Increased receptive field size of dorsal horn neurons following chronic spinal cord hemisections in cats

doi:10.1016/0006-8993(81)91277-4

Brain Research

Volume 216, Issue 1, 6 July 1981, Pages 45-59

https://doi.org/10.1016/0006-8993(81)91277-4 Get rights and content

Abstract

The somatotopic organization of the 17 dorsal horn was studied using extracellular recordings in normal cats, and in cats with acute or chronic spinal cord hemisection at T13, sparing the dorsal columns. Based on data concerning recovery of function and collateral sprouting of afferents following hemisections, we predicted that the lesion would result in increases in receptive field size and decreases in the specificity of the somatotopic map. In normal animals, the usual mediolateral, rostrocaudal and dorsoventral somatotopic sequences were found. Following acute hemisections (6 h–5 days), there were changes in spontaneous and evoked activity, but receptive field sizes and somatotopic organization remained unchanged. Following chronic hemisections (88–174 days), proximal hindlimb receptive fields in the lateral dorsal horn ipsilateral to the lesion increased dramatically in size and were significantly larger than similar receptive fields on the contralateral side. The largest of these fields extended from the dorsal midline to the middle of the foot. Receptive field sizes elsewhere in the dorsal horn remained unchanged, as did somatotopic organization in general. These findings indicate that hemisections result in a complex series of changes consisting of an early stage of anatomically generalized changes in excitability and a later stage of highly localized changes in receptive field size. Possible mechanisms for these changes, as well as their relationship to recovery of function, are discussed.

