Single-cell and ensemble activity of lumbar intermediate and ventral horn interneurons in the spinal air-stepping cat

Abstract

We explored the relationship between population interneuronal network activation and motor output in the adult, in-vivo, air stepping, spinal cat. By simultaneously measuring the activity of large numbers of spinal interneurons, we explored ensembles of coherently firing interneurons and their relation to motor output. Additionally, the networks were analyzed in relation to their spatial distribution along the lumbar enlargement for evidence of localized groups driving particular phases of the locomotor step cycle. We simultaneously recorded hindlimb EMG activity during stepping and extracellular signals from 128 channels across two polytrodes inserted within lamina V-VII of two separate lumbar segments. Results indicated that spinal interneurons participate in one of two ensembles that are highly correlated with the flexor or the extensor muscle bursts during stepping. Interestingly, less than half of the isolated single units were significantly unimodally tuned during the step cycle while >97% of the single units of the ensembles were significantly correlated with muscle activity. These results show the importance of population scale analysis in neural studies of behavior as there is a much greater correlation between muscle activity and ensemble firing than between muscle activity and individual neurons. Finally, we show that there is no correlation between interneurons' rostrocaudal locations within the lumbar enlargement and their preferred phase of firing or ensemble participation. These findings indicate that spinal interneurons of lamina V-VII encoding for different phases of the locomotor cycle are spread throughout the lumbar enlargement in the adult spinal cord.

Lumbar multiunit activity power spectrum during air stepping in the spinal cat: evidence for a flexor-dominated rostrocaudally distributed locomotor center

“…The dorsoventral recording depth spanned from 1,560 ± 217 μm to 2,960 ± 217 μm. Single-unit activity results for those animals are reported in McMahon et al ( 41 ).…”

“…First, a T11/T12 spinal transection was performed 22–23 days before the recording session to potentiate the air stepping induced by clonidine administration during the terminal procedure ( 41 ). Spinal transection and postprocedure care followed the laboratory standard procedures ( 41 , 42 ). No locomotor training was provided to the animals at any point.…”

“…Consistent with other multiunit recording experiments in our laboratory ( 35 , 36 , 41 ), animals were initially injected with atropine (0.05 mg/kg, IM) and anesthetized with isoflurane (1.5–3.5% in oxygen) supplied through an endotracheal tube. Heart rate, blood pressure, end-tidal CO 2 , tidal volume, arterial oxyhemoglobin saturation, respiration rate, and temperature were monitored and recorded every 15 min.…”

“…Five criteria ( 35 , 36 ) were used to test the quality of the stepping in terms of both left-right limb alternation and flexor-extensor alternation. Details of the methods and results about the quality of stepping can be found in McMahon et al ( 41 ).…”

Toward Assessing the Functional Connectivity of Spinal Neurons

“…This work has been done in several species during a relatively small range of behaviors. Most of these have focused on quantifying interneuronal activity during endogenous behaviors, such as locomotion in the cat ( AuYong et al, 2011a , b ; Dominguez-Rodriguez et al, 2020 ; Musienko et al, 2020 ; McMahon et al, 2021 ), scratching in the turtle ( Radosevic et al, 2019 ), or under anesthesia in the rat ( McPherson and Bandres, 2021 ). While such behaviors are critical to understand input-output properties within and between interneurons and motoneurons, these relationships are difficult to extract in an intrinsically oscillating circuit.…”