COGNITION AND EMOTION, 2004, 18 2), 281±287 BRIEF REPORT. Effects of spinal cord injuries on the subjective component of emotions.

Transcription

1 COGNITION AND EMOTION, 2004, 18 2), 281±287 BRIEF REPORT Effects of spinal cord injuries on the subjective component of emotions Pilar Cobos Malaga University, Spain MarõÂa SaÂnchez, Nieves PeÂrez, and Jaime Vila Granada University, Spain Responses to a structured interview by 19 patients with spinal cord injuries SCI) 7 women and 12 men) concerning their past pre-injury) and present emotions were analysed and compared with responses by 19 SCI-free controls matched for sex, age, and education. In addition, subjects assessed the valence and arousal of 10 pleasant, 10 neutral, and 10 unpleasant pictures selected from the International Affective Picture System. The results indicate that there is no decrease in emotional experience among individuals with SCI compared with those without. For all the emotional scales joy, love, sentimentalism, positive emotions as a whole, fear, anger, sadness, and negative emotions as a whole) the SCI group always showed either no change or an increase; this increase was significantly higher in SCI than in control subjects for sadness. No differences were observed between the two groups in the subjective assessment of the pictures. The implications of the results for the James versus Cannon controversy on the theory of emotions are discussed. The implication of bodily responses in the experience and expression of emotion has long been controversial. The historic debate between supporters of James and Cannon theories established the coordinates from which later theories evolved throughout the 20th century: peripheralism vs. centralism; bodily responses vs. cognition; and specificity vs. Correspondence should be addressed to Pilar Cobos, Departamento de Personalidad, EvaluacioÂn y Tratamiento PsicoloÂgico, Facultad de PsicologõÂa, Universidad de Malaga, Spain; mpcobos@uma.es Support for this research was provided by the Spanish Ministry of Education research project PB ) and Junta de AndalucõÂa research group HUM 388). # 2004 Psychology Press Ltd DOI: /

2 282 COBOS ET AL. dimensionality. James maintained that the experience of emotion derives from the perception of physiological changes produced under different situations. This perspective led to the so-called peripheral, physiological, and specificity theories. In contrast, Cannon claimed that corticothalamic interactions are responsible for the experience and expression of emotions and that accompanying physiological reactions are general and vary only in intensity. Thus, we are unable to distinguish one emotion from another on the basis of peripheral bodily responses. Cannon's approach led to the so-called central, cognitive, and dimensionality theories. Examination of patients with spinal cord lesions represents one of the oldest research lines for testing theories of emotions. Since the seminal work of William James 1884), patients with differing degrees of reduction in their peripheral feedback have been considered ideal subjects for this purpose. The results of such studies have not all pointed in the same direction, with mutual criticism among authors regarding methodological flaws Chwalisz, Diener, & Gallagher, 1988; Reisenzein, 1983; Richards, Hirt, & Melamed, 1982; Trieschmann, 1980; Tucker, 1980), absence of a complete injury Fehr & Stern, 1970), problems in controlling medication, and differences in styles of coping with the injury Chwalisz et al., 1988). Surprisingly, Hohmann's classic study 1966) is still frequently quoted in textbooks in support of the hypothesis that loss in peripheral feedback from somatic responses reduces emotional feeling, despite successive failures to confirm Hohmann's results see Bermond, Nieuwenhuyse, Fasotti, & Schuerman, 1991; Chwalisz et al., 1988). Studies of emotions in this type of patient have relied on self-reports from structured interviews, questionnaires, or in response to the presentation of emotional slides. The present study is part of an investigation combining the visualisation of affective pictures and self-reports. The startle-probe paradigm during visualisation of affective pictures Lang, 1995) was used in combination with a structured interview similar to that used by Hohmann. The visualisation of affective pictures, using the Spanish adaptation of the International Affective Picture System Molto et al., 1999), yield subjective indices of the emotional response to visual images that have previously been calibrated for valence and arousal Bradley, 2000). Our use of the structured interview allowed direct replication of Hohmann's study, although we added the following modifications: 1) a control group of injury-free subjects matched for sex, age, and education; 2) additional scales to assess positive emotions joy and love); and 3) specific questions on sexual behaviour and social activity. This brief report is limited to the subjective measurements of emotion. METHOD Subjects A total of 19 subjects with spinal cord injuries 7 women and 12 men) and 19 control subjects matched for sex, age, and education were included in the study. The characteristics of the injuries and patients' age, sex, marital status, and educational level are shown in Table 1. The spinal cord injury group included patients with a minimum 18 month history of complete or incomplete traumatic or surgical spinal cord injury. Exclusion criteria were presence of psychopathological disorder, severe visual or auditory deficit, and/or higher central nervous system involvement.

