Evidence that C1 and C2 propriospinal neurons mediate the inhibitory effects of viscerosomatic spinal afferent input on primate spinothalamic tract neurons

1. Lumbosacral spinothalamic tract (STT) neurons can be inhibited by noxious pinch of the contralateral hindlimb or either forelimb and by electrical stimulation of cardiopulmonary sympathetic, splanchnic, and hypogastric afferents. A previous study found that spinal transections between C2 and C4 sometimes abolished the inhibitory effect of spinal afferent input and sometimes left it intact. This suggested that propriospinal neurons in the C1 and C2 segments might mediate this effect. To test whether neurons in the C1 and C2 segments were involved in producing this inhibitory effect, the magnitude of the reduction in neural activity was measured in the same STT neuron before and after spinal transection at C1 or between C3 and C7. 2. All neurons were antidromically activated from the contralateral thalamus and thoracic spinal cord. For us to accept a neuron for analysis, the characteristics of the somatic input and the latency and shape of the antidromatic spike produced by spinal cord stimulation had to be the same before and after the spinal transection. Also, spinal transection often causes a marked increase in spontaneous cell activity, which may affect the magnitude of an inhibitory response. To avoid this confounding problem, a cell was accepted for analysis only if it showed marked inhibition of high cell activity evoked by somatic pinch before spinal transection. For analysis 13 STT neurons met these criteria: 6 neurons were in monkeys with C1 transections, and 7 neurons were in animals with transections between C3 and C7.(ABSTRACT TRUNCATED AT 250 WORDS)

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Responses of T2-4 spinal cord neurons to irritation of the lower airways in the rat

AJP Regulatory Integrative and Comparative Physiology ◽

10.1152/ajpregu.1997.273.3.r1147 ◽

1997 ◽

Vol 273 (3) ◽

pp. R1147-R1157 ◽

Cited By ~ 7

Author(s):

T. Hummel ◽

J. N. Sengupta ◽

S. T. Meller ◽

G. F. Gebhart

Keyword(s):

Spinal Cord ◽

Afferent Input ◽

Sprague Dawley ◽

Spinal Neurons ◽

Thoracic Spinal Cord ◽

Spinal Cord Neurons ◽

Thoracic Spinal ◽

Balloon Distension ◽

Sprague Dawley Rats ◽

Lower Airways

The aim of the study was to investigate the information processing in the thoracic spinal cord (T2-4) after chemical irritation of the lower airways. Experiments were performed in pentobarbital sodium-anesthetized and pancuronium-paralyzed male Sprague-Dawley rats. Balloon distension of the esophagus was used as the search stimulus. Ammonia and smoke were applied by means of a tracheal cannula; they produced excitatory, inhibitory, and biphasic responses in a concentration-related manner (ammonia 39/39; smoke 23/ 39). Inhaled irritant-responsive neurons exhibited a number of similarities that have been described for neurons responding to stimulation of other thoracic viscera. These similarities relate to the distribution of neurons in the deeper laminae of the thoracic spinal cord, the relatively small number of neurons receiving input from the lower airways, the extensive convergent input from the skin and other thoracic viscera, and the pattern of responses. In addition, both stimulus-induced responses and spontaneous activity are subject to modulation from supraspinal sites. On the basis of responses to inhaled irritants after either spinal cord or vagus nerve block/transection, these T2-4 spinal neurons are likely to receive spinal afferent input that is modulated by vagal-brain stem input.

