Spinal dorsal horn neuronal responses to myelinated versus unmyelinated heat nociceptors and their modulation by activation of the periaqueductal grey in the rat

Hypertension and Stroke Research Laboratory, Royal North Shore Hospital, St Leonards, Sydney, NSW 2065, Australia.
The Journal of Physiology (Impact Factor: 5.04). 11/2006; 576(Pt 2):547-56. DOI: 10.1113/jphysiol.2006.117754
Source: PubMed


The aim of this study was to further understand the central processing of inputs arising from unmyelinated and myelinated nociceptors by (i) determining the response characteristics of Class 2 dorsal horn neurones to preferential activation of C- and A-fibre heat nociceptors, and (ii) investigating the control exerted by the dorsolateral/lateral region of the midbrain periaqueductal grey (DL/L-PAG) on C- and A-fibre-evoked responses of these neurones. The use of different rates of skin heating to preferentially activate unmyelinated (C-fibre; 2.5 degrees C s(-1)) versus myelinated (A-fibre; 7.5 degrees C s(-1)) heat nociceptors revealed that, in response to C-nociceptor activation, Class 2 neurones encode well only over the first 5 degrees C above threshold, and that at higher temperatures responses decline. In contrast, responses to A-nociceptor activation are linear and encode skin temperature over more than 10 degrees C, and almost certainly into the tissue-damaging range. PAG stimulation raised thresholds and decreased significantly the magnitude of responses to A- and C-nociceptor activation. However, differences were revealed in the effects of descending control on the relationships between skin temperature and neuronal firing rate; the linear relationship that occurred over the first 5 degrees C of slow rates of skin heating was no longer evident, whereas that to fast rates of skin heating was maintained over the entire range, albeit shifted to the right. These data indicate that the sensori-discriminative information conveyed in A-fibre nociceptors is maintained and that the information from C-nociceptors is lost in the presence of descending control from the DL/L-PAG. The data are discussed in relation to the role of the DL/L-PAG in mediating active coping strategies.

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Available from: Bridget M Lumb, Jan 05, 2016
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    • "Passive coping is coordinated by a column of neurons located in ventrolateral (vl) PAG and is associated with a reduced responsiveness to external stimuli, and a general cessation in movements and a fixed (freezing) posture (Zhang et al., 1990; Bandler et al., 1991; Carrive, 1993; Lovick, 1993; Bandler and Keay, 1996). As part of these complex coping strategies, the PAG exerts descending control of spinal sensory processing that not only discriminates between noxious and nonnoxious events but also between nociceptive inputs of different behavioral significance; C-nociceptor-evoked activity (mediating the slowly conducted, poorly localized and therefore distracting component of the nociceptive message) is depressed while A-nociceptor-evoked activity (the rapidly conducted component that encodes the intensity of the nociceptive signal; McMullan and Lumb, 2006b) is left intact or even enhanced. Indeed, previous "
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    ABSTRACT: How does the cerebellum, the brain's largest sensorimotor structure, contribute to complex behaviors essential to survival? While we know much about the role of limbic and closely associated brainstem structures in relation to a variety of emotional, sensory, or motivational stimuli, we know very little about how these circuits interact with the cerebellum to generate appropriate patterns of behavioral response. Here we focus on evidence suggesting that the olivo-cerebellar system may link to survival networks via interactions with the midbrain periaqueductal gray, a structure with a well known role in expression of survival responses. As a result of this interaction we argue that, in addition to important roles in motor control, the inferior olive, and related olivo-cortico-nuclear circuits, should be considered part of a larger network of brain structures involved in coordinating survival behavior through the selective relaying of "teaching signals" arising from higher centers associated with emotional behaviors.
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    • "There is direct evidence from peripheral nerve recordings (Yeomans & Proudfit, 1996) that the same slow and fast rates of heating as used in the present study preferentially activate primary afferents that conduct in the C-and A-fibre range, respectively. Furthermore, evidence that slow and fast rates of skin heating preferentially activate C-and A-nociceptors, respectively, is provided by four lines of evidence from this laboratory: (i) differential capsaicin sensitivity of reflex responses evoked by slow, compared with fast, rates of skin heating (McMullan et al., 2004), which is consistent with preferential activation of C-heat nociceptors, the majority of which express Transient Receptor Potential Channel V1 (TRPV1) receptors; (ii) differential dimethylsulphoxide sensitivity of responses evoked by fast, compared with slow, rates of skin heating (J.L. Leith, A.W. Wilson, L.F. Donaldson and B.M. Lumb, unpublished observation , and see Baumann et al., 1991; Wilson et al., 1999); (iii) response characteristics of dorsal horn neurones to slow vs. fast rates of skin heating closely resemble those of peripheral C-and A-nociceptive afferents, respectively (McMullan & Lumb, 2006b) and (iv) in contrast to dorsal horn neurones with C-fibre inputs, neurones lacking C-fibre inputs (C-negative neurones) do not respond to slow rates of skin heating (Leith et al., unpublished observation). "
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    ABSTRACT: The periaqueductal grey can differentially control A- vs. C-nociceptor-evoked spinal reflexes and deep spinal dorsal horn neuronal responses. However, little is known about the control of A- vs. C-fibre inputs to lamina I and the lateral spinal nucleus, and how this correlates with the control of deeper laminae. To address this, the laminar distributions of neurones expressing Fos-like immunoreactivity were determined following preferential activation of A- or C-heat nociceptors, using fast or slow rates of skin heating, respectively, in the absence or presence of descending control evoked from the periaqueductal grey. In lamina I, numbers of Fos-positive neurones following both fast and slow rates of skin heating were reduced significantly following activation in the ventrolateral and dorsolateral/lateral periaqueductal grey. In contrast, in the deep dorsal horn (laminae III-VI), activation in both the ventrolateral and dorsolateral/lateral periaqueductal grey significantly reduced the numbers of Fos-positive neurones evoked by C- but not A-nociceptor stimulation. C- but not A-heat nociceptor activation evoked Fos bilaterally in the lateral spinal nucleus. Stimulation in the ventrolateral but not the dorsolateral/lateral periaqueductal grey significantly increased the numbers of Fos-positive neurones evoked by A- and C-nociceptor stimulation bilaterally in the lateral spinal nucleus. These data have demonstrated differences in the descending control of the superficial vs. the deep dorsal horn and lateral spinal nucleus with respect to the processing of A- and C-fibre-evoked events. The data are discussed in relation to the roles of A- and C-nociceptors in acute and chronic pain.
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