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

Abstract

Does the spinal cord use a single network to generate locomotor and scratching rhythms or two separate networks? Previous research showed that simultaneous swim and scratch stimulation (“dual stimulation”) in immobilized, spinal turtles evokes a single rhythm in hindlimb motor nerves with a frequency often greater than during swim stimulation alone or scratch stimulation alone. This suggests that the signals that trigger swimming and scratching converge and are integrated within the spinal cord. However, these results could not determine whether the integration occurs in motoneurons themselves or earlier, in spinal interneurons. Here, we recorded intracellularly from hindlimb motoneurons during dual stimulation. Motoneuron membrane potentials displayed regular oscillations at a higher frequency during dual stimulation than during swim or scratch stimulation alone. In contrast, arithmetic addition of the oscillations during swimming alone and scratching alone with various delays always generated irregular oscillations. Also, the standard deviation of the phase-normalized membrane potential during dual stimulation was similar to those during swimming or scratching alone. In contrast, the standard deviation was greater when pooling cycles of swimming alone and scratching alone for two of the three forms of scratching. This shows that dual stimulation generates a single rhythm prior to motoneurons. Thus, either swimming and scratching largely share a rhythm generator or the two rhythms are integrated into one rhythm by strong interactions among interneurons.

Neurotransmitters and Motoneuron Contacts of Multifunctional and Behaviorally Specialized Turtle Spinal Cord Interneurons

“…12). That many multifunctional interneurons directly contact motoneurons is consistent with our recent finding that the scratching and swimming CPGs largely converge before motoneurons (Hao and Berkowitz, 2017).…”

“…Multifunctional interneurons, including T neurons, that are rhythmically activated during swimming and scratching are good candidates to contribute to central pattern generation for multiple types of rhythmic motor patterns. Previous evidence suggested that the spinal CPG networks for swimming and all three forms of scratching are largely shared (Berkowitz and Stein, 1994b;Berkowitz, 2001bBerkowitz, , 2002Berkowitz, , 2008Hao et al, 2011;Hao and Berkowitz, 2017). Combined with the current findings, it seems likely that these CPG networks include both excitatory and inhibitory interneurons.…”

“…Three of the scratch-specialized interneurons successfully tested in this study were excitatory and one was inhibitory. Together, these findings suggest that some scratch-specialized interneurons may directly excite motoneurons that are more strongly activated during scratching than swimming, such as ipsilateral hip-flexor motoneurons (or contralateral hip-extensor motoneurons), whereas others may directly inhibit motoneurons that are less strongly activated during scratching than swimming, such as ipsilateral hip-extensor motoneurons (or contralateral hip-flexor motoneurons; Juranek and Currie, 2000;Berkowitz, 2002Berkowitz, , 2008Hao et al, 2011;Hao and Berkowitz, 2017). If ipsilateral hip-flexor motoneurons receive excitation from both multifunctional and scratch-specialized interneurons during scratching, but only from multifunctional interneurons during swimming, this could explain why ipsilateral hip-flexor motoneurons are more strongly activated during scratching than swimming (Fig.…”

“…We found two behaviorally specialized hindlimb-enlargement motoneurons, one scratch-specialized and the other flexion reflex-selective. This was surprising because motor nerves and muscles studied to date are all activated during all three forms of turtle scratching and swimming (Lennard and Stein, 1977;Robertson et al, 1985;Juranek and Currie, 2000;Berkowitz, 2002Berkowitz, , 2008Hao et al, 2011;Hao and Berkowitz, 2017); hip-flexor and, to a lesser extent, hip-extensor motor nerves are also activated during flexion reflex (Stein et al, 1982;Currie and Lee, 1996). The general assumption has been that all hindlimb muscles contribute to all hindlimb behaviors.…”

Feedforward discharges couple the singing central pattern generator and ventilation central pattern generator in the cricket abdominal central nervous system

“…In all animals the timing of rhythmic muscle activity during simultaneous repetitive motor behaviors is well coordinated (von Holst 1935, 1943; Kutsch 1969; Syed and Winlow 1991; Dick et al 1993; Chrachri and Neil 1993; Ramirez 1998; Boggs 2002; Moore et al 2014; Stein 2018). The coupling between the motor cycles can range from strict synchrony in absolute coordination to periodic phase coupling as in relative coordination (von Holst 1935; Berger et al 1970; Bramble and Carrier 1983; Kawahara et al 1989; Paripovic et al 1996; Moore et al 2014; Hao and Berkowitz 2017). Repetitive motor activity is generally produced by central pattern generators (CPGs), networks of interneurons within the central nervous system that generate rhythmic activity, even in the absence of sensory feedback (Delcomyn 1980; Marder and Bucher 2001; Mulloney and Smarandache 2010; Selverston 2010).…”