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Convergence of visceral and cutaneous input onto spinothalamic tract cells in the thoracic spinal cord of the cat

Pain ◽

10.1016/0304-3959(76)90013-0 ◽

1976 ◽

Vol 2 (3) ◽

pp. 326

Author(s):

M. B. Hancock ◽

R. D. Foreman ◽

W. D. Willis

Keyword(s):

Spinal Cord ◽

Spinothalamic Tract ◽

Thoracic Spinal Cord ◽

Thoracic Spinal

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Segmental organization of visceral and somatic input onto C3-T6 spinothalamic tract cells of the monkey

Journal of Neurophysiology ◽

10.1152/jn.1992.68.5.1575 ◽

1992 ◽

Vol 68 (5) ◽

pp. 1575-1588 ◽

Cited By ~ 51

Author(s):

S. F. Hobbs ◽

M. J. Chandler ◽

D. C. Bolser ◽

R. D. Foreman

Keyword(s):

Spinal Cord ◽

Electrical Stimulation ◽

Urinary Bladder ◽

Visceral Pain ◽

Cell Activity ◽

Afferent Input ◽

Spinothalamic Tract ◽

Afferent Fibers ◽

Increased Activity ◽

Stimulation Of

1. Referred pain of visceral origin has three major characteristics: visceral pain is referred to somatic areas that are innervated from the same spinal segments as the diseased organ; visceral pain is referred to proximal body regions and not to distal body areas; and visceral pain is felt as deep pain and not as cutaneous pain. The neurophysiological basis for these phenomena is poorly understood. The purpose of this study was to examine the organization of viscerosomatic response characteristics of spinothalamic tract (STT) neurons in the rostral spinal cord. Interactions were determined among the following: 1) segmental location, 2) effects of input by cardiopulmonary sympathetic, greater splanchnic, lumbar sympathetic, and urinary bladder afferent fibers, 3) location of excitatory somatic field, e.g., hand, forearm, proximal arm, or chest, 4) magnitude of response to hair, skin, and deep mechanoreceptor afferent input, and 5) regional specificity of thalamic projection sites. 2. A total of 89 STT neurons in segments C3-T6 were characterized for responses to visceral and somatic stimuli. Neurons were activated antidromically from the contralateral ventroposterolateral oralis or caudalis nuclei of the thalamus. Cell responses to visceral and somatic stimuli were not different on the basis of the thalamic site of antidromic activation. Recording sites for 61 neurons were located histologically; 87% of lesion sites were located in laminae IV-VII or X. There was no relationship between response properties of the neurons and spinal laminar location. 3. Different responses to visceral stimuli were observed in three zones of the rostral spinal cord: C3-C6, C7-C8, and T1-T6. In C3-C6, urinary bladder distension (UBD) and electrical stimulation of greater splanchnic and lumbar sympathetic afferent fibers inhibited STT cells. Electrical stimulation of cardiopulmonary sympathetic afferents increased cell activity in C5 and C6 and either excited or inhibited STT cells in C3 and C4. In the cervical enlargement (C7-C8), STT cells generally were either inhibited or showed little response to stimulation of visceral afferent fibers. In T1-T6, input from greater splanchnic and cardiopulmonary sympathetic afferent nerves increased activity of STT cells. Lumbar sympathetic afferent input inhibited cells in T1-T2 and had little effect on cells in T3-T6, whereas UBD decreased cell activity in all segments studied. 4. In general, stimulation of somatic structures increased activity of STT neurons in segments that received primary afferent innervation from the excitatory somatic receptive field or in the segments immediately adjacent to these segments. Only input from the forelimb, especially the hand, markedly excited cells in C7 and C8.+

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Convergence of visceral and cutaneous input onto spinothalamic tract cells in the thoracic spinal cord of the cat

Experimental Neurology ◽

10.1016/0014-4886(75)90253-8 ◽

1975 ◽

Vol 47 (2) ◽

pp. 240-248 ◽

Cited By ~ 88

Author(s):

M.B. Hancock ◽

R.D. Foreman ◽

W.D. Willis

Keyword(s):

Spinal Cord ◽

Spinothalamic Tract ◽

Thoracic Spinal Cord ◽

Thoracic Spinal

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Inspiratory action of separate external and parasternal intercostal muscle contraction

Journal of Applied Physiology ◽

10.1152/jappl.1989.67.4.1395 ◽

1989 ◽

Vol 67 (4) ◽

pp. 1395-1400 ◽

Cited By ~ 15

Author(s):

