Segmental Oscillators in Axial Motor Circuits of the Salamander: Distribution and Bursting Mechanisms

Abstract

The rhythmic and coordinated activation of axial muscles that underlie trunk movements during locomotion are generated by specialized networks in the spinal cord. The operation of these networks has been extensively investigated in limbless swimming vertebrates. But little is known about the architecture and functioning of the axial locomotor networks in limbed vertebrates. We investigated the rhythm-generating capacity of the axial segmental networks in the salamander (Pleurodeles waltlii). We recorded ventral root activity from hemisegments and segments that were surgically isolated from the mid-trunk cord and chemically activated with bath-applied N-methyl-d-aspartate (NMDA). We provide evidence that the rhythmogenic capacity of the axial network is distributed along the mid-trunk spinal cord without an excitability gradient. We demonstrate that the burst generation in a hemisegment depends on glutamatergic excitatory interactions. Reciprocal glycinergic inhibition between opposite hemisegments ensures left-right alternation and lowers the rhythm frequency in segments. Our results further suggest that persistent sodium current contributes to the rhythmic regenerating process both in hemisegments and segments. Burst termination in hemisegments is not achieved through the activation of apamine-sensitive Ca(2+)-activated K(+) channels and burst termination in segments relies on crossed glycinergic inhibition. Together our results indicate that the basic design of the salamander axial network is similar to most of axial networks investigated in other vertebrates, albeit with some significant differences in the cellular mechanism that underlies segmental bursting. This finding supports the view of a phylogenetic conservation of basic building blocks of the axial locomotor network among the vertebrates.

Sensory feedback plays a significant role in generating walking gait and in gait transition in salamanders: a simulation study

“…Salamanders swim with a lamprey-like undulatory pattern (anguilliform swimming) with the limbs held back to the body (Frolich and Biewener, 1992; Delvolve et al, 1997). Although, there are some significant differences in the cellular mechanism that underlie segmental bursting (Ryczko et al, 2010a), for simplicity, we use the same basic structure of the lamprey spinal locomotor network for generating axial motor patterns for the salamander (Cangiano and Grillner, 2005; Ryczko et al, 2010b). The only difference is that the salamanders have 40 anatomical segments instead of 100 segments of the lamprey.…”

Interfacing a salamander brain with a salamander-like robot: Control of speed and direction with calcium signals from brainstem reticulospinal neurons

“…To this end we used the salamander as an animal model, where the brainstem networks are easily accessible experimentally. In salamanders as in other vertebrates, the basic muscle contractions are programmed by a specialized neural network in the spinal cord called the Central Pattern Generator (CPG, see [25]), which controls axial and limb movements [26], [27], [28], [29]. This network integrates sensory signal and is under the control of brainstem locomotor networks.…”

Rhythmic Bursting in the Pre-Bötzinger Complex

“…In the classical model of an I NaP -dependent bursting neuron proposed by Butera et al (1999a, Model 1), burst termination was based on the slow inactivation of the persistent sodium channels themselves. The other proposed burst-terminating mechanisms were based on the slowly activating, voltage-dependent (e.g., Butera et al, 1999a, Model 2) or calcium-dependent (e.g., El Manira et al, 1994; Ryczko et al, 2010) potassium currents. In our previous (Jasinski et al, 2013) and present studies, we have suggested and investigated the possible involvement of a mechanism based on the activity-dependent accumulation of sodium ions within the cell ([Na + ] in ), and subsequent activation of the electrogenic Na + /K + pump ( I Pump ) removing the intracellularly accumulated sodium ions.…”

“…Several proposals have been made concerning other potential burst-terminating mechanisms, including mechanisms based on (a) slowly activating voltage-dependent potassium current (e.g., Butera et al, 1999a, Model 2) or Ca 2+ -activated potassium current (suggesting [Ca 2+ ] in accumulation during bursts via high voltage-activated calcium currents, e.g., Bevan and Wilson, 1999; El Manira et al, 1994; Ryczko et al, 2010), (b) Na + -activated potassium currents (e.g., Krey et al, 2010; Wallen et al, 2007; Yuan et al, 2003), and (c) activation of the Na + /K + electrogenic pump (e.g., Ballerini et al, 1997; Darbon et al, 2003; Del Negro et al, 2009; Krey et al, 2010). The two latter mechanisms suggest an important role of [Na + ] in accumulation during bursts.…”