ابراز هیجانی مطرح عروضی در بیماران سکته مغزی یک طرفه: بازیابی، محل ضایعه، و درک عاطفی

Abstract Recovery of emotional functioning following stroke has received limited attention in the neuropsychological literature. By emotional functioning, we refer to a range of processing modes, including perception, expression, experience, and behavior. The aim of the current study was to evaluate the course of prosodic emotional expression over time in individuals with stroke. Posed prosodic expression tasks from the New York Emotion Battery were administered to right brain-damaged (RBD), left brain-damaged (LBD), and demographically matched normal control (NC) participants at two separate testing times (median interval of 25 months). Posers (i.e., individuals producing the emotional expressions) were required to produce neutral-content sentences using four different emotional tones (happiness, sadness, anger, and fear). Raters judged poser output for accuracy, intensity, and confidence. For accuracy ratings, RBDs and LBDs were impaired relative to NCs at baseline. In terms of recovery, there was a tendency for LBDs to improve over time, and there was a significant decline for RBDs. Inspection of the group mean data suggested that frontal lesions had a negative impact on prosodic emotional expression in RBDs and that lesion extent did not systematically influence performance at baseline or over time. Participants maintained their relative standing on the NYEB expression tasks over time. Finally, no significant relationships were found between participant performance on prosodic emotional perception and expression tasks at either testing time, suggesting that these two processing modes are relatively independent

Introduction Despite an ever-increasing literature on the recovery of brain functions following stroke, there are relatively few investigations on the recovery of emotional functioning. Emotional processing is an integral component of behavioral and psychological adaptation necessary for learning, motivation, coping, and decision-making. Thus, increasing our understanding of emotional sequelae following stroke is important (e.g., Eslinger, Parkinson, & Shamay, 2002). Previous research examining speech and language functions in aphasic patients (e.g., Fazzini, Bachman, & Alpert, 1986) has shown that whereas most spontaneous recovery occurs in the first 6 months following stroke, significant improvement can continue to take place several years after stroke (Kertesz, 1993). Moreover, neuroimaging studies have demonstrated a complex pattern of brain reorganization subsequent to recovery from stroke that can be viewed as a mechanism enabling recovery (e.g., Chollet et al., 1991 and Weiller, 1995). The course of functional recovery following stroke is uncertain and may depend on a number of factors, including lesion location (Nelson, Cicchetti, Satz, Sowa, & Mitrushina, 1994) and environmental variables (Eslinger et al., 2002). For instance, Nelson et al. (1994) assessed behavioral disturbance (e.g., depression, mania, and indifference) in left brain-damaged (LBD) and right brain-damaged (RBD) patients at 2-week, 2-month, and 6-month intervals. Their findings revealed differential recovery rates, depending on hemispheric side of lesion. Initially, LBDs exhibited a slower rate of recovery, as compared to RBDs; however, at 6 months post-stroke onset, the rate of recovery for the LBDs stabilized, whereas the RBDs continued to demonstrate functional decline. Few studies have examined the recovery of prosodic emotional expression, however, aprosodia is a condition commonly observed in stroke patients. Although case reports have documented recovery of prosodic functioning, aprosodia can persist (Hughes, Chan, & Su, 1983). Ross and Mesulam (1979) described two patients with aprosodia following a right-hemisphere lesion. One regained the ability to express emotion 8 months later, but the second did not show improvement at a 5-year follow-up. Egelko et al. (1989) investigated the recovery of facial and prosodic affective comprehension in RBD, LBD, and normal control (NC) participants and reported improvements in facial perception in RBDs but not in LBDs. More recently, a study of facial, prosodic, and lexical emotional perception conducted in our laboratory (Zgaljardic, Borod, & Sliwinski, 2002) revealed limited