Comparison of Responses of Primate Spinothalamic Tract Neurons to Pruritic and Algogenic Stimuli

Simone, Donald A.; Zhang, Xijing; Li, Jun; Zhang, Jintao; Honda, Christopher N.; LaMotte, Robert H.; Giesler, Glenn J.

doi:10.1152/jn.00527.2003

Cited by 85 publications

(72 citation statements)

References 32 publications

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“…Also consistent with these latter reports, the majority of 5-HTsensitive Vc units were presently categorized as WDR or NS, with a small percentage being mechanically insensitive. Importantly, the vast majority of 5-HT-responsive units additionally responded to the algogens AITC and capsaicin (Table 3), consistent with previous studies from our laboratory as well as studies of histamine-or cowhage-sensitive primate spinothalamic tract neurons that always also responded to capsaicin (Davidson et al 2007;Simone et al 2004).…”

Section: Discussionsupporting

confidence: 86%

“…These data support the concept of a labeled line for itch. However, the vast majority of spinal neurons that respond to cutaneous application of pruritogens such as histamine, 5-HT, or cowhage spicules (containing itch-inducing proteases; Reddy et al 2008) also responded to capsaicin and/or allyl isothiocyanate (AITC) (Akiyama et al 2009a(Akiyama et al , 2009bDavidson et al 2007;Jinks and Carstens 2002;Simone et al 2004). Behavioralgenetic studies also indicate that nociceptive neurons may be capable of signaling itch (Imamachi et al 2009;Shim et al 2007), arguing against labeled-line coding for itch versus pain.…”

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confidence: 99%

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Facial injections of pruritogens or algogens elicit distinct behavior responses in rats and excite overlapping populations of primary sensory and trigeminal subnucleus caudalis neurons

Klein

Carstens

2011

Journal of Neurophysiology

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Klein A, Carstens MI, Carstens E. Facial injections of pruritogens or algogens elicit distinct behavior responses in rats and excite overlapping populations of primary sensory and trigeminal subnucleus caudalis neurons. J Neurophysiol 106: 1078 -1088. First published June 8, 2011 doi:10.1152/jn.00302.2011In the present study, we investigated whether intradermal cheek injection of pruritogens or algogens differentially elicits hindlimb scratches or forelimb wipes in Sprague-Dawley rats, as recently reported in mice. We also investigated responses of primary sensory trigeminal ganglion (TG) and dorsal root ganglion (DRG) cells, as well as second-order neurons in trigeminal subnucleus caudalis (Vc), to pruritic and algesic stimuli. 5-HT was the most effective chemical to elicit dose-dependent bouts of hindlimb scratches directed to the cheek, with significantly less forelimb wiping, consistent with itch. Chloroquine also elicited significant scratching but not wiping. Allyl isothiocyanate (AITC; mustard oil) elicited dose-dependent wiping with no significant scratching. Capsaicin elicited equivalent numbers of scratch bouts and wipes, suggesting a mixed itch and pain sensation. By calcium imaging, ϳ6% of cultured TG and DRG cells responded to 5-HT. The majority of 5-HT-sensitive cells also responded to chloroquine, AITC, and/or capsaicin, and one-third responded to histamine. Using a chemical search strategy, we identified single units in Vc that responded to intradermal cheek injection of 5-HT. Most were wide dynamic range (WDR) or nociceptive specific (NS), and a few were mechanically insensitive. The large majority additionally responded to AITC and/or capsaicin and thus were not pruritogen selective. These results suggest that primary and second-order neurons responsive to pruritogens and algogens may utilize a population coding mechanism to distinguish between itch and pain, sensations that are behaviorally manifested by distinct hindlimb scratching and forelimb wiping responses.

