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Forebrain Mechanisms of Nociception and Pain: Analysis Through Imaging

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Forebrain Mechanisms of Nociception and Pain: Analysis Through Imaging Proc. Natl. Acad. Sci. USA Vol. 96, pp. 7668–7674, July 1999 Colloquium Paper This paper was presented at the National Academy of Sciences colloquium ‘‘The Neurology of Pain,’’ held December 11–13, 1998, at the Arnold and Mabel Beckman Center in Irvine, CA. Forebrain mechanisms of nociception and pain: Analysis through imaging KENNETH L. CASEY Neurology Service, Veterans Affairs Medical Center, University of Michigan, 2215 Fuller Road, Ann Arbor, MI 48105 ABSTRACT Pain is a unified experience composed of the noxious or aversive quality of the stimulus in animals and interacting discriminative, affective-motivational, and cogni- the perceived affective quality of pain in humans (4, 5). tive components, each of which is mediated and modulated Anterior cingulate neurons that respond to noxious stimuli through forebrain mechanisms acting at spinal, brainstem, have large, often bilateral receptive fields, consistent with a and cerebral levels. The size of the human forebrain in relation limited role in spatial discriminative capacity (6). There is no to the spinal cord gives anatomical emphasis to forebrain comparable information about the neuronal substrate for the control over nociceptive processing. Human forebrain pathol- cognitive dimension of pain, but there are numerous studies ogy can cause pain without the activation of nociceptors. and observations showing the profound influences of atten- Functional imaging of the normal human brain with positron tion, suggestion, and emotional state on the perception of pain emission tomography (PET) shows synaptically induced in- (7). The broad range of environmental influences, such as creases in regional cerebral blood flow (rCBF) in several attention, fear, and the placebo effect on the perception of regions specifically during pain. We have examined the vari- pain suggests that cortical association areas and their subcor- ables of gender, type of noxious stimulus, and the origin of tical connections are critical participants in mediating the nociceptive input as potential determinants of the pattern and cognitive aspects of pain. intensity of rCBF responses. The structures most consistently The Forebrain Modulation of Pain. The processing of activated across genders and during contact heat pain, cold nociceptive stimuli is modulated by the forebrain at spinal, pain, cutaneous laser pain or intramuscular pain were the brainstem, and diencephalic levels. Stimulation of the cerebral contralateral insula and anterior cingulate cortex, the bilat- cortex or thalamus can facilitate or suppress the responses of eral thalamus and premotor cortex, and the cerebellar vermis. spinothalamic or trigeminothalamic tract neurons (8, 9). In the These regions are commonly activated in PET studies of pain awake monkey, the response of trigeminothalamic cells to conducted by other investigators, and the intensity of the brain noxious heat depends on behavioral state (10, 11). Corticob- rCBF response correlates parametrically with perceived pain ulbar and corticothalamic neurons have marked effects on the intensity. To complement the human studies, we developed an excitability of brainstem and thalamic cells that receive noci- animal model for investigating stimulus-induced rCBF re- ceptive input (12–16). sponses in the rat. In accord with behavioral measures and the Because of the large volume of the human forebrain in results of human PET, there is a progressive and selective relation to that of the spinal cord (77% vs. 2% of central activation of somatosensory and limbic system structures in nervous system volume), these descending modulatory influ- the brain and brainstem following the subcutaneous injection ences may assume greater importance in humans than in other of formalin. The animal model and human PET studies should species, such as the laboratory rat, where the forebrain is less be mutually reinforcing and thus facilitate progress in under- anatomically dominant (31% vs. 35% of central nervous standing forebrain mechanisms of normal and pathological system volume) (17). The human spinothalamic tract, for pain. example, contains an estimated 2,000 to 5,000 fibers whereas the corticospinal tract, which includes fibers terminating in the Forebrain Mediation of Pain. Pain is a conscious experience superficial layers of the dorsal horn (18, 19), is estimated to ϫ 5 ϫ 6 that includes discriminative, affective-motivational, and cog- contain from 5 10 to 1 10 fibers (20, 21). Corticothalamic nitive components that produce the unified sensation of pain. influences are also likely to be dominant in the human; in the These components are each mediated through separate, in- cat, approximately 