3 EMOTIONS IN SPINAL CORD INJURY PATIENTS 283 TABLE 1 Clinical and demographic characteristics of the spinal cord injury group Level and extent of injury Age yrs.mths) Years since injury Education Marital status Men C1±2 b Se S C4 b Su S T4 b Se S/P T6 b,c Su S/P T6 b Se M T6 a 24 4 Pri S T7 b Pri S/P T8 a,b Se S/P T8±9 a Pri M T10 b,c Pri M T11 b Pri D L1±4 a 34 4 Se M Women C3 a Se S/P C6 a Se S/P T5 b Se M T7 b,c 53 6 Pri M T9 b Se S T10 a,c Pri D T12 b Pri M a Extent of the injury: Incomplete. b Extent of the injury: Complete. c Incomplete sensory loss. Pri = Primary; Se = Secondary; Su = Superior; S = Single; M = Married; D = Divorced; S/P = single with partner. Design For comparisons between injured and noninjured subjects, a design for two independent groups was used. For comparisons within the study group, the 19 patients were subdivided into three groups according to the level of their injury: High lesion 6 patients with lesions from C1to T5); Middle lesion 7 patients with lesions from T6 to T8); or Low lesion 6 patients with lesions from T9 to L4). Finally, the 19 patients were also divided into two groups according to the extent of their injury: ``complete'' 12 patients with complete section of the spinal cord) or ``incomplete'' injury 7 patients with partial section of the spinal cord). Procedure Recruitment of spinal cord injury SCI) patients was conducted by contacting the Base Center for the Disabled of the province of Malaga Spain) and all local associations for the disabled in the same province. Control subjects were selected from members of

4 284 COBOS ET AL. the staff of the faculty of psychology or from contacts fulfilling the necessary requirements. All patients and controls underwent a laboratory session, in which psychophysiological and subjective responses to the slides were recorded, followed by a structured interview and completion of a mental health questionnaire to confirm the absence of psychopathology in both groups. In the startle paradigm, 10 pleasant, 10 neutral, and 10 unpleasant pictures selected from the Spanish adaptation of the International Affective Picture System Molto et al., 1999) were randomly presented to assess different physiological responses eyeblink, heart rate, and skin conductance) and then the emotional response to the slides. Using the Self-Assessment Manikin Lang, Bradley, & Cuthbert, 1999), subjects rated the valence unpleasant-pleasant) and arousal calm-excited) values of each slide on a 9-point scale. The interview gathered sociodemographic data and characteristics of the subjects as well as data on their subjective experience of the following emotions: joy, love, sentimentalism, fear, anger, and sadness. For the analysis, two derived scales were obtained: positive emotions as a whole sum of joy, love, and sentimentalism); and negative emotions as a whole sum of anger, fear, and sadness). Subjects were asked to search for memories of important and intense experiences in their past and present; past experiences were defined as those from the adolescence period and as always preceding the injury in the SCI group. Using the scale employed by Hohmann, they were asked whether they perceived each emotion the same, more, or less than in the past, assigning a value of 1to the answer ``less'', 2 to ``the same'', and 3 to ``more''. The following variables were also evaluated in the patient group: sexual behaviour, degree of autonomy, work, outings, spare time activities, and delimitation of the perceived sensitivity on contact with an object. In all cases, the interview was conducted by the first author, who met the subjects at the entrance to the faculty and accompanied them to the laboratory. The atmosphere for the interview was always relaxed and unhurried, with no objections being raised by any participant at any point. All patients cooperated fully. Data analysis Subjective ratings of the slides were analysed using parametric statistics: Student's t-test. Self-reported emotions were analysed using nonparametric statistics: Mann-Whitney U- test for two-group comparisons and Kruskal-Wallis for three-group comparisons. In addition, in order to directly compare our results with those of Hohmann, an analysis w 2 ) was undertaken of the frequency of patients reporting decrement, no change, or increment in each emotional scale. RESULTS Subjective ratings of slides Average valence ratings were: pleasant, SCI = 7.51 SD = 0.86), control, 7.83 SD = 0.6); neutral, SCI = 4.45 SD = 0.75), control = 4.51 SD = 0.43); and unpleasant, SCI = 1.63 SD = 0.59), control = 1.66 SD = 0.66). Average arousal ratings were: pleasant, SCI = 4.85 SD = 2.01), control = 3.89 SD = 2.51); neutral, SCI = 3.67 SD =1.74), control = 3.62 SD =1.52); and unpleasant, SCI = 7.37 SD =1.31), control = 7.32 SD =1.37). No significant differences were found between SCI and control subjects in either valence or arousal ratings all ts 1, 36) were < 1.3 and all ps >.2).

