Sacrocaudal Afferents Induce Rhythmic Efferent Bursting in Isolated Spinal Cords of Neonatal Rats

Abstract

The ability of mammalian spinal cords to generate rhythmic motor behavior in nonlimb moving segments was examined in isolated spinal cords of neonatal rats. Stimulation of sacrocaudal afferents (SCA) induced alternating left-right bursts in lumbosacral efferents and in tail muscles. On each side of the tail, flexors, extensors, and abductors were coactive during each cycle of activity. This rhythm originated mainly in the sacrocaudal region because it persisted in sacrocaudal segments after surgical removal of the thoracolumbar cord. Sacrocaudal commissural pathways were sufficient to maintain the left-right alternation of lumbar efferent bursts, because their timing was unaltered after a complete thoracolumbar hemisection. The lumbar rhythm originated in part from sacrocaudal activity ascending in lateral and ventrolateral funiculi, because efferent bursts in rostral lumbar segments were nearly abolished on a particular side by lesions of the lateral quadrant of the cord at the L(4)-L(5) junction. Intracellular recordings from S(2)-S(3) motoneurons, obtained during the rhythm, revealed the presence of phasic oscillations of membrane potential superimposed on a tonic depolarization. Bursts of spikes occurred on the depolarizing phases of the oscillation. Between these bursts the membrane input conductance increased, and hyperpolarizing drive potentials were revealed. The inhibitory drive and the decreased input resistance coincided with contralateral efferent bursts, suggesting that crossed pathways controlled it. Our studies indicate that pattern generators are not restricted to limb-moving spinal segments and suggest that regional specializations of pattern-generating circuitry and their associated interneurons are responsible for the different motor patterns produced by the mammalian spinal cord.

Spastic Long-Lasting Reflexes in the Awake Rat After Sacral Spinal Cord Injury

“…5B). This EMG activity is reminiscent of the rhythmic activity evoked in the neonatal rat tail in vitro by afferent stimulation (Lev-Tov et al 2000). In Fig.…”

Characterization of Sacral Interneurons That Mediate Activation of Locomotor Pattern Generators by Sacrocaudal Afferent Input

“…The ability of input from load and joint receptors to retrain the locomotor CPGs and improve motor function in humans with SCI (Dietz et al, 1997;Dietz, 2009;Edgerton et al, 2006;2008;Wernig et al, 1998) raises questions about the functional organization of the mediating pathways and the possibility of other sensory modalities to reactivate the CPGs. Our finding that stimulation of nociceptive and nonnociceptive sacrocaudal afferents (SCAs) has an extraordinary capacity to activate the CPGs in isolated spinal cords of neonatal rats (Lev-Tov et al, 2000;Strauss and Lev-Tov, 2003;Blivis et al, 2007; also see Klein and Tresch, 2010;for rat;and Mandadi and Whelan, 2009; for mouse) provided us not only with an additional potent means for activating the CPGs, but also with an experimentally accessible model to study the neuronal circuitry linking the SCA and CPGs and their mechanism of action. Using this model, we showed that activation of the CPGs by SCA stimulation required glutamatergic synaptic excitation (Strauss and Lev-Tov, 2003) of heterogeneous groups of sacral neurons with crossed and uncrossed ascending projections through the ventral (VF) and lateral white matter funiculi (Etlin et al, 2010;Lev-Tov et al, 2010).…”

“…Spinal cords (T6-Co3) were isolated from P1-P3 isoflurane-anesthetized male or female rats (Lev-Tov and Delvolvé, 2000;Lev-Tov et al, 2000;Delvolvé et al, 2001;Blivis et al, 2007). Preparations were transferred to a recording chamber and superfused continuously with an oxygenated artificial CSF (Kremer and Lev-Tov, 1997;Lev-Tov et al, 2000;Delvolvé et al, 2001;Blivis et al, 2007).…”

“…Unlike the thoracolumbar network, the reciprocal inhibition between flexor and extensor motoneurons in the sacrocaudal network is suppressed during the rhythm, and the two sacral hemicords define hypothetical half centers producing the alternating left-right excitation and crossed-inhibition responsible for the alternating rhythmic output (Lev-Tov and Delvolvé, 2000;Delvolvé et al, 2001). Therefore, it is tempting to suggest that the rhythmic VF neurons with contralateral phase preference may be linked to phasic excitation and those with ipsilateral phase preference are involved in activation of phasic inhibitory drive.…”

Interaction Between Developing Spinal Locomotor Networks in the Neonatal Mouse

“…Previous work has shown that cauda equina stimulation can effectively activate thoracosacral CPGs (Lev-Tov et al 2000;Whelan et al 2000). Because it offers a complementary method to activate thoracosacral CPGs, we examined whether afferent stimulation could evoke coordinated bursting from cervical segments.…”