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. 2010 May 19;30(20):7061-71.
doi: 10.1523/JNEUROSCI.0450-10.2010.

Evidence for specialized rhythm-generating mechanisms in the adult mammalian spinal cord

Affiliations

Evidence for specialized rhythm-generating mechanisms in the adult mammalian spinal cord

Alain Frigon et al. J Neurosci. .

Abstract

Locomotion and scratch are characterized by alternation of flexion and extension phases within one hindlimb, which are mediated by rhythm-generating circuitry within the spinal cord. By definition, the rhythm generator controls cycle period, phase durations, and phase transitions. The aim was to determine whether rhythm-generating mechanisms for locomotion and scratch are similar in adult decerebrate cats. The regulation of cycle period during fictive scratching was evaluated, as were the effects of specific sensory inputs on phase durations and transitions during spontaneous fictive locomotion and pinna-evoked fictive scratching. Results show that cycle period during fictive scratching varied predominantly with flexion phase duration, contrary to spontaneous fictive locomotion, where cycle period varied with extension phase duration. Ankle dorsiflexion greatly increased extension phase duration and cycle period during fictive locomotion but did not alter cycle period during scratching. Moreover, stimulating the plantaris (ankle extensor muscle) nerve during flexion reset the locomotor rhythm to extension but not the scratch rhythm. Stimulating the plantaris nerve during extension prolonged the extension phase and cycle period during fictive locomotion but not during fictive scratching. Stimulating the sartorius nerve (hip flexor muscle) during early flexion reduced the flexion phase and cycle period during fictive locomotion, but considerably prolonged the flexion phase and cycle period during fictive scratching. These data indicate that cycle period, phase durations, and phase transitions are not regulated similarly during fictive locomotion and scratching, with or without sensory inputs, providing evidence for specialized rhythm-generating mechanisms within the adult mammalian spinal cord.

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Figures

Figure 1.
Figure 1.
Regulation of cycle period during a switch from spontaneous fictive locomotion to fictive scratching in the same cat. A, ENG from extensor (LGS) and flexor (TA) nerves during spontaneous fictive locomotion followed by pinna stimulation and fictive scratching in one cat. B, C, Measurements during fictive locomotion (B) and scratching (C). D, E, Scatter plots and regression lines for flexion (black circles), extension (gray diamonds), and flexion-interval (white triangles) phase durations expressed relative to the corresponding cycle period during spontaneous fictive locomotion (D) and pinna-evoked fictive scratching (E) for the episode illustrated in A. The dotted line has a slope of 0.5 and passes through the origin and is used as a reference line.
Figure 2.
Figure 2.
Phase/cycle period relationships during fictive scratching in the decerebrate cat. Left panels show ENG from extensor (MG) and flexor (TA) nerves during flexor-dominated (A) and non-flexor-dominated (B) fictive scratching episodes in 2 cats. Right panels show scatter plots and regression lines for flexion (black circles), extension (gray diamonds), and flexion-interval (white triangles) phase durations expressed relative to the corresponding cycle period. The dotted line has a slope of 0.5 and passes through the origin and is used as a reference line.
Figure 3.
Figure 3.
Parameters of the fictive scratching cycle during flexor-dominated and non-flexor-dominated episodes. A, Average duration of CPFLEX, and of the FLEX, EXT, and FLEX-INT phases. B, Mean slope of the flexion (rFLEX), extension (rEXT), and flexion-interval (rFLEX-INT) phase durations/cycle period regressions. C, Percentage of flexion, extension, and flexion-interval phase duration as a function of cycle period. Each bar is the mean ± SE of 20 flexor-dominated and 8 non-flexor-dominated scratching episodes. *p < 0.05, **p < 0.01, ***p < 0.01.
Figure 4.
Figure 4.
Effects of ankle dorsiflexion during spontaneous fictive locomotion and fictive scratching. The left panels show ENG from extensor (SmAB and MG during fictive locomotion and PBSt and MG during fictive scratching) and flexor (TA and EDL) nerves during extensor-dominated (A) and flexor-dominated (B) locomotor episodes in 2 cats, and during 2 flexor-dominated (C, D) scratching episodes in 2 cats. Right panels show scatter plots and regression lines for extension (gray) and flexion (black) phase durations relative to cycle period before (Ctrl) and during (DF) dorsiflexion. During fictive scratching, the flexion-phase interval (white) duration as a function of cycle period is also represented. The dotted line has a slope of 0.5 and passes through the origin and is used as a reference line.
Figure 5.
Figure 5.
Effects of ankle dorsiflexion during spontaneous fictive locomotion and fictive scratching for the group. A, B, Average duration of the CPFLEX, and of the FLEX, EXT, and FLEX-INT phases before (Ctrl) and during (DF) dorsiflexion. C, D, Mean slope of the flexion (rFLEX), extension (rEXT), and flexion-interval (rFLEX-INT) phase durations/cycle period regressions before and during dorsiflexion. Each bar is the mean ± SE of 20 flexor-dominated and 8 non-flexor-dominated scratching episodes. *p < 0.05, **p < 0.01, ***p < 0.01.
Figure 6.
Figure 6.
Effects of Pl or LGS nerve stimulation during fictive locomotion and scratching. A–D, Top panels show ENG from extensor (LGS or MG) and flexor (TA) nerves in 2 cats with short trains of electrical stimuli to the Pl nerve (25p at 1.8T, 200 Hz) during early flexion in fictive locomotion (A) and scratching (B) and during the late extension (C) or late flexion (D) interval epochs of fictive locomotion and scratching, respectively. The onset of the flexion phase and cycle period is indicated above the TA waveform. E, F, Average phase duration of the flexion phase F1 or F2 stimulation during EF, MF, LF, and EXT or FLEX-INT epochs, expressed relative to control flexion phase durations. The duration of the extension or flexion-interval phase (i.e., between F1 and F2) is also shown. Note that when the stimuli fall in EXT or FLEX-INT the extension or flexion-interval phase is the stimulated phase. G, H, Mean flexor cycle period CPstim and CPafter stimulation measured for the same epochs as in E, F. The number of data points used in each condition to calculate phase durations and cycle periods is indicated below the epoch of G, H. Each bar is the mean ± SE. Asterisks indicate significant differences with control cycles (paired t tests). *p < 0.05, **p < 0.01, ***p < 0.01.
Figure 7.
Figure 7.
Effects of Sart nerve stimulation during fictive locomotion and scratching. A–D, Top panels show ENG from extensor (LGS or MG) and flexor (TA) nerves in 2 cats with short trains of electrical stimuli to the Sart nerve (25p at 5T, 200 Hz) during early flexion in fictive locomotion (A) and scratching (B) and during the late extension (C) or late flexion (D) interval epochs of fictive locomotion and scratching, respectively. The onset of the flexion phase and cycle period is indicated above the TA waveform. E, F, Average phase duration of the flexion phase F1 or F2 stimulation during EF, MF, LF, and EXT or FLEX-INT epochs, expressed relative to control flexion phase durations. The duration of the extension or flexion-interval phase (i.e., between F1 and F2) is also shown. Note that when the stimuli fall in EXT or FLEX-INT the extension or flexion-interval phase is the stimulated phase. G, H, Mean flexor cycle period CPstim and CPafter stimulation measured for the same epochs as in E, F. The number of data points used in each condition to calculate phase durations and cycle periods is indicated below the epoch of G, H. Each bar is the mean ± SE. Asterisks indicate significant differences with control cycles (paired t tests). *p < 0.05, **p < 0.01, ***p < 0.01.

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