Flexibility of Motor Pattern Generation Across Stimulation Conditions by the Neonatal Rat Spinal Cord

Abstract

Klein DA, Patino A, Tresch MC. Flexibility of motor pattern generation across stimulation conditions by the neonatal rat spinal cord. J Neurophysiol 103: 1580 -1590, 2010. First published January 20, 2010 doi:10.1152/jn.00961.2009. Previous studies have demonstrated that "locomotor-like" rhythmic patterns can be evoked in the isolated neonatal rat spinal cord by several means, including pharmacological neuromodulation and electrical stimulation of various pathways. Recent studies have used stimulation of afferent pathways to evoke rhythmic patterns, relying on synaptic activation of interneuronal systems rather than global imposition of neuromodulatory state by pharmacological agents. We use the in vitro neonatal rat spinal cord with attached hindlimb to examine the muscle activation patterns evoked by stimulation of these different pathways and evaluate whether stimulation of these pathways all evoke the same patterns. We find that the patterns evoked by bath application of serotonin (5-HT) and N-methyl-D-aspartic acid (NMDA) consisted of alternation between hip flexors and extensors and similar alternation was observed in the patterns evoked by electrical stimulation of the cauda equina (CE) or contralateral fifth lumbar (L 5 ) dorsal nerve root. In contrast, the knee extensor/hip flexor rectus femoris (RF) and knee flexor/hip extensor semitendinosus (ST) were activated differentially across stimulation conditions. In 5-HT/NMDA patterns, RF was active in late flexion and ST in late extension. In CE patterns, these two muscles switched places with RF typically active in late extension and ST active in flexion. In L 5 patterns, ST was activated in extension and RF was silent or weakly active during flexion. There were also systematic differences in the consistency of rhythms evoked by each stimulation method: patterns evoked by electrical stimulation of CE or L 5 were less consistently modulated with the rhythm when compared with 5-HT/NMDA-evoked patterns. All differences were preserved following deafferentation, demonstrating that they reflect intrinsic properties of spinal systems. These results highlight the intrinsic flexibility of motor pattern generation by spinal motor circuitry which is present from birth and provides important information to many studies examining spinal pattern generating networks.

Spatiotemporal Dynamics of Rhythmic Spinal Interneurons Measured With Two-Photon Calcium Imaging and Coherence Analysis

“…It is known that the hindlimb locomotor circuit can be modulated to generate multiple motor patterns (Grillner 2003) so neurotransmitter application, as an artificial means of exciting virtually all spinal neurons to elicit the motor rhythm, may simultaneously activate neurons that are normally used for different motor tasks. Avoiding this conundrum would require more detailed comparisons between locomotor activity in vivo and the different methods for eliciting fictive locomotion in vitro Klein et al 2010).…”

The Generation of Antiphase Oscillations and Synchrony by a Rebound-Based Vertebrate Central Pattern Generator

“…Much less is known about circuit architecture in vertebrates. It is widely thought that polymorphic neural networks can mediate multiple motor outputs (Getting, 1989;Soffe, 1993;Marder and Calabrese, 1996;Marder et al, 2005;Briggman and Kristan, 2008;Doi and Ramirez, 2008;Rauscent et al, 2009;Klein et al, 2010). However, a number of recent nonmammalian vertebrate studies suggest that circuit reconfiguration is needed to generate different motor responses (Ritter et al, 2001;Kimura et al, 2006;Berkowitz, 2007Berkowitz, , 2008Li et al, 2007;McLean et al, 2007McLean et al, , 2008Liao and Fetcho, 2008;Frigon, 2009;Satou et al, 2009;Wyart et al, 2009;Berkowitz et al, 2010).…”

Specificity of Intramuscular Activation During Rhythms Produced by Spinal Patterning Systems in the In Vitro Neonatal Rat With Hindlimb Attached Preparation

“…This capability is intrinsic to spinal cord circuitry immediately at birth (Cazalets et al 1992;Kiehn 2006;Kudo and Yamada 1987;Smith and Feldman 1987;Smith et al 1988;Sqalli-Houssaini et al 1993;Whelan 2003) and, although the motor patterns are often considered to consist of a simple alternation between flexion and extension, it is clear that muscle activations even in the neonate can be more complex (Grillner 1981;Hayes 2009;Kiehn and Kjaerulff 1996;Klein et al 2010;Rossignol 1996). Muscles can be active across the boundaries between flexion and extension phases or for only a fraction of a phase in the rhythms produced by the isolated neonatal spinal cord (Hayes et al 2009;Kiehn and Kjaerulff 1996;Klein et al 2010). Further, the activity of some muscles can shift, depending on the conditions within which the rhythms are produced (Hayes et al 2009;Kiehn and Kjaerulff 1996;Klein et al 2010).…”

“…Muscles can be active across the boundaries between flexion and extension phases or for only a fraction of a phase in the rhythms produced by the isolated neonatal spinal cord (Hayes et al 2009;Kiehn and Kjaerulff 1996;Klein et al 2010). Further, the activity of some muscles can shift, depending on the conditions within which the rhythms are produced (Hayes et al 2009;Kiehn and Kjaerulff 1996;Klein et al 2010). For instance, we have shown in the in vitro neonatal rat that "bifunctional" muscles, such as semitendinosus (ST) and rectus femoris (RF), switch between flexor-and extensor-related activity in the rhythms evoked by application of serotonin (5-HT) and N-methyl-Daspartate (NMDA) compared with cauda equina (CE) stimulation (Klein et al 2010).…”

“…Specificity of intramuscular activation during rhythms produced by spinal patterning systems in the in vitro neonatal rat with hindlimb attached preparation. J Neurophysiol 104: 2158 -2168, 2010. First published July 21, 2010 doi:10.1152/jn.00477.2010.…”