Physiological and Morphological Characteristics of Spinal Neurons Projecting to the Parabrachial Region of the Cat

Light, Alan R.; Sedivec, Mathius J.; Casale, Eugene J.; Jones, Susan Y.

doi:10.3109/08990229309028840

Cited by 80 publications

(96 citation statements)

References 41 publications

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“…Presumably, this effect is due to a series of descending pain-inhibitory pathways: First, the PAG projects to the raphe magnus nucleus; then, a descending raphe projection terminating in laminae I and II of the dorsal horn functions to inhibit incoming nociceptive information (Budai and Fields, 1998; for review, see Fields et al, 1991). However, both anatomical studies (Cechetto et al, 1985;Slugg and Light, 1994;Feil and Herbert, 1995; and physiological studies (Light et al, 1993;Menendez et al, 1996;Bester et al, 1995) have shown that the PB is an important nociceptive relay nucleus. Therefore, the PAG system may also modulate ascending pain information through PAG=PB connections.…”

Section: Discussionmentioning

confidence: 99%

Periaqueductal gray matter projection to the parabrachial nucleus in rat

1998

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The efferent projections from the periaqueductal gray matter (PAG) to the parabrachial nucleus (PB) were studied in the rat following microinjections of the anterograde axonal tracer Phaseolus vulgaris-leucoagglutinin (PHA-L) into restricted regions of the PAG. The dorsomedial and dorsolateral PAG columns project almost exclusively to the superior lateral PB subnucleus, whereas the lateral and ventrolateral PAG columns project to five lateral PB sites: dorsal lateral subnucleus, medial and lateral crescent areas (which flank the dorsal lateral PB subnucleus), central lateral subnucleus (rostral portion), and superior lateral subnucleus. The PAG region lying near the cerebral aqueduct projects to five lateral PB sites: external lateral subnucleus (inner subdivision), medial and lateral crescent areas, central lateral subnucleus (rostral portion), and dorsal lateral subnucleus. The internal lateral PB subnucleus, which projects exclusively to the intralaminar thalamic nuclei, and the Kölliker-Fuse nucleus were not innervated by the PAG. The PAG selectively innervates individual PB subnuclei that may be part of the spino-parachio-forebrain pathway. All PAG columns, including the aqueductal region, project to the superior lateral PB subnucleus, a presumed nociceptive relay site that receives inputs from multiple spinal cord regions (laminae I, V, and VIII) and projects to the ventromedial and retrochiasmatic hypothalamic areas-two regions that have been implicated in complex goal-directed behavior (e.g., food intake and reproductive function). Earlier studies demonstrated that the dorsal lateral and external lateral PB subnuclei (inner division) receive overlapping inputs from the superficial dorsal horn (laminae I and II) and the nucleus tractus solitarius, and both PB subnuclei send projections to limbic forebrain areas (e.g., hypothalamus, preoptic region, amygdala). Because the PAG projects to both of these PB subnuclei, this projection system possibly functions as a behavioral state-dependent filter system that modulates ascending nociceptive and/or visceral information as it is relayed through the PB to forebrain sites.

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Section: Discussionmentioning

confidence: 99%

Periaqueductal gray matter projection to the parabrachial nucleus in rat

1998

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“…Even though these afferents invade dorsal horn superficial laminae, a role for them in the inhibition of nociceptive transmission has been suggested (Boada andWoodbury 2007, 2008;Lu and Perl 2003;Melzack and Wall 1965;Narikawa et al 2000). As we know, substantia gelatinosa neurons integrate both light tactile and nociceptive information (Bennett et al 1980;Light et al 1993) (for review, see Light 1992); therefore, we speculate that, after injury, reduced or silenced tactile inputs should provide uninhibited access of greatly sensitized nociceptors to substantia gelatinosa circuits, and this may contribute to the development of a chronic pain state. It is also tempting to speculate that the large population of silent afferents with an F-type signature, typical of LTMRs found after injury, may reflect a terminal desensitization state of some cells of this class, although further studies (anatomical and immunohistochemical) are required to definitively elucidate their identity and contribution, if any, to pain and hypersensitivity after injury.…”

Section: Tactilesmentioning

confidence: 99%

Nerve injury induces a new profile of tactile and mechanical nociceptor input from undamaged peripheral afferents

