Skip to main content
Top
Published in: Neurological Sciences 2/2012

01-04-2012 | Brief Communication

A possible synaptic configuration underlying coeruleospinal inhibition of visceral nociceptive transmission in the rat

Authors: Bunsho Hayashi, Masayoshi Tsuruoka, Masako Maeda, Junichiro Tamaki, Tomio Inoue

Published in: Neurological Sciences | Issue 2/2012

Login to get access

Abstract

A synaptic arrangement underlying descending inhibition from the locus coeruleus/subcoeruleus (LC/SC) on visceral nociceptive transmission in the spinal cord was investigated in the anesthetized rat. Extracellular recordings were made from the L6-S2 segmental level using a carbon filament glass microelectrode (4–6 MΩ). Colorectal distention (CRD) was produced by inflating a balloon inside the descending colon and rectum. All neurons tested responded to both CRD and to cutaneous pinch (a force of 613 g/mm2), indicating that nociceptive signals from visceral organs and nociceptive signals from the cutaneous receptive field converge on a single neuron. These neurons were divided into two groups based on their response to CRD: short latency-abrupt and short latency-sustained neurons. Electrical stimulation of the LC/SC (30 or 50 μA, 100 Hz, 0.1 ms pulses) inhibited both CRD-evoked and cutaneous pinch-evoked responses in short latency-abrupt and short latency-sustained neurons. When graded CRD (20, 40, 60, and 80 mmHg) was delivered, LC/SC stimulation produced a reduction in slope of the linear CRD intensity-response magnitude curve without a change in the response threshold in both short latency-abrupt (n = 42) and short latency-sustained neurons (n = 11). This result suggests that coeruleospinal inhibition of visceral nociceptive transmission is due to a synaptic configuration in which inhibitory and excitatory terminals are in close spatial proximity, including presynaptic inhibition.
Literature
1.
go back to reference Al-Chaer ED, Feng Y, Willis WD (1999) Comparative study of viscerosomatic input onto postsynaptic dorsal column and spinothalamic tract neurons in the primate. J Neurophysiol 82:1876–1882PubMed Al-Chaer ED, Feng Y, Willis WD (1999) Comparative study of viscerosomatic input onto postsynaptic dorsal column and spinothalamic tract neurons in the primate. J Neurophysiol 82:1876–1882PubMed
2.
go back to reference Al-Chaer ED, Lawand NB, Westlund KN, Willis WD (1996) Pelvic visceral input into the nucleus gracilis is largely mediated by the postsynaptic dorsal column pathway. J Neurophysiol 76:2675–2690PubMed Al-Chaer ED, Lawand NB, Westlund KN, Willis WD (1996) Pelvic visceral input into the nucleus gracilis is largely mediated by the postsynaptic dorsal column pathway. J Neurophysiol 76:2675–2690PubMed
3.
go back to reference Carstens E, Klumpp D, Zimmermann M (1980) Differential inhibitory effects of medial and lateral midbrain stimulation on spinal neuronal discharges to noxious skin heating in the cat. J Neurophysiol 43:242–332 Carstens E, Klumpp D, Zimmermann M (1980) Differential inhibitory effects of medial and lateral midbrain stimulation on spinal neuronal discharges to noxious skin heating in the cat. J Neurophysiol 43:242–332
4.
go back to reference Carstens E, Yokota T, Zimmermann M (1979) Inhibition of spinal neuronal responses to noxious skin heating by stimulation of the mesencephalic periaqueductal gray in the cat. J Neurophysiol 42:558–568PubMed Carstens E, Yokota T, Zimmermann M (1979) Inhibition of spinal neuronal responses to noxious skin heating by stimulation of the mesencephalic periaqueductal gray in the cat. J Neurophysiol 42:558–568PubMed
5.
go back to reference Furue H, Sonohara M, Ito A, Kawasaki Y, Baba H, Yoshimura M (2003) In vivo patch-clamp analysis of norepinephrine effects on nociceptive transmission in substantia gelatinosa neurons of the rat spinal cord. Proc 10th World Congress Pain 24:245–250 Furue H, Sonohara M, Ito A, Kawasaki Y, Baba H, Yoshimura M (2003) In vivo patch-clamp analysis of norepinephrine effects on nociceptive transmission in substantia gelatinosa neurons of the rat spinal cord. Proc 10th World Congress Pain 24:245–250
7.
go back to reference Jone S, Gebhar GF (1988) Inhibition of spinal nociceptive transmission from the midbrain, pons and medulla in the rat: activation of descending inhibition by morphine, glutamate and electrical stimulation. Brain Res 460:281–296CrossRef Jone S, Gebhar GF (1988) Inhibition of spinal nociceptive transmission from the midbrain, pons and medulla in the rat: activation of descending inhibition by morphine, glutamate and electrical stimulation. Brain Res 460:281–296CrossRef
8.
go back to reference Kawasaki Y, Kumamoto E, Furue H, Yoshimura M (2003) Alpha2 adorenoceptor-mediated presynaptic inhibition of primary afferent glumatergic transmission in rat substantia gelatinosa neurons. Anesthesiology 98:682–689PubMedCrossRef Kawasaki Y, Kumamoto E, Furue H, Yoshimura M (2003) Alpha2 adorenoceptor-mediated presynaptic inhibition of primary afferent glumatergic transmission in rat substantia gelatinosa neurons. Anesthesiology 98:682–689PubMedCrossRef