recovery, whereby RBDs significantly improved relative to LBDs and NCs, but only on lexical perception tasks. The current study extended previous work from our laboratory by focusing on the recovery of emotional expression. Posed prosodic emotional expression tasks from the New York Emotion Battery (NYEB; Borod, Welkowitz, & Obler, 1992) were administered, on two separate occasions, to individuals with unilateral stroke and to demographically matched NCs. The prosodic output was later evaluated by raters for accuracy and intensity of emotional expression. A second objective of this study was to investigate brain lateralization of prosodic emotional expression functions. The literature on prosodic expression in brain-damaged patients points to the right hemisphere as dominant for this function (e.g., Blonder, Pickering, Heath, Smith, & Butler, 1995; Borod, Bloom, Brickman, Nakhutina, & Curko, 2002; Borod, Koff, Lorch, & Nicholas, 1985; Gorelick & Ross, 1987; Ross, 1993 and Ross, 1997; Ross & Mesulam, 1979; Schmitt, Hartje, & Willmes, 1997; Tucker, Watson, & Heilman, 1977). These findings have been corroborated by studies that have employed a wide variety of methods: (a) the Wada technique (Ross, Edmondson, Siebert, & Homan, 1988), (b) progressively reduced verbal-articulatory conditions (Ross, Thompson, & Yenkosky, 1997), (c) acoustical analysis of fundamental frequency (Pell, 1999a and Pell, 1999b), and (d) the examination of the use of tonal languages, such as Chinese and Thai (Gandour, Larsen, Dechongkit, Ponglorpisit, & Khunadorn, 1995). When examining site of lesion, there is considerable literature implicating frontal brain structures in the expression of emotion (e.g., Hornak, Rolls, & Wade, 1996; Kolb & Taylor, 1990; Pick, Borod, Ehrlichman, & Bloom, 2003; Wasserman, Borod, & Winnick, 1998; Weddell, Miller, & Trevarthen, 1990) and some specifically within the right hemisphere (Borod, 1993, Borod et al., 1985, Ross, 1985 and Ross, 1997; Ross & Rush, 1981). In spite of these findings, the right-hemisphere hypothesis has not received unequivocal support (e.g., Borod et al., 2002a and Borod et al., 2002b; Bradvik et al., 1991, Davidson, 1984 and Heller, 1990; Kinsbourne & Bemporad, 1984). For instance, Van Lancker and Sidtis (1992) suggested that prosodic processes involve multiple functions that are distributed across the two cerebral hemispheres. Moreover, several brain structures, regardless of hemispheric location, have been implicated as playing an important role in the ability to express emotion through prosody. These include the supra-Sylvian region (Ross, 1985), deep white matter below the supplemental motor area (Ross et al., 1997), and the basal ganglia (Cancelliere & Kertesz, 1990). Thus, identifying brain structures that are critical for prosodic emotional expression remains a relevant objective in emotion research. The current study will explore the role of intra-hemispheric sites, while focusing on investigating hemispheric specialization for this function. The third objective of the current study was to examine the relationship between expressive and perceptual prosodic emotion. Research using brain-damaged and NC participants has demonstrated that a lesion may affect one mode but not the other (Borod, 1993; Borod, Koff, Lorch, & Nicholas, 1986; Gainotti, 1987 and Ross, 1981; Ross & Mesulam, 1979). Furthermore, findings in RBDs have suggested a dissociation, whereby emotional expression may be subserved by anterior brain structures and emotional perception by posterior structures (Ross, 1985 and Ross, 1997; Ross & Rush, 1981). The relationship between posed prosodic emotional perception and expression was previously explored by Borod, Welkowitz, et al. (1990) in RBD, Parkinson's disease, depressed, and schizophrenic patients, as well as healthy controls, but no significant relationships were reported. The current study examined this same relationship in RBDs, LBDs, and NCs, utilizing perception data from an earlier study (Zgaljardic et al., 2002). In summary, the current study had the following objectives: (1) to examine the recovery of prosodic emotional expression function in stroke patients; (2) to investigate hemispheric lateralization for posed prosodic emotional expression; and (3) to examine the relationship between expressive and perceptual modes of prosodic emotional processing.