K. Budzinska ◽

G. Supinski ◽

A. F. DiMarco

Keyword(s):

Spinal Cord ◽

Muscle Contraction ◽

Airway Pressure ◽

Thoracic Spinal Cord ◽

Thoracic Spinal ◽

Before And After ◽

Subsequent Section ◽

Electrical Stimuli ◽

Negative Airway Pressure ◽

Relative Capacity

We have previously shown that electrical stimulation of the thoracic spinal cord produces near maximal activation of the inspiratory intercostal muscles. In the present investigation, we used this technique to evaluate the relative capacity of separate external (EI) and parasternal intercostal (PA) muscle contraction to produce changes in airway pressure and inspired volume. Studies were performed in 23 anesthetized phrenicotomized dogs. Electrical stimuli were applied to the spinal cord after hyperventilation-induced apnea, before and after sequentially severing either the PA or EI muscles from the first through sixth intercostal spaces. During spinal cord stimulation (SCS), measurements were made of inspired volume (delta V) with the airway open and negative airway pressure (delta P) during tracheal occlusion. Compared with control values, sectioning of the PA muscles resulted in a 40.9% reduction in delta P and 35.7% reduction in delta V during SCS. In other animals, initial sectioning of the EI muscles produced reductions in delta P and delta V of 67.4 and 63.0, respectively, during SCS. After subsequent section of the PA muscles, SCS produced only negligible inspired volumes and changes in airway pressure. We conclude that 1) the EI and PA muscles are each capable of generating substantial changes in airway pressure and large inspired volumes and 2) the ventilatory capacity of the EI muscles exceeds that of the PA muscles.

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Silencing long ascending propriospinal neurons after spinal cord injury improves hindlimb stepping in the adult rat

10.1101/2021.05.18.444653 ◽

2021 ◽

Author(s):

David SK Magnuson ◽

Courtney T Shepard ◽

Amanda M Pocratsky ◽

Brandon L Brown ◽

Morgan A Van Rijswijck ◽

...

Keyword(s):

Spinal Cord ◽

Spinal Cord Injury ◽

Injury Severity ◽

Dependent Manner ◽

Thoracic Spinal Cord ◽

Locomotor Function ◽

Adult Rat ◽

Thoracic Spinal ◽

Cord Injury ◽

Propriospinal Neurons

Long ascending propriospinal neurons (LAPNs) are a subpopulation of spinal cord interneurons that directly connect the lumbar and cervical enlargements. In uninjured animals, conditionally silencing LAPNs resulted in disrupted left-right coordination of the hindlimbs and forelimbs in a context-dependent manner, demonstrating that LAPNs secure alternation of the fore- and hindlimb pairs during overground stepping in the adult rat. Given their ventrolateral location in the spinal cord white matter, many LAPN axons likely remain intact following thoracic spinal cord injury (SCI), suggesting a potential role in the recovery of stepping. Thus, we hypothesized that silencing LAPNs after SCI would result in diminished hindlimb locomotor function. We found instead that silencing of spared LAPNs post-SCI restored the left-right hindlimb coordination associated with alternating gaits that was lost as a result of SCI. Several other fundamental characteristics of hindlimb stepping were also improved and the number of abnormal steps were reduced. However, hindlimb-forelimb coordination was not restored. These data suggest that the temporal information carried between the enlargements by the LAPNs after SCI may be detrimental to hindlimb locomotor function. These observations have implications for our understanding of the relationship between injury severity and functional outcome, for the efforts to develop neuro- and axo-protective therapeutic strategies, and also for the clinical study/implementation of spinal stimulation and neuromodulation.

