Intermittent Hypoxia Enhances Functional Connectivity of Midcervical Spinal Interneurons

Streeter, Kristi A.; Sunshine, Michael D.; Patel, Shweta; Gonzalez‐Rothi, Elisa J.; Reier, Paul J.; Baekey, David M.; Fuller, David D.

doi:10.1523/jneurosci.0992-17.2017

Cited by 35 publications

(37 citation statements)

References 54 publications

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“…This is supported by the parallel time course of changes in the amplitude of MEPs elicited by both TMS and electrical stimulation after AIH. Further supporting this idea, rat studies demonstrate that even a single AIH exposure changes the connectivity of spinal interneurons that may project to relevant motoneurons ( Streeter et al, 2017 ). To further examine the origin of subcortical effects, we measured transmission at spinal synapses and the excitability of spinal motoneurons.…”

Section: Discussionmentioning

confidence: 93%

“…Other studies showed that AIH elicits plasticity in neural systems not directly linked to the respiratory system. For example, exposure to AIH transiently increases sympathetic nerve activity ( Dick et al, 2007 ; Xing and Pilowsky, 2010 ) and connectivity of spinal interneurons projecting to midthoracic motoneurons ( Streeter et al, 2017 ). A critical question is if AIH can modulate activity in descending motor pathways in intact humans and its mechanisms of action.…”

Section: Introductionmentioning

confidence: 99%

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Acute intermittent hypoxia enhances corticospinal synaptic plasticity in humans

Christiansen

Urbin

Mitchell

et al. 2018

eLife

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Acute intermittent hypoxia (AIH) enhances voluntary motor output in humans with central nervous system damage. The neural mechanisms contributing to these beneficial effects are unknown. We examined corticospinal function by evaluating motor evoked potentials (MEPs) elicited by cortical and subcortical stimulation of corticospinal axons and the activity in intracortical circuits in a finger muscle before and after 30 min of AIH or sham AIH. We found that the amplitude of cortically and subcortically elicited MEPs increased for 75 min after AIH but not sham AIH while intracortical activity remained unchanged. To examine further these subcortical effects, we assessed spike-timing dependent plasticity (STDP) targeting spinal synapses and the excitability of spinal motoneurons. Notably, AIH increased STDP outcomes while spinal motoneuron excitability remained unchanged. Our results provide the first evidence that AIH changes corticospinal function in humans, likely by altering corticospinal-motoneuronal synaptic transmission. AIH may represent a novel noninvasive approach for inducing spinal plasticity in humans.

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Section: Discussionmentioning

confidence: 93%

Section: Introductionmentioning

confidence: 99%

Acute intermittent hypoxia enhances corticospinal synaptic plasticity in humans

Christiansen

Urbin

Mitchell

et al. 2018

eLife

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“…However, since synaptic scaling is the mechanism by which synaptic strength increases in motoneurons, this interpretation is not unreasonable. Second, despite acceptance that motoneuron firing rates and/or recruitment explains the motor amplitude in respiratory preparations (Nichols & Mitchell, ), interneurons may also shape the activity of respiratory motoneurons, and thus, amplitude of the motor output (Streeter et al, ). Therefore, whether DNQX reduces motor amplitude after hibernation due to actions exclusively on motoneurons or other network components is not yet clear.…”

Section: Evidence For Compensatory Forms Of Plasticity In the Respiramentioning

confidence: 99%

Motor inactivity in hibernating frogs: Linking plasticity that stabilizes neuronal function to behavior in the natural environment