5 Self-reported emotions EMOTIONS IN SPINAL CORD INJURY PATIENTS 285 Table 2 summarises the main results. Most patients reported that their emotions had increased or not changed, with only a few patients describing them as decreased. When only the patient group was considered, there were significant differences in the scales of anger, w 2 2) = 8.1, p =.02, sadness, w 2 2) = 8.95, p =.01, and negative emotions as a whole, w 2 2) = 11.23, p =.004Ðalways in the direction of increment. When compared with the control group, significant differences appeared only in the sadness scale U = 104.5, p =.048), with a significantly greater increase reported by the SCI patients. To determine the existence of possible differences between the subgroups of patients with high, middle or low lesions, the corresponding statistical analyses were carried out. There was a general tendency in the group with middle lesions to score higher for both pleasant and unpleasant emotions, although in no case did the differences attain statistical significance. With regards to the categories of pleasant and unpleasant emotions as a whole, the group with low lesions scored least, although the differences were not significant all K-W w 2 s were < 4 and all ps were >.2). Finally, the scores of subjects with spinal cord injuries were compared according to the extent of the injury. There was a tendency for the group with incomplete injuries to have higher scores in the positive emotions and lower scores in the negative emotions, although the difference was significant only in the joy scale U =12.5, p =.01). TABLE 2 Comparison of perceived emotions before and after spinal cord injury Level of injury Years since injury Joy Love Sentiment Anger Fear Sadness C1±2 b 7 * * 7 * * * C3 a * + + C4 b 21 * * * * 7 + C6 a 6 * * * * * * T4 b 26. * T5 b 1.10 * * + * + + T6 b,c 23 * * + + * * T6 b * + T6 a * * + T7 b T7 b,c T8 a,c T8±9 a 5 * 7 * * * * T9 b 20 * * T10 b,c * + T10 a,c 3 + * * * * + T11 b * T12 b *. L1±4 a 4 * + * a Extent of the injury: Incomplete. b Extent of the injury: Complete. c Incomplete sensory loss. +, increased; 7, reduced; *, no change;., unable to compare.

6 286 COBOS ET AL. DISCUSSION Our results do not support Hohmann's conclusions that fear, anger, and general emotional feelings are reduced in patients with spinal cord injuries. On the contrary, there was a general tendency in the SCI group to report increases in all emotional scales except for joy. When compared with the control group, the increases were significant for sadness. As regards subjective ratings of pleasant, neutral, and unpleasant pictures, both valence and arousal ratings were similar among SCI patients and control subjects. Thus, our results are contrary to Hohmann's and are in line with those of Chwalisz et al. 1988) and Bermond et al. 1991), who reported either no change or an increase in emotional experience after the injury. Our results are also consistent with those of Dana 1921), Lowe and Carroll 1985), Montoya and Schandry 1994), and Richards et al. 1982), who concluded that the loss of peripheral information in spinal cord injured patients does not necessarily lead to a decrease in the subjective experience of emotions. These data clearly contradict James' theory 1984) and the so-called strong form of the arousal theory Chwalisz et al., 1988), according to which the internal perception of peripheral physiological changes is responsible for the emotional experience. They are also incompatible with the so-called weak form of the arousal theory Chwalisz et al., 1988), by which physiological feedback, although not necessary, can enhance the intensity of emotional experience. Our only result consistent with these theories is the reduction in the emotion of joy reported by patients with complete spinal injury in comparison with patients with an incomplete one. Given the severe life consequences of such an injury, this finding can hardly be interpreted as indicative of an impaired emotional reaction. Finally, our results concerning subjective ratings of the slides must be considered alongside those obtained in the same subjects for the modulation of physiological responses Cobos, Rius, GarcõÂa-Berdones, RamõÂrez, & Vila, 1999; Cobos, SaÂnchez, GarcõÂa, Vera, & Vila, 2002). Using the startle-probe paradigm during visualisation of affective pictures Lang, 1995), we found similar emotional modulation of the heart rate response in the patient and control groups: Both groups showed significantly greater heart rate deceleration while viewing unpleasant pictures than while viewing pleasant ones, with neutral pictures producing intermediate heart rate responses. These results replicate those found in normal subjects Bradley, 2000) and are in agreement with those recently reported by Birbaumer 2001) in completely paralysed blocked in patients suffering from amyotrophic lateral sclerosis ALS). Using a communication device based on the recording of slow cortical potentials, Birbaumer found that ALS patients showed normal emotional reactivity in an affective pictures paradigm, with no significant differences between patients and normal controls in either physiological or subjective responses. Given the modest correlations normally found between physiological and subjective measurements of emotions, evidence of peripheral physiology corroborating the normal affective reports of patients is a further argument against the idea of impaired emotional processing in subjects with spinal cord injury. Manuscript received 20 March 2001 Revised manuscript received 18 October 2002

