Fos induction in lamina I projection neurons in response to noxious thermal stimuli

Todd, Andrew J.; Spike, Rosemary C.; Young, Steven J.; Puskár, Zita

doi:10.1016/j.neuroscience.2004.11.001

Cited by 49 publications

(43 citation statements)

References 55 publications

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“…Consistent with our data, Khasabov et al (2001) found that an almost identical proportion of wide-dynamic-range (class 2) neurons responded to cold delivered via a Peltier thermode, which encoded intensity to noxious cold over a broad range of temperatures. Furthermore, functional anatomical studies have shown that hindpaw and facial cold stimulation evoke intensitydependent Fos expression in dorsal horn neurons, including NK-1-positive lamina I projection neurons, which are believed to form spinal-brainstem feedback loops with important roles in the development of chronic pain states (Strassman et al, 1993;Abbadie et al, 1994;Doyle and Hunt, 1999;Suzuki et al, 2002;Todd et al, 2005). However, in contrast to our findings, Khasabov et al (2001) found a higher proportion of cold-responsive class 3 neurons, but around half (42%) only responded to cooling Ͻ0°C.…”

Section: Neural Mechanisms Of Cold Somatosensationcontrasting

confidence: 97%

“…At the spinal level, electrophysiological studies have demonstrated that wide-dynamicrange and nociceptive-specific neurons in the dorsal horn are excited by cold stimuli and encode intensity to noxious cold over a wide range of temperatures (Christensen and Perl, 1970;Khasabov et al, 2001;Brignell et al, 2008). Additionally, cold stimulation of the hindpaw or face evokes intensity-dependent Fos expression in spinal and medullary dorsal horn neurons, respectively (Strassman et al, 1993;Abbadie et al, 1994;Doyle and Hunt, 1999;Todd et al, 2005).…”

Section: Introductionmentioning

confidence: 99%

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Spinal Processing of Noxious and Innocuous Cold Information: Differential Modulation by the Periaqueductal Gray

Leith¹,

Koutsikou²,

Lumb³

et al. 2010

J. Neurosci.

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In addition to cold being an important behavioral drive, altered cold sensation frequently accompanies pathological pain states. However, in contrast to peripheral mechanisms, central processing of cold sensory input has received relatively little attention. The present study characterized spinal responses to noxious and innocuous intensities of cold stimulation in vivo and established the extent to which they are modulated by descending control originating from the periaqueductal gray (PAG), a major determinant of acute and chronic pain. In lightly anesthetized rats, hindpaw cooling with ethyl chloride, but not acetone, was sufficiently noxious to evoke withdrawal reflexes, which were powerfully inhibited by ventrolateral (VL)-PAG stimulation. In a second series of experiments, subsets of spinal dorsal horn neurons were found to respond to innocuous and/or noxious cold. Descending control from the VL-PAG distinguished between activity in nociceptive versus non-nociceptive spinal circuits in that innocuous cold information transmitted by non-nociceptive class 1 and wide-dynamic-range class 2 neurons remained unaltered. In contrast, noxious cold information transmitted by class 2 neurons and all cold-evoked activity in nociceptive-specific class 3 neurons was significantly depressed. We therefore demonstrate that spinal responses to cold can be powerfully modulated by descending control systems originating in the PAG, and that this control selectively modulates transmission of noxious versus innocuous information. This has important implications for central processing of cold somatosensation and, given that chronic pain states are dependent on dynamic alterations in descending control, will help elucidate mechanisms underlying aberrant cold sensations that accompany pathological pain states.

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Section: Neural Mechanisms Of Cold Somatosensationcontrasting

confidence: 97%

Section: Introductionmentioning

confidence: 99%

Spinal Processing of Noxious and Innocuous Cold Information: Differential Modulation by the Periaqueductal Gray

Leith¹,

Koutsikou²,

Lumb³

et al. 2010

J. Neurosci.

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“…Given the large proportion of nociceptive afferents in the DR A␦-and C-fiber populations, it is possible to speculate that our patterns of SDH connections are part of mechanisms contributing to nociception and pain. Along this line, three of our lamina I cells that received excitatory projections from lamina II vertical cells did appear morphologically similar to fusiform lamina I neurons that have been proposed as a nociceptive specific class (Han et al,1998) (but see Todd et al, 2005). On the other hand, significant numbers of low-threshold DR A␦ and DR C mechanoreceptors project to lamina II (Light and Perl, 1979b;Sugiura et al, 1986;Woodbury et al, 2000).…”

Section: Discussionsupporting

confidence: 68%

Modular Organization of Excitatory Circuits between Neurons of the Spinal Superficial Dorsal Horn (Laminae I and II)

Lü¹,

Perl²

2005

J. Neurosci.

226

268

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“…In the rat, those that express the heat-gated channel TRPV1 are known to predominately terminate in lamina I and II, although some fibers are observed deeper in lamina V and X (Tominaga et al, 1998). It is likely that cold fibers have similar central projections, suggested by peripheral cold induction of c-fos expression, an indicator of neural activity, in superficial lamina (Todd et al, 2005).…”

Section: Central Projections Of Trpm8 Fibers In the Dorsal Spinal Cordmentioning

confidence: 99%

Diversity in the Neural Circuitry of Cold Sensing Revealed by Genetic Axonal Labeling of Transient Receptor Potential Melastatin 8 Neurons

Takashima¹,

Daniels²,

Knowlton³

et al. 2007

J. Neurosci.

192

214

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Sensory nerves detect an extensive array of somatosensory stimuli, including environmental temperatures. Despite activating only a small cohort of sensory neurons, cold temperatures generate a variety of distinct sensations that range from pleasantly cool to painfully aching, prickling, and burning. Psychophysical and functional data show that cold responses are mediated by both C-and A␦-fibers with separate peripheral receptive zones, each of which likely provides one or more of these distinct cold sensations. With this diversity in the neural basis for cold, it is remarkable that the majority of cold responses in vivo are dependent on the cold and menthol receptor transient receptor potential melastatin 8 (TRPM8). TRPM8-null mice are deficient in temperature discrimination, detection of noxious cold temperatures, injury-evoked hypersensitivity to cold, and nocifensive responses to cooling compounds. To determine how TRPM8 plays such a critical yet diverse role in cold signaling, we generated mice expressing a genetically encoded axonal tracer in TRPM8 neurons. Based on tracer expression, we show that TRPM8 neurons bear the neurochemical hallmarks of both C-and A␦-fibers, and presumptive nociceptors and non-nociceptors. More strikingly, TRPM8 axons diffusely innervate the skin and oral cavity, terminating in peripheral zones that contain nerve endings mediating distinct perceptions of innocuous cool, noxious cold, and first-and second-cold pain. These results further demonstrate that the peripheral neural circuitry of cold sensing is cellularly and anatomically complex, yet suggests that cold fibers, caused by the diverse neuronal context of TRPM8 expression, use a single molecular sensor to convey a wide range of cold sensations.

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Fos induction in lamina I projection neurons in response to noxious thermal stimuli

Cited by 49 publications

References 55 publications

Spinal Processing of Noxious and Innocuous Cold Information: Differential Modulation by the Periaqueductal Gray

Spinal Processing of Noxious and Innocuous Cold Information: Differential Modulation by the Periaqueductal Gray

Modular Organization of Excitatory Circuits between Neurons of the Spinal Superficial Dorsal Horn (Laminae I and II)

Diversity in the Neural Circuitry of Cold Sensing Revealed by Genetic Axonal Labeling of Transient Receptor Potential Melastatin 8 Neurons

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