9.
go back to reference Liu L, Tsuruoka M, Maeda M, Hayashi B, Inoue T (2007) Coerulespinal inhibition of visceral nociceptive processing in the rat spinal cord. Neurosci Lett 426:139–144PubMedCrossRef Liu L, Tsuruoka M, Maeda M, Hayashi B, Inoue T (2007) Coerulespinal inhibition of visceral nociceptive processing in the rat spinal cord. Neurosci Lett 426:139–144PubMedCrossRef
10.
go back to reference Ness TJ (2000) Evidence for ascending visceral nociceptive information in the dorsal midline and lateral spinal cord. Pain 87:83–88PubMedCrossRef Ness TJ (2000) Evidence for ascending visceral nociceptive information in the dorsal midline and lateral spinal cord. Pain 87:83–88PubMedCrossRef
11.
go back to reference Ness TJ, Gebhar GF (1988) Colorectal distention as a noxious visceral stimulus: physiologicic and pharmacologic characterization of pseudaffective reflexes in the rat. Brain Res 450:153–169PubMedCrossRef Ness TJ, Gebhar GF (1988) Colorectal distention as a noxious visceral stimulus: physiologicic and pharmacologic characterization of pseudaffective reflexes in the rat. Brain Res 450:153–169PubMedCrossRef
12.
go back to reference Palecek J, Paleckova V, Willis WD (2002) The role of pathways in the spinal cord lateral and dorsal funiculi in signaling nociceptive somatic and visceral stimuli in rats. Pain 96:297–307PubMedCrossRef Palecek J, Paleckova V, Willis WD (2002) The role of pathways in the spinal cord lateral and dorsal funiculi in signaling nociceptive somatic and visceral stimuli in rats. Pain 96:297–307PubMedCrossRef
13.
go back to reference Palecek J, Paleckova V, Willis WD (2003) Fos expression in spinothalamic and postsynaptic dorsal column neurons following noxious visceral and cutaneous stimuli. Pain 104:249–257PubMedCrossRef Palecek J, Paleckova V, Willis WD (2003) Fos expression in spinothalamic and postsynaptic dorsal column neurons following noxious visceral and cutaneous stimuli. Pain 104:249–257PubMedCrossRef
14.
go back to reference Paxinos G, Watson C (1998) The rat brain in stereotaxic coodinates. Academic Press, New York Paxinos G, Watson C (1998) The rat brain in stereotaxic coodinates. Academic Press, New York
15.
go back to reference Proudfit HK, Clark FM (1991) The projections of locus coeruleus neurons to the spinal cord. Prog Brain Res 85:123–141CrossRef Proudfit HK, Clark FM (1991) The projections of locus coeruleus neurons to the spinal cord. Prog Brain Res 85:123–141CrossRef
16.
go back to reference Sonohara M, Furue H, Katafuchi T, Yasaka T, Doi A, Kumamoto E et al (2004) Actions of noradorenaline on substantia gelatinosa neurons in the rat spinal cord revealed by in vivo patchi recording. J Physiol 555:515–526CrossRef Sonohara M, Furue H, Katafuchi T, Yasaka T, Doi A, Kumamoto E et al (2004) Actions of noradorenaline on substantia gelatinosa neurons in the rat spinal cord revealed by in vivo patchi recording. J Physiol 555:515–526CrossRef
17.
go back to reference Tsuruoka M, Maeda M, Nagasawa I, Inoue T (2004) Spinal pathways mediating coeruleospinal antinociception in the rat. Neurosci Lett 362:236–239PubMedCrossRef Tsuruoka M, Maeda M, Nagasawa I, Inoue T (2004) Spinal pathways mediating coeruleospinal antinociception in the rat. Neurosci Lett 362:236–239PubMedCrossRef
18.
go back to reference Tsuruoka M, Matsutani K, Inoue T (2003) Coeruleospinal inhibition of nociceptive processing in the dorsal horn during unilateral hindpaw inflammation in the rat. Pain 104:353–361PubMedCrossRef Tsuruoka M, Matsutani K, Inoue T (2003) Coeruleospinal inhibition of nociceptive processing in the dorsal horn during unilateral hindpaw inflammation in the rat. Pain 104:353–361PubMedCrossRef
19.
go back to reference Tsuruoka M, Matsutani K, Maeda M, Inoue T (2003) Coeruleotrigeminal inhibition of nociceptive processing in the rat trigeminal subnucleus caudalis. Brain Res 993:146–153PubMedCrossRef Tsuruoka M, Matsutani K, Maeda M, Inoue T (2003) Coeruleotrigeminal inhibition of nociceptive processing in the rat trigeminal subnucleus caudalis. Brain Res 993:146–153PubMedCrossRef
20.
go back to reference Zimmermann M (1983) Ethical guidelines for investigation of experimental pain in conscious animals. Pain 16:109–110PubMedCrossRef Zimmermann M (1983) Ethical guidelines for investigation of experimental pain in conscious animals. Pain 16:109–110PubMedCrossRef
Metadata
Title
A possible synaptic configuration underlying coeruleospinal inhibition of visceral nociceptive transmission in the rat
Authors
Bunsho Hayashi
Masayoshi Tsuruoka
Masako Maeda
Junichiro Tamaki
Tomio Inoue
Publication date
01-04-2012
Publisher
Springer Milan
Published in
Neurological Sciences / Issue 2/2012
Print ISSN: 1590-1874
Electronic ISSN: 1590-3478
DOI
https://doi.org/10.1007/s10072-011-0739-5

Other articles of this Issue 2/2012

Neurological Sciences 2/2012 Go to the issue