Rostral spinal cord segments are sufficient to generate a rhythm for both locomotion and scratching but affect their hip extensor phases differently

Abstract

Rostral segments of the spinal cord hindlimb enlargement are more important than caudal segments for generating locomotion and scratching rhythms in limbed vertebrates, but the adequacy of rostral segments has not been directly compared between locomotion and scratching. We separated caudal segments from immobilized low-spinal turtles by sequential spinal cord transections. After separation of the caudal four segments of the five-segment hindlimb enlargement, the remaining enlargement segment and five preenlargement segments still produced rhythms for forward swimming and both rostral and pocket scratching. The swimming rhythm frequency was usually maintained. Some animals continued to generate swimming and scratching rhythms even with no enlargement segments remaining, using only preenlargement segments. The preenlargement segments and rostral-most enlargement segment were also sufficient to maintain hip flexor (HF) motoneuron quiescence between HF bursts [which normally occurs during each hip extensor (HE) phase] during swimming. In contrast, the HF-quiescent phase was increasingly absent (i.e., HE-phase deletions) during rostral and pocket scratching. Moreover, respiratory motoneurons that normally burst during HE bursts continued to burst during the HF quiescence of swimming even with the caudal segments separated. Thus the same segments are sufficient to generate the basic rhythms for both locomotion and scratching. These segments are also sufficient to produce a reliable HE phase during locomotion but not during rostral or pocket scratching. We hypothesize that the rostral HE-phase interneurons that rhythmically inhibit HF motoneurons and interneurons are sufficient to generate HF quiescence during HE-biased swimming but not during the more HF-biased rostral and pocket scratching.

Shared Components of Rhythm Generation for Locomotion and Scratching Exist Prior to Motoneurons

“…Collectively, these studies make it unlikely that the swimming and scratching pathways are completely separate prior to motoneurons. However, earlier studies also suggest that there are some differences between the spinal interneuronal networks for two rhythmic behaviors ( Ritter et al, 2001 ; Berkowitz, 2002 , 2008 ; Li et al, 2007 ; McLean et al, 2007 ; Liao and Fetcho, 2008 ; McLean and Fetcho, 2008 ; Satou et al, 2009 ; Frigon and Gossard, 2010 ; Mui et al, 2012 ; Hao et al, 2014 ). Combining these findings with the current findings, one can conclude that to the extent that there are swim and/or scratch-specialized spinal interneurons that contribute to rhythm and/or pattern generation, they appear to have their effects predominately or exclusively on interneurons, not motoneurons.…”

“…The swim stimulation amplitude and frequency were usually adjusted to evoke a swimming motor pattern with a cycle frequency that differed from the scratching cycle frequencies. Rostral, pocket, and caudal scratching motor patterns were evoked by continual gentle rubbing of a single site in the receptive field of each scratch form at ∼3 N, ∼3–4 Hz, using a glass probe with a fire-polished tip ( Mortin et al, 1985 ; Hao et al, 2014 ). “Swim/scratch dual stimulation” refers to the combination of swim and scratch stimulation delivered at overlapping times.…”

Lognormal firing rate distribution reveals prominent fluctuation–driven regime in spinal motor networks

“…To avoid the confounding factors of supraspinal input, we spinalized the turtle. The transection was performed at the spinal cord at segments (D3-4) caudal to the cervical segments, where the local circuitry has only little or no involvement in generation of motor patterns (Mortin and Stein, 1989; Hao et al, 2014; Mui et al, 2012). The adult turtle preparation is capable of producing elaborate motor patterns such as scratching.…”

Lognormal firing rate distribution reveals prominent fluctuation-driven regime in spinal motor networks

“…To avoid the confounding factors of supraspinal input, we spinalized the turtle. The transection was performed at the spinal cord at segments (D3-4) caudal to the cervical segments, where the local circuitry has only little or no involvement in generation of motor patterns [Hao et al, 2014;Mortin and Stein, 1989;Mui et al, 2012]. The adult turtle preparation is capable of producing elaborate motor patterns such as scratching.…”