Pain Affect Without Pain Sensation in a Patient With a Postcentral Lesion PDF

Pain 81 (1999) 211–214 Clinical Note Pain affect without pain sensation in a patient with a postcentral lesion M. Ploner, H.-J. Freund, A. Schnitzler* Departmen...

Pain 81 (1999) 211–214 Clinical Note Pain affect without pain sensation in a patient with a postcentral lesion M. Ploner, H.-J. Freund, A. Schnitzler* Department of Neurology, University of Duesseldorf, Moorenstrasse 5, 40225 Duesseldorf, Germany Received 13 October 1998; received in revised form 29 December 1998; accepted 1 January 1999 Abstract We report findings from clinical examination and cutaneous laser stimulation in a 57-year-old male, who suffered from a right-sided postcentral stroke. In this patient, we were able to demonstrate (i) a dissociation of discriminative and affective components of pain perception and, for the first time in humans, (ii) the dependence of sensory-discriminative pain component and first pain sensation on the integrity of the lateral pain system.  1999 International Association for the Study of Pain. Published by Elsevier Science B.V. Keywords: Pain perception; Somatosensory cortex 1. Introduction following single painful stimuli. Peripherally, the neural basis of this phenomenon is a dual pathway for pain with Cerebral structures involved in pain processing are com- Ad-fibers mediating pricking first pain and C-fibers mediat- monly divided into a lateral and a medial pain system (Albe- ing dull second pain (Bishop and Landau, 1958). Centrally, Fessard et al., 1985). These two systems diverge at the a representation of first pain in the lateral pain system has thalamic level. The main constituents of the lateral pain been suggested (Hassler, 1976), but no direct evidence for system are the lateral thalamic nuclei and the primary (SI) this has been presented so far. and secondary (SII) somatosensory cortices (Kenshalo and Here, we report findings from clinical examination, cuta- Willis, 1991). The medial pain system essentially consists neous laser stimulation and magnetic resonance imaging of the medial thalamic nuclei and the anterior cingulate (MRI) of a patient with a selective ischemic lesion of the cortex (Vogt et al., 1993). right SI and SII cortices. This patient offered the unique These anatomically segregated systems are supposed to possibility to study possible dissociations between sen- subserve functionally different components of pain percep- sory-discriminative and motivational-affective components tion. Experimental and lesion data in humans indicate a of pain perception and between first and second pain. Our close association between motivational-affective aspects results demonstrate, for the first time in humans, a loss of of pain and the medial pain system (Vogt et al., 1993; pain sensation with preserved pain affect, and provide clear Craig et al., 1996; Rainville et al., 1997). However, an asso- evidence for the crucial role of the lateral pain system in the ciation between the sensory-discriminative component of sensory-discriminative pain component and in first pain sen- pain perception and the lateral pain system, as deduced sation. from neurophysiological experiments in monkeys (Ken- shalo and Willis, 1991), has not yet unequivocally been proven in humans. 2. Case report A further characteristic of pain perception is the appear- ance of two subsequent and qualitatively distinct sensations 2.1. Case history * Corresponding author. Tel.: +49-211-811-7893; fax: +49-211-811- A 57-year-old male with no history of previous neurolo- 9033; e-mail: [email protected] gical diseases suffered from a cardioembolic stroke in the 0304-3959/99/$20.00  1999 International Association for the Study of Pain. Published by Elsevier Science B.V. PII: S03 04-3959(99)000 12-3 212 M. Ploner et al. / Pain 81 (1999) 211–214 territory of the right middle cerebral artery. While initial left marginal left-sided pronation when maintenance of arms hemiparesis resolved within the first few hours left-sided against gravity was examined without any further motor sensory deficits persisted. MRI performed 3 days