Slowly-Conducting Pyramidal Tract Neurons in Macaque and Rat

Kraskov, Alexander; Soteropoulos, Demetris S.; Glover, Isabel S; Lemon, Roger; Baker, Stuart N.

doi:10.1093/cercor/bhz318

Cited by 12 publications

(16 citation statements)

References 52 publications

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“…10 , bottom). It is well known that extracellular recordings have a bias toward large cells with faster-conducting axons ( Humphrey and Corrie, 1978 ; Kraskov et al, 2019 , 2020 ). An even more extreme bias is likely for intracellular records, as penetrations into small cells are usually rapidly lost because of mechanical instability.…”

Section: Discussionmentioning

confidence: 99%

Extensive Cortical Convergence to Primate Reticulospinal Pathways

et al. 2020

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Early evolution of the motor cortex included development of connections to brainstem reticulospinal neurons; these projections persist in primates. In this study we examined the organisation of corticoreticular connections in five macaque monkeys (one male) using both intra-and extracellular recordings from reticular formation neurons, including identified reticulospinal cells. Synaptic responses to stimulation of different parts of primary motor cortex (M1) and supplementary motor area (SMA) bilaterally were assessed. Widespread short latency excitation, compatible with monosynaptic transmission over fast-conducting pathways, was observed, as well as longer latency responses likely reflecting a mixture of slower monosynaptic and oligosynaptic pathways. There was a high degree of convergence: 56% of reticulospinal cells with input from M1 received projections from M1 in both hemispheres; for SMA, the equivalent figure was even higher (70%). Of reticulospinal neurons with input from the cortex, 78% received projections from both M1 and SMA (irrespective of hemisphere); 83% of reticulospinal cells with input from M1 received projections from more than one of the tested M1 sites. This convergence at the single cell level allows reticulospinal neurons to integrate information from across the motor areas of the cortex, taking account of the bilateral motor context. Reticulospinal connections are known to strengthen following damage to the corticospinal tract, such as after stroke, partially contributing to functional recovery. Extensive corticoreticular convergence provides redundancy of control, which may allow the cortex to continue to exploit this descending pathway even after damage to one area. SIGNIFICANCE STATEMENT The reticulospinal tract provides a parallel pathway for motor control in primates, alongside the more sophisticated corticospinal system. We found extensive convergent inputs to primate reticulospinal cells from primary and supplementary motor cortex bilaterally. These redundant connections could maintain transmission of voluntary commands to the spinal cord after damage (e.g. after stroke or spinal cord injury), possibly assisting recovery of function.

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Section: Discussionmentioning

confidence: 99%

Extensive Cortical Convergence to Primate Reticulospinal Pathways

et al. 2020

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“…They are largely missing from the primate neurophysiological literature [ 14 ], most likely because their action potentials are small and difficult to record stably with conventional recording techniques. Newer methods have revealed that it is possible to identify them [ 15 ], and therefore possible to begin to study their function.…”

Section: The Wide Spectrum Of Primate Corticospinal Fibresmentioning

confidence: 99%

The Cortical “Upper Motoneuron” in Health and Disease

Lemon

2021

Brain Sciences

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Upper motoneurons (UMNs) in motor areas of the cerebral cortex influence spinal and cranial motor mechanisms through the corticospinal tract (CST) and through projections to brainstem motor pathways. The primate corticospinal system has a diverse cortical origin and a wide spectrum of fibre diameters, including large diameter fibres which are unique to humans and other large primates. Direct cortico-motoneuronal (CM) projections from the motor cortex to arm and hand motoneurons are a late evolutionary feature only present in dexterous primates and best developed in humans. CM projections are derived from a more restricted cortical territory (‘new’ M1, area 3a) and arise not only from corticospinal neurons with large, fast axons but also from those with relatively slow-conducting axons. During movement, corticospinal neurons are organised and recruited quite differently from ‘lower’ motoneurons. Accumulating evidence strongly implicates the corticospinal system in the early stages of ALS, with particular involvement of CM projections to distal limb muscles, but also to other muscle groups influenced by the CM system. There are important species differences in the organisation and function of the corticospinal system, and appropriate animal models are needed to understand disorders involving the human corticospinal system.

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“…These estimates should be considered conservative as they assume a monosynaptic connection; in reality, some effects from the corticospinal tract to SC cells will take a more indirect route which would require a larger compensation that the 1 ms synaptic delay which we allowed. Additionally, our dataset of PTN recordings is biased towards the fastest PTNs (Firmin et al 2014;Innocenti et al 2019;Kraskov et al 2018;Kraskov et al 2019). If M1 contributes to SC responses through the many PTNs which are even slower than those recorded here, then M1 contributions to SC responses would be even smaller than assessed here.…”

Section: Do Spinal Cells Respond Directly To the Perturbation Or Indmentioning

confidence: 77%

Long-latency Responses to a Mechanical Perturbation of the Index Finger Have a Spinal Component

Soteropoulos

Baker

2020

J. Neurosci.

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In an uncertain external environment, the motor system may need to respond rapidly to an unexpected stimulus. Limb displacement causes muscle stretch; the corrective response has multiple activity bursts, which are suggested to originate from different parts of the neuraxis. The earliest response is so fast, it can only be produced by spinal circuits; this is followed by slower components thought to arise from primary motor cortex (M1) and other supraspinal areas. Spinal cord (SC) contributions to the slower components are rarely considered. To address this, we recorded neural activity in M1 and the cervical SC during a visuomotor tracking task, in which two female macaque monkeys moved their index finger against a resisting motor to track an on-screen target. Following the behavioral trial, an increase in motor torque rapidly returned the finger to its starting position (lever velocity >200°/s). Many cells responded to this passive mechanical perturbation (M1: 148/211 cells, 70%; SC: 67/119 cells, 56%). The neural onset latency was faster for SC compared to M1 cells (21.7±11.2ms vs 25.5±10.7ms respectively, mean ± SD). Using spike triggered averaging, some cells in both regions were identified as likely premotor cells, with monosynaptic connections to motoneurons. Response latencies for these cells were compatible with a contribution to the muscle responses following the perturbation. Comparable fractions of responding neurons in both areas were active up to 100ms after the perturbation, suggesting that both SC circuits and supraspinal centers could contribute to later response components. Significance Statement Following a limb perturbation, multiple reflexes help to restore limb position. Given conduction delays, the earliest part of these reflexes can only arise from spinal circuits. By contrast, long latency reflex components are typically assumed to originate from supraspinal centers. We recorded from both spinal and motor cortical cells in monkeys responding to index finger perturbations. Many spinal interneurons, including those identified as projecting to motoneurons, responded to the perturbation; the timing of responses was compatible with a contribution to both short-and longlatency reflexes. We conclude that spinal circuits also contribute to long latency reflexes in distal and forearm muscles, alongside supraspinal regions such as the motor cortex and brainstem.

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Slowly-Conducting Pyramidal Tract Neurons in Macaque and Rat

Cited by 12 publications

References 52 publications

Extensive Cortical Convergence to Primate Reticulospinal Pathways

Extensive Cortical Convergence to Primate Reticulospinal Pathways

The Cortical “Upper Motoneuron” in Health and Disease

Long-latency Responses to a Mechanical Perturbation of the Index Finger Have a Spinal Component

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