Behavioral and electrophysiological evidence of pain inhibition from midbrain stimulation in the cat

Olivéras, Jean-Louis; Besson, Jean‐Marie; Guilbaud, G.; Liebeskind, John C.

doi:10.1007/bf00239016

Cited by 382 publications

(63 citation statements)

References 35 publications

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“…These procedures include systemic and intrathecal morphine administration, dorsal column stimulation, transcutaneous electrical stimulation, stimulation of periaqueductal, periventricular and thalamic structures and heterotopic noxious stimulation. (ii) Secondly, these cells are strongly modulated by supraspinal structures; in particular electrical stimulation of the PAG induces marked inhibitory effects on dorsal horn convergent neurones (Guilbaud et al, 1972;Liebeskind et al, 1973;Oliveras et al, 1974;Duggan & Griersmith, 1979;Hayes et al, 1979;Carstens et al, 1980;Yezierski et al, 1982). Thus this type of neurone appears appropriate for an effect to be found following PAG morphine.…”

Section: Introductionmentioning

confidence: 99%

Lack of evidence for increased descending inhibition on the dorsal horn of the rat following periaqueductal grey morphine microinjections

Dickenson

Bars

1987

British J Pharmacology

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1 Recordings were made from 18 neurones in the dorsal horn of the rat, anaesthetized with halothane. All cells received A-and C-fibre inputs and responded to innocuous and noxious stimuli applied to their excitatory receptive fields located on the extremity of the ipsilateral hindpaw. Transcutaneous application of suprathreshold (mean 3.2T) 2 ms square-wave pulses to the centre of the receptive fields resulted in responses to A-and C-fibre activation being observed; a mean 32.4 ± 6.0 C-fibre latency spikes were evoked per stimulus.2 A high dose (20 pg) of morphine in 0.5 pli sterile saline, microinjected into the periaqueductal grey matter (PAG) had no effect on the C-fibre-evoked activity of thirteen cells (72%) and facilitated 5 neurones (28%). Microinjection sites covered most of the PAG particularly the caudal medioventral zone.3 A relatively high dose (6 mg kg-', i.v.) of systemic morphine chloride, sufficient to elicit the direct spinal action of the opiate, inhibited all 5 cells tested. 4 We conclude that there is little evidence that the supraspinal action of morphine includes increased descending controls and depression of dorsal horn neurones in the rat.

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Section: Introductionmentioning

confidence: 99%

Lack of evidence for increased descending inhibition on the dorsal horn of the rat following periaqueductal grey morphine microinjections

Dickenson

Bars

1987

British J Pharmacology

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“…Electrical stimulation of the PAG in man produces analgesia (Hosobuchi et al, 1977;Richardson and Akil, 1977) and inhibits responses to noxious stimuli in rats, cats, and monkeys (Reynolds, 1969;Mayer and Liebeskind, 1974;Oliveras et al 1974; Lewis and Gebhart, 1977;Gebhart and Toleikis, 1978;Hayes et al, 1979). The PAG has relatively high concentrations of opiate binding sites (Atweh and Kuhar, 1977), as well as of endogenous opioid peptides (Uhl et al, 1977;Sar et al, 1978;Finley et al, 1981a;Moss et al, 1983) and direct injection of opiate agonists into the PAG suppresses behavioral and neuronal responses to noxious stimulation (Liebeskind et al, 1973;Jacquet and Lajtha, 1976;Lewis and Gebhart, 1977;Yeung et al, 1977;Yaksh and Rudy, 1978;Bennett and Mayer, 1979;Cheng et al, 1986).…”

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confidence: 99%

Evidence for two classes of nociceptive modulating neurons in the periaqueductal gray

Heinricher¹,

Cheng²,

Fields³

1987

J. Neurosci.

111

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The midbrain periaqueductal gray (PAG) and the rostral ventromedial medulla (RVM) are important links in a neuronal network that modulates nociceptive transmission. In the RVM, 2 classes of cells have been identified that show changes in activity at the time of the tail-flick response (TF) elicited by noxious heat (Fields et al., 1983a). We now report that neurons in the PAG region also show changes in activity related to TF. Extracellular recordings were made from the PAG and the ventrally adjacent tegmentum at sites from which it was possible to inhibit TF using stimulating currents of 10 microA or less. Cell activity, time of TF occurrence, and tail temperature were recorded during 5 repetitions of the heat stimulus. Periresponse and peristimulus histograms were plotted with reference to the TF and tail temperature, respectively. A significant number of neurons in the PAG region showed changes in activity that preceded the TF. “Midbrain On- cells” (13.6% of the sample) displayed an abrupt increase in firing just prior to the TF. “Midbrain Off-cells” (4.4%) paused just prior to the TF. The remaining neurons (241 of 294, or 82%) did not exhibit changes in firing prior to the TF. Thus, cells with changes in activity related to the TF are present in the PAG region as well as in the RVM. The PAG has a large projection to the RVM, and microinjection of morphine in the PAG increases activity of RVM Off-cells and decreases that of RVM On-cells.(ABSTRACT TRUNCATED AT 250 WORDS)