Boada

Gutiérrez

Aschenbrenner

et al. 2015

Journal of Neurophysiology

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Boada MD, Gutierrez S, Aschenbrenner CA, Houle TT, Hayashida K, Ririe DG, Eisenach JC. Nerve injury induces a new profile of tactile and mechanical nociceptor input from undamaged peripheral afferents. J Neurophysiol 113: 100 -109, 2015. First published October 1, 2014 doi:10.1152/jn.00506.2014.-Chronic pain after nerve injury is often accompanied by hypersensitivity to mechanical stimuli, yet whether this reflects altered input, altered processing, or both remains unclear. Spinal nerve ligation or transection results in hypersensitivity to mechanical stimuli in skin innervated by adjacent dorsal root ganglia, but no previous study has quantified the changes in receptive field properties of these neurons in vivo. To address this, we recorded intracellularly from L 4 dorsal root ganglion neurons of anesthetized young adult rats, 1 wk after L 5 partial spinal nerve ligation (pSNL) or sham surgery. One week after pSNL, hindpaw mechanical withdrawal threshold in awake, freely behaving animals was decreased in the L 4 distribution on the nerve-injured side compared with sham controls. Electrophysiology revealed that highthreshold mechanoreceptive cells of A-fiber conduction velocity in L 4 were sensitized, with a seven-fold reduction in mechanical threshold, a seven-fold increase in receptive field area, and doubling of maximum instantaneous frequency in response to peripheral stimuli, accompanied by reductions in after-hyperpolarization amplitude and duration. Only a reduction in mechanical threshold (minimum von Frey hair producing neuronal activity) was observed in C-fiber conduction velocity high-threshold mechanoreceptive cells. In contrast, low-threshold mechanoreceptive cells were desensitized, with a 13-fold increase in mechanical threshold, a 60% reduction in receptive field area, and a 40% reduction in instantaneous frequency to stimulation. No spontaneous activity was observed in L 4 ganglia, and the likelihood of recording from neurons without a mechanical receptive field was increased after pSNL. These data suggest massively altered input from undamaged sensory afferents innervating areas of hypersensitivity after nerve injury, with reduced tactile and increased nociceptive afferent response. These findings differ importantly from previous preclinical studies, but are consistent with clinical findings in most patients with chronic neuropathic pain. chronic pain model; in vivo electrophysiology; sensory neurons; spinal nerve ligation IN HUMANS, NEUROPATHIC PAIN includes both spontaneous and evoked pain, often accompanied by hypersensitivity to normal nociceptive stimuli (hyperalgesia) and normally nonnociceptive stimuli (allodynia). This pathological condition is also sometimes accompanied by dysesthesias and paresthesias (von Hehn et al. 2012), suggesting that both tactile and nociceptive information channels and/or processing are disrupted.

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“…Thus, nociceptive-responsive spinal cord neurons that project to PB have been demonstrated (Hylden et al, 1986;Light et al, 1987Light et al, , 1993Menetrey and de Pommery, 1991;Noguchi and Ruda, 1992;Ding et al, 1994;Jasmin et al, 1994;Wang et al, 19941, and neurons in the lateral part of PB that are activated by noxious stimuli have been recorded (Bernard and Besson, 1990;Slugg and Light, 1990;Bernard et al, 1994). The anterograde tracing study by Feil and Herbert (1995) demonstrated that the superficial dorsal horn of lumbar segments projects preferentially to the contralateral PBdl and adjacent lateral portions of PBcl; in the present study, the same PB regions contained many FOS-LI neurons after noxious hindpaw stimulation.…”

Section: Correlation Of the Fos Expression With The Ascending Spinal mentioning

confidence: 99%

Subnuclear localization of FOS-like immunoreactivity in the rat parabrachial nucleus after nociceptive stimulation

Hermanson

Blomqvist

1996

J. Comp. Neurol.

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The effect of noxious stimulation on the expression of FOS-like immunoreactivity (FOS-LI) in neurons of the parabrachial nucleus (PB) was studied in awake, freely moving rats. In one series of experiments, the rats were subjected to noxious mechanical stimulation (pinch) of either the nape of the neck or the base of the tail for 20 seconds every 5 minutes for 90 minutes, and then they were killed by transcardial perfusion after 45-210 minutes. Control animals received innocuous mechanical stimulation (brush) of the tail. Noxious stimuli resulted in FOS-LI in neurons in the dorsal part of the lateral PB, with heavy labeling in the superior lateral (PBsl) and the dorsal lateral (PBdl) subnuclei. FOS-LI was also elicited in the central lateral subnucleus (PBcl) and, although much more sparsely, in the external lateral subnucleus and the Kölliker-Fuse nucleus. Tail and neck stimulation resulted in similar labeling patterns, but more neurons, particularly in PBsl, expressed FOS-LI after pinch of the tail than of the neck. In another series of experiments, rats received injection of 5% formalin into one hindpaw. After 75-90 minutes, FOS-LI was seen in the same parts of PB as after noxious mechanical stimulation. The heaviest labeling was seen on the side contralateral to the injection side, with statistically significant (P < 0.05) side differences present in PBsl and PBdl. In a third series of experiments, rats were hemisected at low cervical-upper thoracic segments, allowed 2 weeks to recover, and then given formalin injections in both hindpaws. Significantly more neurons were FOS-labeled in PBdl, PBsl, and PBcl on the side contralateral to the hemisection than on the ipsilateral side. These observations are discussed in relation to the organization of the spinal afferent input and the efferent connections of PB. It is concluded that the FOS-LI expression in PBdl and PBsl and probably also in PBcl, to a large extent, is evoked by the ascending spinal nociceptive input to PB. Because these subnuclei project to several hypothalamic regions, it is suggested that neurons in PB that express FOS after noxious mechanical and chemical stimulation primarily are involved in autonomic and homeostatic responses to behavioral situations that involve tissue-damaging stimuli.

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Physiological and Morphological Characteristics of Spinal Neurons Projecting to the Parabrachial Region of the Cat

Cited by 80 publications

References 41 publications

Periaqueductal gray matter projection to the parabrachial nucleus in rat

Periaqueductal gray matter projection to the parabrachial nucleus in rat

Nerve injury induces a new profile of tactile and mechanical nociceptor input from undamaged peripheral afferents

Subnuclear localization of FOS-like immunoreactivity in the rat parabrachial nucleus after nociceptive stimulation

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