Abstract
The neuronal generation of vertebrate locomotion has been extensively studied in the lamprey. Models at different levels of abstraction are being used to describe this system, from abstract nonlinear oscillators to interconnected model neurons comprising multiple compartments and a Hodgkin-Huxley representation of the most relevant ion channels. To study the role of sensory feedback by simulation, it eventually also becomes necessary to incorporate the mechanical movements in the models. By using simplifying models of muscle activation, body mechanics, counteracting water forces, and sensory feedback through stretch receptors and vestibular organs, we have been able to close the feedback loop to enable studies of the interaction between the neuronal and the mechanical systems. The neuromechanical simulations reveal that the currently known network is sufficient for generating a whole repertoire of swimming patterns. Swimming at different speeds and with different wavelengths, together with the performance of lateral turns can all be achieved by simply varying the brainstem input. The neuronal mechanisms behind pitch and roll manoeuvres are less clear. We have put forward a 'crossed-oscillators' hypothesis where partly separate dorsal and ventral circuits are postulated. Neuromechanical simulations of this system show that it is also capable of generating realistic pitch turns and rolls, and that vestibular signals can stabilize the posture during swimming.
Full Text
The Full Text of this article is available as a PDF (220.9 KB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Brodin L., Tråvén H. G., Lansner A., Wallén P., Ekeberg O., Grillner S. Computer simulations of N-methyl-D-aspartate receptor-induced membrane properties in a neuron model. J Neurophysiol. 1991 Aug;66(2):473–484. doi: 10.1152/jn.1991.66.2.473. [DOI] [PubMed] [Google Scholar]
- Buchanan J. T. Identification of interneurons with contralateral, caudal axons in the lamprey spinal cord: synaptic interactions and morphology. J Neurophysiol. 1982 May;47(5):961–975. doi: 10.1152/jn.1982.47.5.961. [DOI] [PubMed] [Google Scholar]
- Buchanan J. T. Neural network simulations of coupled locomotor oscillators in the lamprey spinal cord. Biol Cybern. 1992;66(4):367–374. doi: 10.1007/BF00203673. [DOI] [PubMed] [Google Scholar]
- Cohen A. H., Ermentrout G. B., Kiemel T., Kopell N., Sigvardt K. A., Williams T. L. Modelling of intersegmental coordination in the lamprey central pattern generator for locomotion. Trends Neurosci. 1992 Nov;15(11):434–438. doi: 10.1016/0166-2236(92)90006-t. [DOI] [PubMed] [Google Scholar]
- Cohen A. H., Holmes P. J., Rand R. H. The nature of the coupling between segmental oscillators of the lamprey spinal generator for locomotion: a mathematical model. J Math Biol. 1982;13(3):345–369. doi: 10.1007/BF00276069. [DOI] [PubMed] [Google Scholar]
- Deliagina T. G., Orlovsky G. N., Grillner S., Wallén P. Vestibular control of swimming in lamprey. II. Characteristics of spatial sensitivity of reticulospinal neurons. Exp Brain Res. 1992;90(3):489–498. doi: 10.1007/BF00230931. [DOI] [PubMed] [Google Scholar]
- Deliagina T. G., Orlovsky G. N., Grillner S., Wallén P. Vestibular control of swimming in lamprey. III. Activity of vestibular afferents: convergence of vestibular inputs on reticulospinal neurons. Exp Brain Res. 1992;90(3):499–507. doi: 10.1007/BF00230932. [DOI] [PubMed] [Google Scholar]
- Di Prisco G. V., Wallén P., Grillner S. Synaptic effects of intraspinal stretch receptor neurons mediating movement-related feedback during locomotion. Brain Res. 1990 Oct 15;530(1):161–166. doi: 10.1016/0006-8993(90)90675-2. [DOI] [PubMed] [Google Scholar]
- Ekeberg O., Wallén P., Lansner A., Tråvén H., Brodin L., Grillner S. A computer based model for realistic simulations of neural networks. I. The single neuron and synaptic interaction. Biol Cybern. 1991;65(2):81–90. doi: 10.1007/BF00202382. [DOI] [PubMed] [Google Scholar]
- Grillner S., Deliagina T., Ekeberg O, el Manira A., Hill R. H., Lansner A., Orlovsky G. N., Wallén P. Neural networks that co-ordinate locomotion and body orientation in lamprey. Trends Neurosci. 1995 Jun;18(6):270–279. [PubMed] [Google Scholar]