after deficit. These deficits remained stable and unchanged across stroke showed a lesion confined to the right postcentral the two examinations. gyrus and the parietal operculum extending from 12 mm to 54 mm above the anterior commissure-posterior commis- 2.3. Cutaneous laser stimulation sure-line, thus comprising the hand area of SI and SII (Fig. 1). No other lesions were visible on the scans studied. Pre- Controlled, selective thermonociceptive stimuli were served median nerve somatosensory evoked short-latency applied by means of cutaneous laser stimulation (Bromm potentials and diminished long latency potentials suggested and Treede, 1991) using a Tm:YAG-Laser (Baasel Laser- integrity of peripheral somatosensory pathways and partial tech) with a wavelength of 2000 nm, a pulse duration of 1 lesion of SI. ms and a spotdiameter of 6 mm. Twelve days after stroke, pain thresholds on the dorsum of feet and hands were deter- 2.2. Clinical examination mined with increasing and decreasing stimulus intensities at 50 mJ steps (actual output intensity can vary up to 5% from Evaluation of the patient’s deficits 5 and 12 days after demanded intensity). The threshold was defined as intensity stroke was based on extensive clinical examination includ- that elicited painful sensations in at least three of five appli- ing light touch, static tactile thresholds with von Frey-hair cations. Reaction times to 20 painful laser stimuli (stimulus stimuli, two-point and sharp-dull discrimination, sense of intensity 450 mJ) applied to the dorsum of each hand were movement, graphaesthesia, stereognosia thermaesthesia measured in two subsequent runs. Stimulation site was (test tubes filled with hot and cold water), pallaesthesia slightly changed between successive stimuli, interstimulus and motor testing. intervals varied randomly between 10 and 14 s. The patient While sensory examination of the patient’s right side was was instructed to lift the index finger contralateral to stimu- within normal limits, left-sided examination revealed lation as soon as any sensation was perceived. Finger lift hypaesthesia of foot, leg and face and anaesthesia of hand was detected by a photoelectric barrier. Due to the failure to and arm, in all the above mentioned tests except for nearly correctly place the index finger of the proprioceptively normal pallaesthesia (Table 1). In particular, thermal stimuli impaired left hand into the photoelectric barrier motor reac- did not evoke any sensation. Motor testing showed only tions of the sensory impaired left hand could not be recorded Fig. 1. Transaxial MRI-slices at 42 mm (left) and 18 mm (right) parallel above the anterior commissure-posterior commissure-line. Scales give coordinates in mm according to the Talairach frame of reference (Talairach and Tournoux, 1988). Markers (*) indicate the central sulcus.  M. Ploner et al. / Pain 81 (1999) 211–214 213 Table 1 contrast, detection of and reaction to painful stimuli as Sensory testing well as pain affect do obviously not require integrity of SI and SII. Nevertheless, damage to SI and SII produced hypal- Right hand Left hand gesia in our patient, suggesting interaction between medial von Frey-hair stimuli (mN) 2.83 >6.65 and lateral pain system in normal pain experience. Two-point-discrimination (mm) 12 – Most previous lesion studies in humans agreed on the Sharp-dull-discriminationa 5/5 0/5 Sense of mcp joint movementa 5/5 0/5 crucial importance of the postcentral gyrus and/or the par- Graphaesthesiaa 5/5 0/5 ietal operculum in pain perception (Sweet, 1982; Boivie et Stereognosiaa 5/5 0/5 al., 1989; Greenspan and Winfield, 1992). Although these Pallaesthesia (tuning fork) 100% 75% studies are clinically well documented, the partial lack of Pain threshold (mJ) 200 –b information about lesion extent, presence of additional a Number of correct trials. lesions and manifold, and ambiguous clinical presentations b At 350 mJ and more the patient described a ‘clearly unpleasant’ feeling. interfered with a consistent concept of these structures in mcp, metacarpophalangeal; –, no sensation. human pain perception. Moreover, clinical