4. Results 4.1. Inter-rater reliability Since IRR was substantial for all experimental and control variables, mean rating scores were computed across raters, separately, for each emotional parameter and across raters for each intonation contour (see Table 3). Table 3. Inter-rater reliability Emotion tasks Intonation contours Accuracyb (%) Intensitya Confidencea Accuracyb (%) Training trials 76 .95 .75 86 Experimental trials 74 .82 .63 86 a Intra-class correlations. b Percent complete agreement. Table options 4.2. Inter-hemispheric site of lesion Repeated-measures ANOVAs were performed to assess recovery for prosodic emotional expression separately for intensity, accuracy, and confidence. For each variable, a 3 × 2 × 4 ANOVA was conducted with one between-subjects factor, Group (RBD, LBD, and NC), and two within-subjects factors, Time (T1 and T2) and Expression Type (happiness, anger, fear, and sadness). Post hoc tests were conducted for statistically significant findings. Before conducting the experimental analyses, the non-emotional control tasks (i.e., neutral expression and Intonation Contours) were analyzed to see whether there were significant group differences. When one-way ANOVAs were computed for Group (NC, RBD, and LBD) at T1 and T2, none of the findings was significant. Thus, it was not necessary to covary for control task performance in the experimental task analyses to follow. 4.2.1. Intensity For intensity, a significant main effect of Emotion was found, F (3, 63) = 38.53, p < .001, such that anger (M = 3.46, S.E. = .17) was expressed more intensely (p < .001) than happiness (M = 3.3, S.E. = .16), followed by fear (M = 3.08, S.E. = .12) and sadness (M = 2.16, S.E. = .11). Post hoc pairwise tests revealed significant differences (p < .001) for all comparisons except for two (anger versus happiness, and fear versus happiness). Although, the three-way interaction revealed a statistical trend, F (6, 63) = 2.09, p = .067, protected t-test post hoc comparisons ( Welkowitz, Ewen, & Cohen, 1976) did not reveal any evidence for recovery. 4.2.2. Accuracy For accuracy, a significant main effect of Emotion was found, F (3, 63) = 8.87, p < .001, such that post hoc pairwise tests revealed significant differences (p < .05) among all comparisons except for two (anger [M = .59, S.E. = .07] versus happiness [M = .48, S.E. = .06; p = .06], and sadness [M = .67, S.E. = .05] versus anger [p = .463]). 3 There was also a significant Group by Time interaction, F (2, 21) = 4.46, p = .024 (see Fig. 1). Using the protected t-test, when examining differences between testing times, LBDs demonstrated an increase (p < .10) from T1 (M = .46, S.E. = .06) to T2 (M = .55, S.E. = .07), whereas RBDs demonstrated a significant decrease (p < .05) from T1 (M = .49, S.E. = .06) to T2 (M = .39, S.E. = .07), and NCs showed no significant difference (T1: M = .64, S.E. = .07, and T2: M = .59, S.E. = .08). When examining group differences, for T1, RBDs and LBDs were each significantly (p < .01) less accurate than NCs. At T2, RBDs were significantly (p < .01) less accurate than both NCs and LBDs. Means for accuracy at Time 1 and Time 2 for RBDs, LBDs, and NCs. Fig. 1. Means for accuracy at Time 1 and Time 2 for RBDs, LBDs, and NCs. Figure options 4.2.3. Confidence For the confidence rating, there were no significant main effects or interactions. The main effect of Group was not significant, with group means as follows: RBDs (M = 3.36, S.E. = .08), LBDs (M = 3.48, S.E. = .09), and NCs (M = 3.40, S.E. = .09). 4.3. Intra-hemispheric site of lesion 4.3.1. Frontal lobe involvement We examined whether individuals with frontal lobe lesions (four RBD and four LBD) were more impaired than those without frontal lobe lesions (four RBD and four LBD), using visual inspection of group means (see Table 4). Using this descriptive approach, the mean group performance of frontal patients was compared to that of non-frontal patients for each parameter at each testing time (3 × 2 comparisons). The data showed that in five out of six comparisons, RBDs with frontal lesions were more impaired than RBDs without frontal lesions. However, the opposite pattern occurred for LBDs, where in all six comparisons, patients with frontal pathology performed better than those without frontal lobe involvement. Table 4. Means (and standard deviations) for the three parameters at Time 1 and Time 2 for RBDs