Noxious and tactile input to medial structures of midbrain and pons in the rat

Eickhoff, René; Handwerker, H. O.; McQueen, Daniel S.; Schick, E.

doi:10.1016/0304-3959(78)90032-5

Cited by 52 publications

(11 citation statements)

References 27 publications

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“…We confirmed that the vlPAG contains three distinct subpopulations of neurons that respond to noxious thermal stimuli applied to the paw. Thus, excitatory or “vlPAG on ,” inhibitory or “vlPAG off ,” and neutral or “vlPAG neutral ” neurons were observed in our unanesthetized rats, as seen previously in lightly anesthetized rats, although the percentage of neurons that were responsive to painful stimuli was higher in the unanesthetized animals [14; 19; 21; 53]. The majority of PAG neurons responded to noxious thermal stimuli with either increases or decreases of neuronal firing, and the firing patterns returned to spontaneous levels after termination of the stimuli.…”

Section: Discussionsupporting

confidence: 82%

Neuropathic pain-induced enhancement of spontaneous and pain-evoked neuronal activity in the periaqueductal gray that is attenuated by gabapentin

Samineni

Premkumar

Faingold

2017

Pain

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Neuropathic pain is a debilitating pathological condition that is poorly understood. Recent evidence suggests that abnormal central processing occurs during the development of neuropathic pain induced by the cancer chemotherapeutic agent, paclitaxel. Yet, it is unclear what role neurons in supraspinal pain network sites, such as the periaqueductal gray, play in altered behavioral sensitivity seen during chronic pain conditions. To elucidate these mechanisms, we studied the spontaneous and thermally-evoked firing patterns of ventrolateral periaqueductal gray (vlPAG) neurons in awake behaving rats treated with paclitaxel to induce neuropathic pain. In the present study vlPAG neurons in naive rats exhibited either excitatory, inhibitory or neutral responses to noxious thermal stimuli, as previously observed. However, after development of behavioral hypersensitivity induced by the chemotherapeutic agent, paclitaxel, vlPAG neurons displayed increased neuronal activity and changes in thermal pain-evoked neuronal activity. This involved elevated levels of spontaneous firing and heightened responsiveness to non-noxious stimuli (allodynia) as well as noxious thermal stimuli (hyperalgesia) as compared to controls. Furthermore, after paclitaxel treatment only excitatory neuronal responses were observed to both non-noxious and noxious thermal stimuli. Systemic administration of gabapentin, a non-opioid analgesic, induced significant dose-dependent decreases in the elevated spontaneous and thermally-evoked vlPAG neuronal firing to both non-noxious and noxious thermal stimuli in rats exhibiting neuropathic pain but not in naïve rats. Thus, these results show a strong correlation between behavioral hypersensitivity to thermal stimuli and increased firing of vlPAG neurons in allodynia and hyperalgesia that occur in this neuropathic pain model.

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Section: Discussionsupporting

confidence: 82%

Neuropathic pain-induced enhancement of spontaneous and pain-evoked neuronal activity in the periaqueductal gray that is attenuated by gabapentin

Samineni

Premkumar

Faingold

2017

Pain

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“…Twenty percent were maximally excited by non-noxious stimulation, and none responded exclusively to noxious stimuli. The findings of Eickhoff et al (1978) in the chloralose-anesthetized rat were similar. They studied neurons in the PAG and adjacent reticular formation that were responsive to electrical stimulation of the coccygeal nerve.…”

Section: Discussionsupporting

confidence: 55%

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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“…For example, input from the hindlimbs (lumbar enlargement) specifically targets the caudal lPAG a region whose excitation evokes flight and escape, whereas selective input from face (Sp5) and forelimbs (cervical enlargement) targets the more rostral part of the lPAG column excitation of which evokes confrontation and threat, intense facio-vocal activity, biting, and occasionally striking with the forelimbs. Although the physiological characteristics of lamina I neurons that project to lPAG have yet to be systematically studied, lamina I neurons activated antidromically from the cuneiform/PAG region are strongly driven by cutaneous noxious manipulation (noxious pinch, radiant heat) (Menétrey et al, 1980;Hylden et al, 1986), and responses to cutaneous noxious stimuli have been recorded also in what appears to correspond to the lPAG column (Eickhoff et al, 1978;Rose, 1979). More recently, cutaneous noxious stimulation has been found to evoke preferential Fos-like IR in the lPAG column (Keay and Bandler, 1993;Keay et al, 1992).…”

Section: Functional Considerationsmentioning

confidence: 96%

Spinal afferents to functionally distinct periaqueductal gray columns in the rat: An anterograde and retrograde tracing study

et al. 1997

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The segmental and laminar organization of spinal projections to the functionally distinct ventrolateral (vlPAG) and lateral periaqueductal gray (lPAG) columns was examined by using retrograde and anterograde tracing techniques. It was found 1) that spinal input to both vlPAG and lPAG columns arose predominantly from neurons in the upper cervical (C1-4) and sacral spinal cord; 2) that there was a topographical separation of vl-PAG projecting and lPAG-projecting neurons within the upper cervical spinal cord; but 3) that below spinal segment C4, vlPAG-projecting and lPAG-projecting spinal neurons were similarly distributed, predominantly within contralateral lamina I, the nucleus of the dorsolateral fasciculus (the lateral spinal nucleus) and the lateral (reticular) part of lamina V. Consistent with the retrograde results, the greatest density of anterograde label, within both the vlPAG and lPAG, was found after tracer injections made either in the superficial or deep dorsal horn of the upper cervical spinal cord. Tracer injections made within the thoraco-lumbar spinal cord revealed that the vlPAG column received a convergent input from both the superficial and deep dorsal horn. However, thoraco-lumbar input to the lPAG was found to arise uniquely from the superficial dorsal horn; whereas the deep dorsal horn was found to innervate the "juxta-aqueductal" PAG region rather than projecting to the lPAG. These findings suggest that similar to spino-parabrachial projections, spinal projections to the lPAG (and juxta-aqueductal PAG) are topographically organised, with distinct subgroups of spinal neurons projecting to specific lPAG or juxta-aqueductal PAG subregions. In contrast, the vlPAG receives a convergent spinal input which arises from the superficial and deep dorsal horn of cervical, thoracic, lumbar, and sacral spinal segments.

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Noxious and tactile input to medial structures of midbrain and pons in the rat

Cited by 52 publications

References 27 publications

Neuropathic pain-induced enhancement of spontaneous and pain-evoked neuronal activity in the periaqueductal gray that is attenuated by gabapentin

Neuropathic pain-induced enhancement of spontaneous and pain-evoked neuronal activity in the periaqueductal gray that is attenuated by gabapentin

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

Spinal afferents to functionally distinct periaqueductal gray columns in the rat: An anterograde and retrograde tracing study

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