examination of pain perception was carried out with non-selective pain- and thus reaction times could not be determined for six evoking stimuli. Thus, activation of pain afferents was stimuli to the normal right hand. In two prior control runs always contaminated by activation of tactile pathways. mean reaction times to binaural acoustic stimuli had been Cutaneous laser stimulation, as applied in our study, over- 300 ms (SD = 67 ms) for right index finger lift and 246 ms comes this limitation by selective activation of thermonoci- (SD = 64 ms) for left index finger lift, so that prolonged ceptive afferents (Bromm and Treede, 1991). Thus, our reaction times due to accompanying left-sided motor defi- findings refer to cutaneous but not necessarily to deep noci- cits could reliably be excluded. ception. Pain thresholds were 200 mJ for right hand and both feet. More recent evidence for an involvement of SI and SII in Evoked pain sensations were characterized as ‘pinprick- pain processing comes from functional imaging studies. like’ and were well localized within 2–3 cm. For left Most of them showed pain associated increases of cerebral hand, up to an intensity of 600 mJ, no pain sensation blood flow in contralateral SI and SII (Talbot et al., 1991; could be elicited. However, at intensities of 350 mJ and Coghill et al., 1994; Casey et al., 1996; Craig et al., 1996; more, the patient spontaneously described a ‘clearly unplea- Andersson et al., 1997; Derbyshire et al., 1997; Rainville et sant’ intensity dependent feeling emerging from an ill-loca- al., 1997). According to the Talairach-coordinates (Talair- lized and extended area ‘somewhere between fingertips and ach and Tournoux, 1988), activation foci were located in shoulder’, that he wanted to avoid. The fully cooperative regions corresponding to our patient’s lesion. But again, and eloquent patient was completely unable to further describe quality, localization and intensity of the perceived stimulus. Suggestions from a given word list containing ‘warm’, ‘hot’, ‘cold’, ‘touch’, ‘burning’, ‘pinprick-like’, ‘slight pain’, ‘moderate pain’ and ‘intense pain’ were denied nor did the patient report any kind of paraesthesias (all descriptions translated from German). Reaction times to laser stimuli on the right hand showed a bimodal distribu- tion with medians at 400 ms and 1000 ms. By contrast, stimulation of the left hand yielded exclusive long-latency responses with a median at 1426 ms (Fig. 2). 3. Discussion In the patient reported here, clinical examination and cutaneous laser stimulation revealed prolonged reaction times to painful laser stimuli, an elevated pain threshold, loss of sensory-discriminative pain component and pre- served motivational-affective dimension of pain. This clear perceptual dissociation was paralleled by an anatomi- cal dissociation between affected lateral pain system and spared medial pain system. This pattern of impairment shows the essential role of SI and/or SII for the sensory- Fig. 2. Reaction times to cutaneous laser stimulation of the normal right discriminative aspects of pain perception in humans. By (N = 14) and the affected left (N = 20) hand. 214 M. Ploner et al. / Pain 81 (1999) 211–214 only in a few of these studies were selective painful stimuli References applied (Andersson et al., 1997; Derbyshire et al., 1997). 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Talairach, J. and Tournoux, P., Co-planar Stereotaxic Atlas of the Human Brain, Thieme, Stuttgart, 1988. Acknowledgements Talbot, J.D., Marrett, S., Evans, A.C., Meyer, E., Bushnell, M.C. and Duncan, G.H., Multiple representations of pain in human cerebral cortex, Science, 251 (1991) 1355–1358. This study was supported by the Huneke-Stiftung and the Vogt, B.A., Sikes, R.W. and Vogt, L.J., Anterior cingulate cortex and the Deutsche Forschungsgemeinschaft (SFB 194). Thanks to medial pain system. In: B.A. Vogt and M. Gabriel (Eds.), Neurobiology Dr. C.J. Ploner (Charité Berlin) for helpful comments on of Cingulate Cortex and Limbic Thalamus: a Comprehensive Hand- the manuscript. book, Birkhauser, Boston, MA, 1993, pp. 313–344.