and LBDs with frontal and non-frontal lesions Parameter Site of lesion RBDs T1 RBDs T2 LBDs T1 LBDs T2 Accuracy Non-frontal 0.51 (.11) 0.43 (.22) 0.43 (.10) 0.49 (.27) Frontal 0.45 (.23) 0.33 (.20) 0.50 (.25) 0.61 (.20) Intensity Non-frontal 3.06 (.51) 3.15 (.70) 2.51 (.23) 2.86 (.63) Frontal 2.93 (.77) 2.98 (1.12) 3.25 (.84) 3.06 (.35) Confidence Non-frontal 3.11 (.26) 3.41 (.20) 3.46 (.32) 3.31 (.13) Frontal 3.33 (.36) 3.33 (.36) 3.50 (.42) 3.63 (.13) Table options 4.3.2. Number of lesion sites We also examined recovery, based upon the number of lesion sites involved. Table 5 provides the means and standard deviations for patient groups at T1 and T2 for all three emotion parameters as a function of the number of lesion sites (i.e., 1–2 versus 3 or more). Based on findings of Ross (1981) and Ross and Mesulam (1979), we expected that RBDs with fewer lesions would demonstrate greater recovery than RBDs with more extensive lesions. For this analysis, group performance at T1 was compared to group performance at T2 for each parameter, for each of the patient subgroups (i.e., 1–2 and 3 or more lesions; 3 × 2 comparisons). For RBDs with fewer lesions, there was improvement over time in two out of three comparisons. By contrast, for RBDs with more lesions, there was a decline in performance over time in two out of three comparisons. For LBDs, regardless of the number of lesion sites, in five out of six comparisons, there was improvement over time. Table 5. Means (and standard deviations) for both patient groups at Time 1 and Time 2 for all three parameters as a function of the number of lesion sites (i.e., 1–2 vs. 3 or more) Parameter Number of lesion sites RBDs T1 RBDs T2 LBDs T1 LBDs T2 Accuracy 1–2 0.50 (.11) 0.39 (.18) 0.41 (.10) 0.53 (.27) 3+ 0.46 (.23) 0.36 (.25) 0.55 (.28) 0.58 (.24) Intensity 1–2 2.79 (.60) 3.03 (.66) 2.85 (.78) 2.97 (.59) 3+ 3.20 (.64) 3.10 (1.15) 2.93 (.68) 2.95 (.33) Confidence 1–2 3.08 (.23) 3.29 (.15) 3.54 (.33) 3.34 (.13) 3+ 3.36 (.34) 3.45 (.37) 3.38 (.43) 3.68 (.06) Table options Finally, we looked at whether the number of lesion sites involved affected the level of performance on prosodic emotional expression tasks (see Table 5). Performance of the patients with 1–2 lesions was compared to the performance of the patients with 3 or more lesions for each parameter at each testing time, separately for each patient group (3 × 2 × 2 comparisons). When these comparisons were made, there were 8 out of 12 instances in which the patients with more lesion sites performed better than those with fewer sites. Thus, these data do not suggest that the more lesion sites involved, the poorer the performance on these emotional expression tasks. 4.4. Relationship between perception and expression Pearson product–moment correlations were performed for all participants between performance accuracy on emotional expression and perception tasks at T1 and T2.4 Correlation coefficients, using the mean of the four emotions, were non-significant for both T1 and T2. Furthermore, when individual emotions were examined, none of the correlations between the processing modes was significant (see Table 6). Table 6. Relationships between emotional expression and perception accuracy for all participants Time of testing Mean of four emotions Happiness Sadness Anger Fear T1 r .27 .18 .03 −.23 .25 p .20 .39 .88 .28 .24 T2 r .32 .14 .23 .17 .06 p .12 .53 .27 .44 .79 Table options 4.5. Supplementary analysis On an exploratory basis, we correlated participants’ performance at T1 with their performance at T2 in order to examine the stability of individual performance relative to other group members on NYEB tasks over time. Examining this trajectory would further shed light on the course that emotional functioning takes following stroke. We predicted that if correlations were positive and significant, it would suggest that individuals maintained their relative standing on this expression task over time. Pearson product–moment correlations were computed between performance at T1 and T2 for all posers, separately for accuracy, intensity, and confidence. For all parameters, correlations were conducted using the average rating for the four emotions under study. Results indicated significant positive correlations for each parameter: accuracy: r = .71, d.f. = 22, p < .001; intensity: r = .62, d.f. = 22, p < .001; and confidence: r = .45, d.f. = 22, p = .027.