Action of capsaicin on dorsal root-evoked synaptic transmission to substantia gelatinosa neurons in adult rat spinal cord slices

Yang, Kun; Kumamoto, Eiichi; Furue, Hidemasa; Li, Yunqing; Yoshimura, Michihiro

doi:10.1016/s0006-8993(99)01408-0

Cited by 84 publications

(73 citation statements)

References 27 publications

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“…An inactivating, VR1-mediated inward current is observed in a subset of NTS neurons and could contribute to the eventual diminution of responses evoked after stimulating the NTS. Thus, VR1 activation could facilitate spontaneous glutamate or GABA release by acting at presynaptic receptors, while reducing action potential-evoked responses via a depolarization block (Katz and Miledi, 1969) or partial depletion of the calciumdependent, readily releasable vesicle pool in the terminal (Yang et al, 1999;Li et al, 2004). The heterogeneous nature of the axons activated by electrical stimulation of the NTS may also contribute to the change in evoked response over time, which could include VR1-mediated release of a different modulator substance (e.g., a neuropeptide) that secondarily enhances GABA release.…”

Section: Discussionmentioning

confidence: 99%

Vanilloid-Mediated Heterosynaptic Facilitation of Inhibitory Synaptic Input to Neurons of the Rat Dorsal Motor Nucleus of the Vagus

Derbenev

Monroe²,

Glatzer³

et al. 2006

J. Neurosci.

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Vanilloid type-1 receptors (VR1) are abundant in the dorsal vagal complex, where their function is mostly unknown. We examined the role of VR1 in regulating synaptic inputs to neurons of the dorsal motor nucleus of the vagus (DMV). Using patch-clamp recordings from DMV neurons in brainstem slices, capsaicin was found to increase action potential-independent inhibitory input onto DMV neurons. This rapid effect was mimicked by application of the endogenous cannabinoid, anandamide and blocked by VR1 antagonists. The VR1-mediated facilitation of synaptic inhibition was reduced by ionotropic and metabotropic glutamate receptor antagonists, suggesting an indirect, heterosynaptic enhancement of GABA release caused by a VR1-mediated increase in glutamate release from presynaptic terminals of excitatory neurons. Application of L-glutamate also increased GABA release. The paired-pulse ratio was increased for IPSCs evoked after electrical stimulation of the nucleus tractus solitarius, but the effect was slower than for the enhancement of spontaneous and miniature IPSCs. Capsaicin also increased the frequency of glutamatergic postsynaptic currents in a VR1-mediated manner. Results of these studies suggest that VR1-containing glutamatergic terminals contact DMV neurons. Activation of VR1 potently enhances glutamate release onto GABAergic terminals, facilitating GABA release. Endogenous cannabinoids can thereby rapidly enhance inhibitory input to DMV neurons via VR1-mediated presynaptic mechanisms.

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Section: Discussionmentioning

confidence: 99%

Vanilloid-Mediated Heterosynaptic Facilitation of Inhibitory Synaptic Input to Neurons of the Rat Dorsal Motor Nucleus of the Vagus

Derbenev

Monroe²,

Glatzer³

et al. 2006

J. Neurosci.

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“…This pattern in NTS appears to differ from the more mixed case for primary afferent processing in the spinal cord. In the spinal cord, C-and A-fiber terminals often converge on the same dorsal horn neurons (Yang et al, 1999). One third or more dorsal root neurons, the source for those dorsal horn afferent terminals, respond to both CAP and ATP , although proportions vary across reports (Oh et al, 2001;Petruska et al, 2002;Labrakakis et al, 2003).…”

Section: Vr1 and P2x Receptors Facilitate Glutamate Release Onto Diffmentioning

confidence: 99%

Purinergic and Vanilloid Receptor Activation Releases Glutamate from Separate Cranial Afferent Terminals in Nucleus Tractus Solitarius

Jin¹,

Bailey²,

Li³

et al. 2004

J. Neurosci.

167

162

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“…At this stimulation intensity, both myelinated and unmyelinated afferent fibers are activated (Yang et al 1999;Nishi 1993, 1995). The conduction velocity of the stimulated fibers was not measured in this study because the attached dorsal root was very short in the thin spinal cord slice preparations.…”