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Citation Excerpt :
In the long term (weeks to months), spinal hemisection can give rise to both cortical reorganization (Ghosh et al., 2009; Martinez et al., 2010) and neuropathic pain (Christensen et al., 1996; Bennett et al., 2000). In the short term (immediately after the lesion), spinal hemisection markedly increases the spontaneous and evoked activity of dorsal horn neurons originating the spinothalamic tract (Brenowitz and Pubols, 1981; Hains et al., 2003), probably due to the loss of descending inhibition (Yaksh and Wilson, 1979; Skagerberg and Bjorklund, 1985; Hains et al., 2002, 2003). However, whether and how these immediate functional changes at spinal level are reflected at cortical level remains unknown.
Chronic injury of the main somatosensory pathways ascending along the spinal cord - the dorsal columns and the spinothalamic tract - can produce both changes in the organization of cortical somatotopic maps and neuropathic pain. Little is known, however, about the early neurophysiological changes occurring immediately after injury. We bilaterally recorded the neural activity of the hindpaw representation of the primary somatosensory cortex evoked by stimuli delivered to the hindpaws before and immediately after a thoracic spinal cord hemisection in anesthetized rats. This unilateral spinal cord injury allowed us to separately investigate the cortical effects of deafferenting the dorsal column (stimuli ipsilateral to the hemisection) or the spinothalamic tract (stimuli contralateral to the hemisection). The hemisection produced immediate bilateral changes in the cortical responses evoked by stimuli delivered to the hindpaw ipsilateral to the hemisection (deafferented dorsal column): an expected loss of classical short-latency cortical responses, accompanied by an unexpected appearance of long-latency activations. At the population level, these activations reflected a progressive stimulus-induced transition of the hindpaw somatosensory cortex from up-and-down states to a sustained activated state. At the single-cell level, these cortical activations resembled the “wind-up” typically observed – with the same type of stimuli – in the dorsal horn cells originating the spinothalamic tract. Virtually no changes were observed in the responses evoked by stimuli delivered to the hindpaw contralateral to the hemisection (deafferented spinothalamic tract). These results suggest that spinal cord hemisection immediately produces an abnormal hyperexcitability of the primary somatosensory cortex in response to preserved spinothalamic inputs from the hindpaw. This immediate cortical hyperexcitability could be important to understand the long-term development of cortical reorganization and neuropathic pain after incomplete spinal cord lesions.
Enhancement of wind-up by the combined administration of adenosine A <inf>1</inf> receptor ligands on spinalized rats with carrageenan-induced inflammation
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The adenosine A₁ receptor agonist N6-cyclopentyladenosine (CPA) is very effective in reducing wind-up in intact but not in spinalized adult rats with carrageenan-induced inflammation, suggesting an adenosine-mediated supraspinal modulation. Since wind-up is a spinal cord mediated phenomenon but highly influenced by descending modulatory systems, especially in situations of sensitization, we assessed the possible involvement of adenosine in the modulation of wind-up. We studied the effect of the adenosine A₁ receptor antagonist 8-cyclopentyl-1,3-dimethylxanthine (CPT) in the presence and in the absence of the adenosine A₁ receptor agonist CPA. The experiments were carried out in spinalized male Wistar rats under α-chloralose anaesthesia. Withdrawal reflexes, studied as single motor units, were activated by noxious mechanical and high-intensity repetitive electrical stimulation (wind-up). While CPA and CPT were not able to induce any change on wind-up when injected alone, the combination of the two drugs, in any order, lead to an important enhancement of wind-up. This enhancement not always paralleled an increase of responses to noxious mechanical stimulation, indicating that the effect is mainly located in the spinal cord. In addition, the enhancement of wind-up was not further increased by the administration of the opioid receptor antagonist naloxone. We conclude that the depression of the wind-up phenomenon observed in spinalized animals is, at least in part, dependent of adenosine systems and can be relieved by the combined administration of CPA and CPT.
Temporal plasticity of dorsal horn somatosensory neurons after acute and chronic spinal cord hemisection in rat
2003, Brain Research
Unilateral T13 hemisection of the rat spinal cord produces a model of chronic spinal cord injury (SCI) that is characterized by bilateral hyperexcitability of lumbar dorsal horn neurons, and behavioral signs of central pain. While we have demonstrated that responsiveness of multireceptive (MR) dorsal horn neurons is dramatically increased at 28 days after injury, the effects of acute hemisection are unknown and predicted to be different than observed chronically. In the present study, the consequences of T13 hemisection are examined acutely at 45 min in MR neurons both ipsilateral and contralateral to the site of injury, and compared to the same class of cells at 28 days after injury (n=20 cells total per group: 2–3 cells/side of the cord from n=5 animals). Acutely, ipsilateral to the hemisection, both spontaneous and evoked activity of MR neurons were significantly increased, whereas contralaterally, only evoked activity was significantly increased. In animals 28 days after hemisection, spontaneous activity of MR neurons was comparable to intact levels ipsilaterally, and cells exhibited hyperexcitability to evoked stimuli bilaterally. Expansion of cutaneous receptive fields was observed only in hindpaws ipsilateral to the lesion, acutely. These results demonstrate dynamic plasticity in properties of dorsal horn somatosensory neurons after SCI.
Enlargement of the receptive field size to low intensity mechanical stimulation in the rat spinal nerve ligation model of neuropathy
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One characteristic of plasticity after peripheral tissue or nerve damage is receptive field reorganization, and enlargement of receptive field size has been suggested to occur in certain models of neuropathic pain. The aim of the present study was to explore whether enlargement of neuronal receptive fields could contribute to the mechanical allodynia found on the ipsilateral paw in the spinal nerve ligation model of neuropathy. After ligation of L₅–L₆ spinal nerves, all rats developed behavioral signs of mechanical allodynia, while the sham-operated control group displayed no such changes. The characteristics of the evoked responses of the neurones recorded in the dorsal horn of the rats were similar between the spinal nerve ligation, the sham operated control group, and the nonoperated control group, except for spontaneous activity, which was significantly increased in the spinal nerve ligation group. The mean size of the receptive field on the ipsilateral hindpaw, mapped using low-intensity stimulation with 9-g von Frey hair, was significantly increased in the spinal nerve ligation group, as compared to the sham-operated group. No significant difference was seen with 15- or 75-g von Frey hairs. The distribution of the receptive fields over the plantar surface of the paw was similar between the study groups. The enlargement of receptive field for nonnoxious touch could be an indication of central sensitization in this model.
Supraspinal influences on the facilitation of rat nociceptive reflexes induced by carrageenan monoarthritis
1996, Neuroscience Letters
During hyperalgesia there is an enhancement of wind-up and the appearance of a novel wind-up of the A-fibre-mediated responses. We have examined if these phenomena are influenced by supraspinal mechanisms by analysing single motor unit activity in control and arthritic rats, either intact or acutely spinalised. Enhancement of the C-fibre wind-up and the novel A-fibre wind-up were only observed in the intact arthritic animals. We conclude that C-fibre wind-up is a spinal phenomenon, whereas the enhancement of the C-fibre wind-up and the novel A-fibre wind-up during arthritis depend also on supraspinal influences.
The recovery of postural reflexes and locomotion following low thoracic hemisection in adult cats involves compensation by undamaged primary afferent pathways
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Spinal hemisection in the adult cat results in motor impairments followed by substantial recovery of function (16, 20, 39, 53). The present study was undertaken to assess the contribution of undamaged ipsilateral segmental and contralateral descending systems to recovery of motor function. Quantitative behavioral methods were used to examine monopedal reflex and bipedal locomotor functions after thoracic hemisection. Different facets of motor behavior recover at different times. The recovery of monopedal postural reflexes precedes the recovery of more complex motor behavior. Since the reflexes tested are initiated by segmental afferent input and show recovery and normal motor patterns during locomotion, as defined by kinematic analysis show recovery, it is likely that dorsal root input compensates for the loss of descending input to one side of the spinal cord. Quantitative immunocytochemical methods for visualizing the central projections of dorsal root fibers (monoclonal antibody RAT-102; 49) and the descending serotoninergic pathway were used to examine the response of these pathways to hemisection. Hemisection results in a permanent decrease in the density of serotoninergic projections and a permanent increase in dorsal root projections in the spinal cord. The increased density of RAT-102 may represent an increase in the projection of dorsal root fibers and provide the increased input necessary to mediate enhanced reflex control. A transient increase in GAP-43 in the dorsal horn ipsilateral to the hemisection suggests that the increased density of RAT-102 immunoreactivity is associated with growth. Taken together, our results suggest that sprouting of primary afferents within the spinal cord is one mechanism underlying the recovery of function after hemisection.