Santin

2019

Developmental Neurobiology

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All animals must generate reliable neuronal activity to produce adaptive behaviors in an ever-changing environment. Neural systems are thought to achieve this goal, in part, through cellular and synaptic plasticity mechanisms that stabilize electrophysiological functions. Despite strong evidence for a role in regulating neuronal properties, these plasticity mechanisms have been difficult to link to natural behaviors in animals. In this review, I discuss how animals that inhabit extreme environments can address this challenge. As an example, I highlight recent work from frogs that stop breathing for several months during hibernation and, in response, use classic mechanisms of stabilizing plasticity to support respiratory motor output shortly after emergence. Furthermore, I describe problems for neuronal stability that may benefit from the study of hibernators: how circuits with variable modes of output control stabilizing mechanisms over long time scales and why some neural systems mount robust compensatory responses and others do not. By continuing to appreciate how diverse animal groups overcome challenges in the natural environment, we will broaden our view of the role that plasticity mechanisms play in stabilizing the nervous system. K E Y W O R D SAMPA receptor, control of breathing, hibernation, homeostatic plasticity, motor systems

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“…This is based on observations that at least a subset of propriospinal neurons are innervated by inspiratory rVRG neurons or display inspiratory-related phasic bursting (Hilaire et al, 1983(Hilaire et al, , 1986Palisses et al, 1989;Duffin and Iscoe, 1996;Hayashi et al, 2003;Lane et al, 2008;Sandhu et al, 2015). Multiunit recordings of spinal neurons and cross-correlation analyses have identified both excitatory and inhibitory pre-phrenic propriospinal neurons in the rat cervical cord (Sandhu et al, 2015;Streeter et al, 2017). Acute intermittent hypoxia (a known driver of respiratory plasticity) enhances functional connectivity between excitatory neurons and pre-phrenic propriospinal neurons, suggesting that changes in propriospinal neuron function can increase motor output (Streeter et al, 2017).…”

Section: Propriospinal Neurons Shape the Pattern Of Respiratory Motormentioning

confidence: 99%

“…Multiunit recordings of spinal neurons and cross-correlation analyses have identified both excitatory and inhibitory pre-phrenic propriospinal neurons in the rat cervical cord (Sandhu et al, 2015;Streeter et al, 2017). Acute intermittent hypoxia (a known driver of respiratory plasticity) enhances functional connectivity between excitatory neurons and pre-phrenic propriospinal neurons, suggesting that changes in propriospinal neuron function can increase motor output (Streeter et al, 2017). In addition, inhibitory neurons help pattern the duration of motor output.…”

Section: Propriospinal Neurons Shape the Pattern Of Respiratory Motormentioning

confidence: 99%

Role of Propriospinal Neurons in Control of Respiratory Muscles and Recovery of Breathing Following Injury

Jensen

Alilain

Crone

2020

Front. Syst. Neurosci.

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Respiratory motor failure is the leading cause of death in spinal cord injury (SCI). Cervical injuries disrupt connections between brainstem neurons that are the primary source of excitatory drive to respiratory motor neurons in the spinal cord and their targets. In addition to direct connections from bulbospinal neurons, respiratory motor neurons also receive excitatory and inhibitory inputs from propriospinal neurons, yet their role in the control of breathing is often overlooked. In this review, we will present evidence that propriospinal neurons play important roles in patterning muscle activity for breathing. These roles likely include shaping the pattern of respiratory motor output, processing and transmitting sensory afferent information, coordinating ventilation with motor activity, and regulating accessory and respiratory muscle activity. In addition, we discuss recent studies that have highlighted the importance of propriospinal neurons for recovery of respiratory muscle function following SCI. We propose that molecular genetic approaches to target specific developmental neuron classes in the spinal cord would help investigators resolve the many roles of propriospinal neurons in the control of breathing. A better understanding of how spinal circuits pattern breathing could lead to new treatments to improve breathing following injury or disease.

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Intermittent Hypoxia Enhances Functional Connectivity of Midcervical Spinal Interneurons

Abstract: Brief, intermittent oxygen reductions [acute intermittent hypoxia (AIH)]

Cited by 35 publications

References 54 publications

Acute intermittent hypoxia enhances corticospinal synaptic plasticity in humans

Acute intermittent hypoxia enhances corticospinal synaptic plasticity in humans

Motor inactivity in hibernating frogs: Linking plasticity that stabilizes neuronal function to behavior in the natural environment

Role of Propriospinal Neurons in Control of Respiratory Muscles and Recovery of Breathing Following Injury

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