- Grillner S., McClellan A., Perret C. Entrainment of the spinal pattern generators for swimming by mechano-sensitive elements in the lamprey spinal cord in vitro. Brain Res. 1981 Aug 3;217(2):380–386. doi: 10.1016/0006-8993(81)90015-9. [DOI] [PubMed] [Google Scholar]
- Grillner S., McClellan A., Sigvardt K., Wallén P., Wilén M. Activation of NMDA-receptors elicits "fictive locomotion" in lamprey spinal cord in vitro. Acta Physiol Scand. 1981 Dec;113(4):549–551. doi: 10.1111/j.1748-1716.1981.tb06937.x. [DOI] [PubMed] [Google Scholar]
- Hellgren J., Grillner S., Lansner A. Computer simulation of the segmental neural network generating locomotion in lamprey by using populations of network interneurons. Biol Cybern. 1992;68(1):1–13. doi: 10.1007/BF00203132. [DOI] [PubMed] [Google Scholar]
- Matsushima T., Grillner S. Neural mechanisms of intersegmental coordination in lamprey: local excitability changes modify the phase coupling along the spinal cord. J Neurophysiol. 1992 Feb;67(2):373–388. doi: 10.1152/jn.1992.67.2.373. [DOI] [PubMed] [Google Scholar]
- Ohta Y., Dubuc R., Grillner S. A new population of neurons with crossed axons in the lamprey spinal cord. Brain Res. 1991 Nov 8;564(1):143–148. doi: 10.1016/0006-8993(91)91364-7. [DOI] [PubMed] [Google Scholar]
- Orlovsky G. N., Deliagina T. G., Wallén P. Vestibular control of swimming in lamprey. I. Responses of reticulospinal neurons to roll and pitch. Exp Brain Res. 1992;90(3):479–488. doi: 10.1007/BF00230930. [DOI] [PubMed] [Google Scholar]
- Tegnér J., Hellgren-Kotaleski J., Lansner A., Grillner S. Low-voltage-activated calcium channels in the lamprey locomotor network: simulation and experiment. J Neurophysiol. 1997 Apr;77(4):1795–1812. doi: 10.1152/jn.1997.77.4.1795. [DOI] [PubMed] [Google Scholar]
- Tråvén H. G., Brodin L., Lansner A., Ekeberg O., Wallén P., Grillner S. Computer simulations of NMDA and non-NMDA receptor-mediated synaptic drive: sensory and supraspinal modulation of neurons and small networks. J Neurophysiol. 1993 Aug;70(2):695–709. doi: 10.1152/jn.1993.70.2.695. [DOI] [PubMed] [Google Scholar]
- UllÉN F, Deliagina T, Orlovsky G, Grillner S. Spatial orientation in the lamprey. I. Control of pitch and roll. J Exp Biol. 1995;198(Pt 3):665–673. doi: 10.1242/jeb.198.3.665. [DOI] [PubMed] [Google Scholar]
- Ullström M., Kotaleski J. H., Tegnér J., Aurell E., Grillner S., Lansner A. Activity-dependent modulation of adaptation produces a constant burst proportion in a model of the lamprey spinal locomotor generator. Biol Cybern. 1998 Jul;79(1):1–14. doi: 10.1007/s004220050453. [DOI] [PubMed] [Google Scholar]
- Wallén P., Ekeberg O., Lansner A., Brodin L., Tråvén H., Grillner S. A computer-based model for realistic simulations of neural networks. II. The segmental network generating locomotor rhythmicity in the lamprey. J Neurophysiol. 1992 Dec;68(6):1939–1950. doi: 10.1152/jn.1992.68.6.1939. [DOI] [PubMed] [Google Scholar]
- Wallén P., Grillner S., Feldman J. L., Bergelt S. Dorsal and ventral myotome motoneurons and their input during fictive locomotion in lamprey. J Neurosci. 1985 Mar;5(3):654–661. doi: 10.1523/JNEUROSCI.05-03-00654.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Williams T. L., Bowtell G., Carling J. C., Sigvardt K. A., Curtin N. A. Interactions between muscle activation, body curvature and the water in the swimming lamprey. Symp Soc Exp Biol. 1995;49:49–59. [PubMed] [Google Scholar]
- Williams T. L. Phase coupling by synaptic spread in chains of coupled neuronal oscillators. Science. 1992 Oct 23;258(5082):662–665. doi: 10.1126/science.1411575. [DOI] [PubMed] [Google Scholar]
- Williams T., BOWTELL G., CURTIN N. A. Predicting force generation by lamprey muscle during applied sinusoidal movement using a simple dynamic model. J Exp Biol. 1998 Mar;201(Pt 6):869–875. doi: 10.1242/jeb.201.6.869. [DOI] [PubMed] [Google Scholar]
- el Manira A., Tegnér J., Grillner S. Calcium-dependent potassium channels play a critical role for burst termination in the locomotor network in lamprey. J Neurophysiol. 1994 Oct;72(4):1852–1861. doi: 10.1152/jn.1994.72.4.1852. [DOI] [PubMed] [Google Scholar]