7 EMOTIONS IN SPINAL CORD INJURY PATIENTS 287 REFERENCES Bermond, B., Nieuwenhuyse, B., Fasotti, L., & Schuerman, J. 1991). Spinal cord lesions, peripheral feedback, and intensities of emotional feelings. Cognition and Emotion, 5, 201±220. Birbaumer, N. 2001). Emotion, brain activation and complete paralysis: fmri and EEG as communication devices. Abstracts of the II International Workshop on Emotion and the Brain. Universidad de las Islas Baleares, Spain. Bradley, M. M. 2000). Emotion and motivation. In J. T. Cacciopo, L. G. Tassinary, & G. Berntson Eds.), Handbook of psychophysiology pp. 602±642). New York: Cambridge University Press. Cobos, P., Rius, F., GarcõÂa-Berdones, C., RamõÂrez, I., & Vila, J. 1999). The James versus Cannon debate on emotion revisited: Startle and autonomic modulation in patients with spinal cord injuries. Psychophysiology, 36, S1, 41±42. Cobos, P., SaÂnchez, M., GarcõÂa, C., Vera, M. N., & Vila, J. 2002). Revisiting the James versus Cannon debate on emotion: Startle and autonomic modulation in patients with spinal cord injuries. Biological Psychology, 61, 251±269. Chwalisz, K., Diener, E., & Gallagher, D. 1988). Autonomic arousal feedback and emotional experience: Evidence from the spinal cord injured. Journal of Personality and Social Psychology, 54, 820±828. Dana, C. L. 1921). The anatomic seat of the emotions: A discussion of the James-Lange theory. Archives of Neurology and Psychiatry, 6, 634±639. Fehr, F. S., & Stern, J. A. 1970). Peripheral physiological variables and emotion: The James-Lange theory revisited. Psychological Bulletin, 74, 411±424. Hohmann, G. W. 1966). Some effects of spinal cord lesion on experienced emotional feelings. Psychophysiology, 3, 526±534. James, W. 1884). What is an emotion? Mind, 9, 188±205. Lang, P. J. 1995). The emotion probe: Studies of motivation and attention. American Psychologist, 50, 372±385. Lang, P. J., Bradley, M. M., & Cuthbert, B. N. 1989). International affective picture system IAPS): Instruction manual and affective ratings. Technical Report A-4. Gainesville, FL: Center for Research in Psychophysiology, University of Florida. Lowe, J., & Carroll, D. 1985). The effects of spinal injury on the intensity of emotional experience. British Journal of Clinical Psychology, 24, 135±136. MoltoÂ, J., MontanÄeÂs, S., Poy, R., Segarra, P., Pastor, M. C., Tormo, M. P., RamõÂrez, I., HernaÂndez, M. A., SaÂnchez, M., FernaÂndez, M. C., & Vila, J. 1999). Un nuevo meâtodo para el estudio experimental de las emociones: El International Affective Picture System IAPS). AdaptacioÂn espanäola. Revista de PsicologõÂa General y Aplicada, 52, 55±87. Montoya, P., & Schandry, R. 1994). Emotional experience and heartbeat perception in patients with spinal cord injury and control subjects. Journal of Psychophysiology, 8, 289±296. Reisenzein, R. 1983). The Schachter theory of emotion: Two decades later. Psychological Bulletin, 94, 239±264. Richards, J. S., Hirt, M. J. S., & Melamed, L. 1982). Spinal cord injury: A sensory restriction perspective. Archives of Physical Medicine and Rehabilitation, 63, 195±200. Trieschmann, R. B. 1980). Spinal cord injuries: Psychological, social and vocational adjustment. New York: Pergamon. Tucker, S. J. 1980). The psychology of spinal cord injury: Patient-staff interaction. Rehabilitation Literature, 41, 114±121.

8