» Articles » PMID: 19703959

Defining the Excitatory Neurons That Drive the Locomotor Rhythm in a Simple Vertebrate: Insights into the Origin of Reticulospinal Control

Overview
Journal J Physiol
Specialty Physiology
Date 2009 Aug 26
PMID 19703959
Citations 45
Authors
Affiliations
Soon will be listed here.
Abstract

Important questions remain about the origin of the excitation that drives locomotion in vertebrates and the roles played by reticulospinal neurons. In young Xenopus tadpoles, paired whole-cell recordings reveal reticulospinal neurons that directly excite swimming circuit neurons in the brainstem and spinal cord. They form part of a column of neurons (dINs) with ipsilateral descending projections which fire reliably and rhythmically in time with swimming. We ask if, at this early stage of development, these reticulospinal neurons are themselves the primary source of rhythmic drive to spinal cord neurons on each cycle of swimming. Loose-patch recordings in the hindbrain and spinal cord from neurons active during fictive swimming distinguished dINs from other neurons by spike shape. These recordings showed that reticulospinal dINs in the caudal hindbrain (rhombomeres 7-8) fire significantly earlier on each swimming cycle than other, ipsilateral, swimming circuit neurons. Whole-cell recordings showed that fast EPSCs typically precede, and probably drive, spikes in most swimming circuit neurons. However, the earliest-firing reticulospinal dINs spike too soon to be driven by underlying fast EPSCs. We propose that rebound following reciprocal inhibition can contribute to early reticulospinal dIN firing during swimming and show rebound firing in dINs following evoked, reciprocal inhibitory PSPs. Our results define reticulospinal neurons that are the source of the primary, descending, rhythmic excitation that drives spinal cord neurons to fire during swimming. These neurons are an integral part of the rhythm generating circuitry. We discuss the origin of these reticulospinal neurons as specialised members of a longitudinally distributed population of excitatory interneurons extending from the brainstem into the spinal cord.

Citing Articles

Mechanisms Underlying the Recruitment of Inhibitory Interneurons in Fictive Swimming in Developing Tadpoles.

Ferrario A, Saccomanno V, Zhang H, Borisyuk R, Li W J Neurosci. 2023; 43(8):1387-1404.

PMID: 36693757 PMC: 9987577. DOI: 10.1523/JNEUROSCI.0520-22.2022.


An early midbrain sensorimotor pathway is involved in the timely initiation and direction of swimming in the hatchling tadpole.

Larbi M, Messa G, Jalal H, Koutsikou S Front Neural Circuits. 2023; 16:1027831.

PMID: 36619662 PMC: 9810627. DOI: 10.3389/fncir.2022.1027831.


From decision to action: Detailed modelling of frog tadpoles reveals neuronal mechanisms of decision-making and reproduces unpredictable swimming movements in response to sensory signals.

Ferrario A, Palyanov A, Koutsikou S, Li W, Soffe S, Roberts A PLoS Comput Biol. 2021; 17(12):e1009654.

PMID: 34898604 PMC: 8699619. DOI: 10.1371/journal.pcbi.1009654.


The early development and physiology of tadpole lateral line system.

Saccomanno V, Love H, Sylvester A, Li W J Neurophysiol. 2021; 126(5):1814-1830.

PMID: 34705593 PMC: 8794055. DOI: 10.1152/jn.00618.2020.


Hindbrain V2a Neurons Pattern Rhythmic Activity of Motor Neurons in a Reticulospinal Coculture.

Bubnys A, Kandel H, Kao L, Pfaff D, Tabansky I Front Neurosci. 2019; 13:1077.

PMID: 31680817 PMC: 6811747. DOI: 10.3389/fnins.2019.01077.


References
1.
Soffe S . Roles of Glycinergic Inhibition and N-Methyl-D-Aspartate Receptor Mediated Excitation in the Locomotor Rhythmicity of One Half of the Xenopus Embryo Central Nervous System. Eur J Neurosci. 1989; 1(6):561-571. DOI: 10.1111/j.1460-9568.1989.tb00363.x. View

2.
Tunstall M, Roberts A . Longitudinal coordination of motor output during swimming in Xenopus embryos. Proc Biol Sci. 1991; 244(1309):27-32. DOI: 10.1098/rspb.1991.0046. View

3.
Barry M, ODonovan M . The effects of excitatory amino acids and their antagonists on the generation of motor activity in the isolated chick spinal cord. Brain Res. 1987; 433(2):271-6. DOI: 10.1016/0165-3806(87)90030-7. View

4.
van Mier P, Ten Donkelaar H . Structural and functional properties of reticulospinal neurons in the early-swimming stage Xenopus embryo. J Neurosci. 1989; 9(1):25-37. PMC: 6569989. View

5.
Buchanan J, Cohen A . Activities of identified interneurons, motoneurons, and muscle fibers during fictive swimming in the lamprey and effects of reticulospinal and dorsal cell stimulation. J Neurophysiol. 1982; 47(5):948-60. DOI: 10.1152/jn.1982.47.5.948. View