition to a tonic excitation at the girdles) a phasic drive which is out of phase in the neck and tail regions in relation to the middle part of the body. To fit the symmetry of the walking pattern, however, the intersegmental connectivity of the network had to be modified by reversing the direction of the crossed inhibitory pathways in the rostral part of the spinal cord. This study suggests that the input drive required for the generation of the distinct walking pattern could, at least partly, be attributed to mechanosensory feedback received by the network directly from the intraspinal stretch-receptor system. Indeed, the input drive required resembles the pattern of activity of stretch receptors sensing the lateral bending of the trunk, as expressed during walking in urodeles. Moreover, our results indicate that a nonuniform distribution of these stretch receptors along the trunk can explain the discontinuities exhibited in the swimming pattern of the newt. Thus, separate limb pattern generators can influence the original network controlling axial movements not only through a direct coupling at the central level but also via a mechanical coupling between trunk and limbs, which in turn influences the sensory signals sent back to the network. Taken together, our findings support the hypothesis of a phylogenetic conservatism of the spinal locomotor networks generating axial motor patterns from agnathans to amphibians.

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“…From experiments like those described here, Cohen (1987a,b) has reported differences in the responses of anterior and posterior segments of the lamprey cord to uniform exposure to glutamate analogs, and differences in their responses to bath-applied serotonin. Although individual preparations were reported to maintain stable differences in the frequencies of anterior and posterior segments, these data showed a wide scatter and have been interpreted to show both the presence and absence of segmental gradients of excitability (Williams et al, 1990;Grillner et al, 1993;Sigvardt, 1993). In newly hatched tadpoles (stage 37/38), Tunstall and Roberts (1994) demonstrated segmental differences in the strength of tonic excitation during swimming and similar differences in the strengths of postsynaptic potentials from local interneurons.…”

Section: Gradients Of Excitability or Excitation In Other Motor Systemsmentioning

confidence: 99%

A Test of the Excitability-Gradient Hypothesis in the Swimmeret System of Crayfish

Mulloney

1997

J. Neurosci.

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The motor pattern that drives coordinated movements of swimmerets in different segments during forward swimming characteristically begins with a power-stroke by the most posterior limbs, followed progressively by power-strokes of each of the more anterior limbs. To explain this caudal-to-rostral progression, the hypothesis was proposed that the neurons that drive the most posterior swimmerets are more excitable than their more anterior counterparts, and so reach threshold first.To test this excitability-gradient hypothesis, I used carbachol to excite expression of the swimmeret motor pattern and used tetrodotoxin ( TTX), sucrose solutions, and cutting to block the flow of information between anterior and posterior segments. I showed that the swimmeret activity elicited by carbachol is like that produced when the swimmeret system is spontaneously active and that blocking an intersegmental connective uncoupled swimmeret activity on opposite sides of the block.When anterior and posterior segments were isolated from each other, the frequencies of the motor patterns expressed by anterior segments were not slower than those expressed by posterior segments exposed to the same concentrations of carbachol. This result was independent of the concentration of carbachol applied and of the number of segmental ganglia that remained connected. When TTX was used to block information flow, the motor patterns produced in segments anterior to the block were significantly faster than those from segments posterior to the block.These observations contradict the predictions of the excitability-gradient hypothesis and lead to the conclusion that the hypothesis is incorrect.

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The neurophysiological bases of undulatory locomotion in vertebrates

Cited by 30 publications

References 37 publications

Muscle activity in autotomized tails of a lizard (Gekko gecko): a naturally occurring spinal preparation

Muscle activity in autotomized tails of a lizard (Gekko gecko): a naturally occurring spinal preparation

From swimming to walking: a single basic network for two different behaviors

A Test of the Excitability-Gradient Hypothesis in the Swimmeret System of Crayfish

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