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Increased receptive field size of dorsal horn neurons following chronic spinal cord hemisections in cats

Abstract

Brain Research

Brain Research

Brain Research

Exp. Neurol.

Neurosci. Lett.

Brain Research

Brain Research

Exp. Neurol.

Neuroscience

Brain Research

Brain Research

Brain Research

Exp. Neurol.

Degeneration studies of long ascending fiber systems in the cat brain stem

J. comp. Neurol.

Spinal afferents to the lateral cervical nucleus in the cat

J. comp. Neurol.

Effects of descending impulses on transmission through the spinocervical tract

J. Physiol. (Lond.)

Inhibition of spinocervical tract discharges from localized areas of the sensorimotor cortex in the cat

J. Physiol. (Lond.)

The density, distribution and topographical organization of spinocervical tract neurones in the cat

J. Physiol. (Lond.)

The morphology of spinocervical tract neurones in the cat

J. Physiol. (Lond.)

Somatotopic representation of hindlimb skin in cat dorsal horn

J. Neurophysiol.

Responses of spinocervical tract neurones to noxious stimulation of the skin

J. Physiol. (Lond.)

Corticospinal tract of the cat

J. comp. Neurol.

Dorsal horn neurons that respond to stimulation of distant dorsal roots

J. Physiol. (Lond.)