50% of the estimated 5,000 to 9,000 syn- teractive forebrain mechanisms (1). For example, the ability to apses on thalamocortical projection neurons are presumed to localize somatic stimuli in time, space, and along a continuum be of cortical origin, whereas only 15% are formed by ascend- of intensities is greatly impaired following lesions limited to the ing afferent fibers (22). primary somatosensory (S1) cortex or the ventral posterolat- The Physiological Rationale of Positron Emission Tomog- eral thalamus. These lesions do not produce analgesia, how- raphy (PET). Synaptic activity generates increases in cerebral ever, because the aversive nature of noxious stimuli, although blood flow (CBF). This physiological fact is the basis for both poorly localized, is still evident in the behavior of animals and PET and functional magnetic resonance imaging (fMRI). The the verbal reports of humans (2). Neurons in the S1 cortex and most commonly used fMRI method relies on local shifts in the ventral posterolateral thalamus, including those responding magnetic field that accompany the shift from deoxyhemoglo- primarily to noxious stimuli, have small, contralateral recep- bin to oxyhemoglobin within activated perfused tissue (23). tive fields consistent with the mediation of spatial stimulus PET and fMRI are complementary methods of assessing brain localization (3). In contrast, lesions within the anterior cingu- activity. This article will be limited to a discussion of PET. late cortex have no effect on innocuous or nociceptive som- esthetic discriminative functions, but impair the recognition of Abbreviations: CBF, cerebral blood flow; rCBF, regional CBF; fMRI, functional magnetic resonance imaging; PET, positron emission to- mography; ROI, region of interest; S1, primary somatosensory (cor- PNAS is available online at www.pnas.org. tex); S2, secondary somatosensory (cortex); VOI, volumes of interest. 7668 Downloaded by guest on September 27, 2021 Colloquium Paper: Casey Proc. Natl. Acad. Sci. USA 96 (1999) 7669 The first indication that brain activity increases global CBF an increase in rCBF, the rCBF computed during a control was reported by Roy and Sherrington over 100 years ago (24). condition is subtracted from that computed during the test Subsequent radioactive tracer techniques revealed increases in condition. The resulting subtraction image, then, shows those regional CBF (rCBF) during sensory stimulation or the per- brain regions with differences in CBF between the two con- formance of motor tasks (25). Recent studies that use the ditions. technique of optical imaging have demonstrated that cortical A voxel-by-voxel statistical subtraction analysis (Z-score) blood flow responses occur within 3 sec of sensory stimulation with adjustment for multiple comparisons is performed by and are initially restricted to the 300- to 500-␮m dimensions of estimating the smoothness of subtraction images (40) following cortical columns before spreading to involve the surrounding three-dimensional Gaussian filtering to enhance signal-to- 3 mm to 5 mm of cortical tissue (26–28). The biochemical noise ratio and compensate for residual anatomical variance. coupling of rCBF and synaptic activity is unknown and is still Typically, only those voxels with normalized CBF values larger an area of active investigation. Studies of regional cerebral than 60% of the global value are analyzed, because these voxels glucose utilization show that it and rCBF are normally tightly represent the gray matter of the brain. Voxels showing a coupled and that the coupling occurs within the synaptic significantly increased CBF compared with the average noise neuropil. The degree of coupling may vary among regions and variance computed across all voxels (pooled variance) are under special experimental conditions (29), but it is reliably identified (41). The critical level of significance is determined present in the normal mammal. Blocking the production of by using this information to adjust P ϭ 0.05 (42). With this nitric oxide has no effect on synaptically induced rCBF re- method, the results of interest are revealed primarily through sponses in the rat somatosensory system (30). There is evi- the data analysis. However, it is also possible to perform dence that adenosine may be a critical link in this process, but correlations between the intensity of the rCBF responses it is likely that the action of several mediators may be impor- throughout the brain and some behavioral parameter of tant (31). interest, such as the perceived intensity of stimulation (43). A reduction of rCBF should occur when synaptic activity is In addition, volumes of interest (VOI) may be established suppressed below some resting or background level. Indeed, within brain structures selected because of a priori hypotheses reductions in rCBF are observed in many PET studies
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