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Section: Discussionsupporting

confidence: 86%

mentioning

confidence: 99%

Facial injections of pruritogens or algogens elicit distinct behavior responses in rats and excite overlapping populations of primary sensory and trigeminal subnucleus caudalis neurons

Klein

Carstens

2011

Journal of Neurophysiology

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“…Neurophysiological studies in cats and monkeys have shown that thermoreceptive and nociceptive spinothalamic tract (STT) neurons in the MZ project to the ventral posterior lateral nucleus (VPL) (Willis et al, 1974;Price et al, 1978;Ferrington et al, 1987;Craig and Dostrovsky, 2001;Simone et al, 2004). However, this projection has remained unexplored in the rat.…”

Section: Introductionmentioning

confidence: 99%

Thermally Identified Subgroups of Marginal Zone Neurons Project to Distinct Regions of the Ventral Posterior Lateral Nucleus in Rats

Zhang¹,

Davidson²,

Giesler³

2006

J. Neurosci.

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Spinal marginal zone (MZ) neurons play a crucial role in the transmission of nociceptive and thermoreceptive information to the brain. The precise areas to which physiologically characterized MZ neurons project in the ventral posterior lateral (VPL) nucleus of the thalamus have not been clearly established. Here, we examine this projection in rats using the method of antidromic activation to map the axon terminals of neurons recorded from the MZ. Thirty-three neurons were antidromically activated using pulses of Յ30 A in the contralateral VPL. In every case, the most rostral point from which the MZ neuron could be antidromically activated was surrounded by stimulating tracks in which large-amplitude current pulses failed to activate the examined neuron, indicating the termination of the spinothalamic tract (STT) axon. Each of 30 examined neurons responded to noxious but not innocuous mechanical stimuli applied to their cutaneous receptive fields, which ranged in size from two digits to the entire limb. Of 17 thermally tested neurons, 16 responded to innocuous or noxious thermal stimuli. Among STT neurons that responded to thermal stimuli, 50% responded to innocuous cooling as well as noxious heat and cold, 31% responded to noxious heat and cold, and 19% responded only to noxious heat. Axons from cells responsive to innocuous cooling terminated in the core region of VPL, significantly dorsal and medial relative to other thermally responsive subgroups. In rats, thermally responsive subgroups of MZ neurons project directly to distinct regions of VPL.

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“…Indeed, in cats, histamine-responsive mechano-insensitive neurons were described in the dorsal horn (lamina I) of the spinal cord [25]. However, histamineresponsive spinothalamic tract neurons were also identified among the mechano-, heat-and capsaicin-sensitive ones in primates [26]. It is therefore suggested that spinal projection neurons may receive innervation from both itch sensitive and nociceptive primary fibers [13] which supports the selectivity over the specificity hypothesis regarding the relation of itch and pain transmitting pathways.…”

Section: Spinal Itch Processingmentioning

confidence: 99%

TRP Channels and Pruritus

Tóth¹,

Bı́ró²

2013

TOPAINJ

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Itch (pruritus) is one of the most often seen sensory phenomena in clinical practice. Recent neurophysiological findings proposed the existence of a novel pruriceptive system which includes a multitude of pruritogenic (itch-inducing) peripheral mediators, itch-selective pruriceptors, sensory afferent networks, spinal cord neurons, and certain central nervous system regions. In this review, we first introduce major features of the pruriceptive system. We then focus on defining the roles of transient receptor potential (TRP) ion channels in skin-coupled itch and provide compelling evidence that certain thermosensitive TRP channels (especially TRPV1, TRPV3, TRPV4, and TRPA1) are indeed key players in pruritus pathogenesis. Finally, we propose TRP-centered future experimental directions towards the therapeutic targeting of TRP channels in the clinical management of itch.

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Comparison of Responses of Primate Spinothalamic Tract Neurons to Pruritic and Algogenic Stimuli

Cited by 85 publications

References 32 publications

Facial injections of pruritogens or algogens elicit distinct behavior responses in rats and excite overlapping populations of primary sensory and trigeminal subnucleus caudalis neurons

Facial injections of pruritogens or algogens elicit distinct behavior responses in rats and excite overlapping populations of primary sensory and trigeminal subnucleus caudalis neurons

Thermally Identified Subgroups of Marginal Zone Neurons Project to Distinct Regions of the Ventral Posterior Lateral Nucleus in Rats

TRP Channels and Pruritus

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