Section: Recordings Of Postsynaptic Currents Of Neurons In Lamina II mentioning

confidence: 99%

“…Recordings were abandoned if the access resistance was Ͼ30 M⍀ and the input resistance changed Ͼ15%. To determine the synaptic input from capsaicin-sensitive fibers to lamina II o and II i neurons, the effect of 1 M capsaicin on mEPSCs was tested (Yang et al 1999). After recording the mEPSCs of neurons in lamina II o or II i for 3 min as the control, 1 M capsaicin was perfused into the slice for 1 min.…”

Section: Experimental Protocolsmentioning

confidence: 99%

Primary Afferent Stimulation Differentially Potentiates Excitatory and Inhibitory Inputs to Spinal Lamina II Outer and Inner Neurons

Pan

Pan²

2004

Journal of Neurophysiology

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Pan, Yu-Zhen and Hui-Lin Pan. Primary afferent stimulation differentially potentiates excitatory and inhibitory inputs to spinal lamina II outer and inner neurons. J Neurophysiol 91: 2413-2421, 2004. First published January 28, 2004 10.1152/jn.01242.2003. Spinal lamina II (substantia gelatinosa) neurons play an important role in processing of nociceptive information from primary afferent nerves. Anatomical studies suggest that neurons in the outer (lamina II o ) and inner (lamina II i ) zone of lamina II receive distinct afferent inputs. The functional significance of this preferential afferent termination in lamina II remains unclear. In this study, we examined the differential synaptic inputs to neurons in lamina II o and II i in response to primary afferent stimulation. Whole cell voltage-clamp recordings were performed on neurons in lamina II o and II i of the rat spinal cord slice under visual guidance. Capsaicin (1 M) significantly increased the frequency of glutamatergic miniature excitatory postsynaptic currents (mEPSCs) in all 27 lamina II o neurons and significantly increased the amplitude of mEPSCs in 12 of 27 lamina II o neurons. However, capsaicin only significantly increased the frequency of mEPSCs in 9 of 22 (40.9%) lamina II i neurons and increased the amplitude of mEPSCs in 6 of these 9 neurons. Furthermore, the peak amplitude of EPSCs, evoked by electrical stimulation of the attached dorsal root, in 40 lamina II o neurons was significantly greater than that [160.5 Ϯ 16.7 vs. 87.0 Ϯ 10.4 (SE) pA] in 37 lamina II i neurons. On the other hand, the peak amplitude of evoked inhibitory postsynaptic currents (IPSCs) in 40 lamina II o neurons was significantly smaller than that (103.1 Ϯ 11.6 vs. 258.4 Ϯ 24.4 pA) in 37 lamina II i neurons. In addition, the peak amplitudes of both EPSCs and IPSCs, evoked by direct stimulation of lamina II, were similar in lamina II o and II i neurons. This study provides new information that stimulation of primary afferents differentially potentiates synaptic inputs to neurons in lamina II o and II i . The quantitative difference in excitatory and inhibitory synaptic inputs to lamina II o and II i neurons may be important for integration of sensory information from primary afferent nerves. I N T R O D U C T I O NLamina II (substantia gelatinosa) of the spinal cord dorsal horn is a critical site for the relay and processing of primary afferent information (Cervero and Iggo 1980; Light and Perl 1979a;Ralston and Ralston 1979;Woolf and Fitzgerald 1983). With a high density of small interneurons and mostly unmyelinated and thinly myelinated primary afferent terminals, lamina II appears to be a heterogenous region both structurally and functionally. Anatomical studies have divided lamina II into two general subdivisions: an outer lamina II (lamina II o ) with small cells and unmyelinated C-fiber terminals and an inner lamina II (lamina II i ) with slightly larger neurons and predominately thinly myelinated A-fiber endings (Light and Perl 1979a,b;Woodbury et al. 2000). Lam...

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Action of capsaicin on dorsal root-evoked synaptic transmission to substantia gelatinosa neurons in adult rat spinal cord slices

Cited by 84 publications

References 27 publications

Vanilloid-Mediated Heterosynaptic Facilitation of Inhibitory Synaptic Input to Neurons of the Rat Dorsal Motor Nucleus of the Vagus

Vanilloid-Mediated Heterosynaptic Facilitation of Inhibitory Synaptic Input to Neurons of the Rat Dorsal Motor Nucleus of the Vagus

Purinergic and Vanilloid Receptor Activation Releases Glutamate from Separate Cranial Afferent Terminals in Nucleus Tractus Solitarius

Primary Afferent Stimulation Differentially Potentiates Excitatory and Inhibitory Inputs to Spinal Lamina II Outer and Inner Neurons

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