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“…During the past year a nonpituitary, brain fl-endorphin system has been described (18)(19)(20). This system also exhibits j3-lipotropin immunoreactivity (21,22) and corticotropin (ACTH)-like immunoreactivity (20,23), suggesting the existence in brain of the common 31,000 molecular weight precursor of (3-lipotropin/corticotropin that has been described in pituitary (24,25 Electrical stimulation of the brain has been shown to elicit analgesia in rat (26) and cat (27). This analgesia bears many of the characteristics of opiate action, including partial reversal with the opiate antagonist naloxone (28)(29)(30) and the development of tolerance to and cross-tolerance with morphine (31).…”

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confidence: 99%

Appearance of beta-endorphin-like immunoreactivity in human ventricular cerebrospinal fluid upon analgesic electrical stimulation.

Akil¹,

Richardson²,

Barchas³

et al. 1978

Proc. Natl. Acad. Sci. U.S.A.

150

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jt-Endorphin-like immunoreactivity in human ventricular cerebrospinal fluid was measured with a specific radioimmunoassay. The subjects were undergoing a surgical procedure for relief of chronic intractable pain. This procedure involved the focal stimulation of a medial thalamic site adjacent to the wall of the third ventricle. Samples were collected before and during the analgesic stimulation. No f-endorphin-like immunoreactivity could be detected prior to stimulation, suggesting that baseline levels are below 25 fmol/ml of cerebrospinal fluid. Electrical stimulation led to substantial increases (13-to 20-fold) in immunoreactive material in every subject. These results suggest that ,kendorphin-like material can be released into the ventricular system and may contribute to the pain blockade that results from periventricular stimulation.The isolation and characterization of f3-endorphin from camel (1), sheep (2), and human (2, 3) pituitaries rapidly led to its identification as an endogenous opioid (1-4). Administration of this 31-amino-acid peptide to laboratory animals results in phenomena like those associated with opiates, including naloxone-reversible analgesia (5-10), tolerance (8-11), and dependence (8,11 Electrical stimulation of the brain has been shown to elicit analgesia in rat (26) and cat (27). This analgesia bears many of the characteristics of opiate action, including partial reversal with the opiate antagonist naloxone (28-30) and the development of tolerance to and cross-tolerance with morphine (31). However, these effects are only partial, suggesting a role of nonopiate as well as opiate mechanisms in this method of pain control. This work has been extended to the human clinical situation. Patients suffering from chronic intractable pain derive long-term relief from the stimulation of medial thalamic and periaqueductal sites (32,33). Stimulation of a site in the vicinity of the posterior commissure, immediately adjacent to the ventricular wall at the level of the nucleus parafascicularis, has been found to combine excellent analgetic effectiveness with minimal side effects. The characteristics of the pain relief obtained from such stimulation have been described (32,33). This stimulation-induced analgesia in man also appears to have an opioid component, because it has been shown to be naloxone reversible (34, 35) and to be accompanied by a rise in enkephalin-like opioid material in the cerebrospinal fluid (CSF) (36). Because the stimulation site in humans is homologous to a region in rodents particularly rich in (3-endorphin activity, we have examined the effect of its stimulation on (3-endorphin immunoreactivity in CSF. The publication costs of this article were defrayed in part by page charge payment. This article must therefore be hereby marked "advertisement" in accordance with 18 U. S. C. §1734 solely to indicate this fact. METHODS

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Behavioral and electrophysiological evidence of pain inhibition from midbrain stimulation in the cat

Cited by 382 publications

References 35 publications

Lack of evidence for increased descending inhibition on the dorsal horn of the rat following periaqueductal grey morphine microinjections

Lack of evidence for increased descending inhibition on the dorsal horn of the rat following periaqueductal grey morphine microinjections

Evidence for two classes of nociceptive modulating neurons in the periaqueductal gray

Appearance of beta-endorphin-like immunoreactivity in human ventricular cerebrospinal fluid upon analgesic electrical stimulation.

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