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Locations of Spinothalamic Tract Axons in Cervical and Thoracic Spinal Cord White Matter in Monkeys

Journal of Neurophysiology ◽

10.1152/jn.2000.83.5.2869 ◽

2000 ◽

Vol 83 (5) ◽

pp. 2869-2880 ◽

Cited By ~ 26

Author(s):

Xijing Zhang ◽

Heather N. Wenk ◽

Christopher N. Honda ◽

Glenn J. Giesler

Keyword(s):

Spinal Cord ◽

White Matter ◽

Dorsal Horn ◽

Dynamic Range ◽

Spinothalamic Tract ◽

Thoracic Spinal Cord ◽

Antidromic Activation ◽

Lateral Funiculus ◽

Thoracic Spinal ◽

Low Threshold

The spinothalamic tract (STT) is the primary pathway carrying nociceptive information from the spinal cord to the brain in humans. The aim of this study was to understand better the organization of STT axons within the spinal cord white matter of monkeys. The location of STT axons was determined using method of antidromic activation. Twenty-six lumbar STT cells were isolated. Nineteen were classified as wide dynamic range neurons and seven as high-threshold cells. Fifteen STT neurons were recorded in the deep dorsal horn (DDH) and 11 in superficial dorsal horn (SDH). The axons of 26 STT neurons were located at 73 low-threshold points (<30 μA) within the lateral funiculus from T9 to C6. STT neurons in the SDH were activated from 33 low-threshold points, neurons in the DDH from 40 low-threshold points. In lower thoracic segments, SDH neurons were antidromically activated from low-threshold points at the dorsal-ventral level of the denticulate ligament. Neurons in the DDH were activated from points located slightly ventral, within the ventral lateral funiculus. At higher segmental levels, axons from SDH neurons continued in a position dorsal to those of neurons in the DDH. However, axons from neurons in both areas of the gray matter were activated from points located in more ventral positions within the lateral funiculus. Unlike the suggestions in several previous reports, the present findings indicate that STT axons originating in the lumbar cord shift into increasingly ventral positions as they ascend the length of the spinal cord.

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Silencing long ascending propriospinal neurons after spinal cord injury improves hindlimb stepping in the adult rat

eLife ◽

10.7554/elife.70058 ◽

2021 ◽

Vol 10 ◽

Author(s):

Courtney T Shepard ◽

Amanda M Pocratsky ◽

Brandon L Brown ◽

Morgan A Van Rijswijck ◽

Rachel M Zalla ◽

...

Keyword(s):

Spinal Cord ◽

Spinal Cord Injury ◽

Dependent Manner ◽

Thoracic Spinal Cord ◽

Locomotor Function ◽

Adult Rat ◽

Thoracic Spinal ◽

Cord Injury ◽

Study Implementation ◽

Propriospinal Neurons

Long ascending propriospinal neurons (LAPNs) are a subpopulation of spinal cord interneurons that directly connect the lumbar and cervical enlargements. Previously we showed, in uninjured animals, that conditionally silencing LAPNs disrupted left-right coordination of the hindlimbs and forelimbs in a context-dependent manner, demonstrating that LAPNs secure alternation of the fore- and hindlimb pairs during overground stepping. Given the ventrolateral location of LAPN axons in the spinal cord white matter, many likely remain intact following incomplete, contusive, thoracic spinal cord injury (SCI), suggesting a potential role in the recovery of stepping. Thus, we hypothesized that silencing LAPNs after SCI would disrupt recovered locomotion. Instead, we found that silencing spared LAPNs post-SCI improved locomotor function, including paw placement order and timing, and a decrease in the number of dorsal steps. Silencing also restored left-right hindlimb coordination and normalized spatiotemporal features of gait such as stance and swing time. However, hindlimb-forelimb coordination was not restored. These data indicate that the temporal information carried between the spinal enlargements by the spared LAPNs post-SCI is detrimental to recovered hindlimb locomotor function. These findings are an illustration of a post-SCI neuroanatomical-functional paradox and have implications for the development of neuronal- and axonal-protective therapeutic strategies and the clinical study/implementation of neuromodulation strategies.

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