Dissociation of autonomic and subjective responses to emotional slides in right hemisphere damaged patients

Pergamon

002%3932(94)E0022-G

DISSOCIATION OF AUTONOMIC AND SUBJECTIVE RESPONSES TO EMOTIONAL SLIDES IN RIGHT HEMISPHERE DAMAGED PATIENTS MARY-ELLEN *Department

of Neurology,

MEADOWS*?

and RICHARD

F. KAPLAN*:

Tufts University School of Medicine and tBoaton Boston, Masaachussetts, U.S.A.

University

School of Mcdicinc.

Abstract-Autonomic and subjective responses to emotional and neutral slides were studied in patients with right hemisphere damage (RHD), left hemisphere damage (LHD) and normal controls (CON). Orienting and habituation to a series of pure tones (1000 Hz) were also examined. All subjects showed appropriate slide recognition and there were no group differences in subjective ratings. The CON group showed higher skin conductance responses (SCRs) to the emotional slides relative to the neutral slides. while the RHD group showed lower SCRs to both sets of slides. The LHD group showed higher SCRs independent of slide type. The results support the hypothesis (HEILMAN and WATXX. Handhook c!f Neuroloq~. Elscvicr Science. 1989) that emotional paucity In RHD patients may be related to reduced autonomic arousal. However. there were no significant differences between groups in the orienting response or habituation to loud tones, suggesting that decreased arousal following RHD ia not ubiquitous.

INTRODUCTION is well documented that the integrity of the right cerebral hemisphere is important for the normal comprehension and expression of emotion. Patients with right hemisphere damage (RHD) have been shown to have difficulty judging the emotional tone of voices [22] and show deficits in the perception of facial affect [S, 9, 15, 161. RHD patients have also been observed to be less facially expressive to slides that contain emotionally charged scenes compared to left hemisphere damaged (LHD) patients [4, 61 and are impaired in the prosodic component of speech [36,39]. Despite the abundance of data implicating the right hemisphere in emotion-related behaviors, the mechanism is not well understood. HEILMAN et ~1.1231 theorized that the right hemisphere’s role in arousal may also mediate emotion. HEILMAN and WATSON [24] postulated that connections between polymodal cortical regions and limbic circuits form the basis for the role of the right hemisphere in arousal and emotion. Limbic system input into these cortical areas determines the biological significance of stimuli, while reciprocal pathways between these areas and the mesencephalic reticular systems serve to regulate arousal. Hence arousal deficits in RHD patients may underlie their paucity of emotional expression. IT

*Address for correspondence: Dr Richard F. Kaplan, 750 Washington Street, Boston. MA 021 I I. U.S.A.

Department

847

of Neurology.

New England

Medical Center,

x4x

M.-t.

M~AIXWS and R. F. KAPLAZ

Psychological theories have long recognized the importance of psychophysiological states in emotion [8, 26, 371. Studies in normals have shown that the autonomic component of emotion can be reliably obtained in response to emotional stimuli and that these responses can be modified by the psychological state of the individual [21,29,38]. However, there have been relatively few studies on the autonomic component of emotional responding in brain damaged populations. HEIL.MANet ~1. 1231 found lower baseline electrodermal activity (EDA) and lower skin conductance responses (SCRs) following mild electrical stimulation in RHD patients in comparison to LHD patients and normal controls. The LHD patients showed higher SCRs than normal controls, suggesting that left hemisphere damage may reciprocally disinhibit sympathetic arousal. MORROW et al. [31] reported a similar finding when emotional and neutral slides were presented to RHD, LHD and control patients. The RHD patients had lower SCRs to both the emotional and neutral slides compared to the LHD or CON groups, who showed greater SCRs to the emotional slides. However, in contrast to the results of HEILMANet N/. [23], the LHD group did not show increased SCRs in comparison to the control group to either the emotional or neutral slides. They also measured respiration rate. another index of autonomic responding, and found no differences between the groups. Zoccolotti and colleagues replicated these findings with respect to RHD and LHD patients but did not test normal subjects [44]. They suggested that it was unlikely that decreased SCRs in their RHD patients could be explained by impaired visual perception since these differences remained after performance on a facial affect recognition task was controlled for statistically. CALTACIRONErt ul. [7] observed lower SCRs in RHD patients compared to LHD patients or controls during the viewing of a negative film. They also reported decreased heart rate (HR) deceleration suggesting hypoarousal in both the sympathetic and parasympathetic nervous systems. Although CALTAGIRONErt ul. [7] noted that their patients were aware of the content of the films, it is not known if these patients correctly perceived the emotional valence of this material. Additionally, it was not clear from these data whether RHD patients would show altered autonomic arousal to all sensory stimulation or just to stimuli which are cognitively meaningful. ZOCCOLOTTIet trl. 1441 reported that the RHD patients showed an SCR to the first slide but not subsequent slides, suggesting preserved orienting. DAVIIIS~N et al. [ 121 recently showed that right temporal lobectomy patients showed more rapid habituation to pure tones than either left temporal lobectomy patients or controls. However, to our knowledge orienting and habituation to nonspecific stimulation following right hemisphere damage from vascular lesions has not been studied. To examine these questions, the physiological and cognitive components of emotion were studied in RHD patients. LHD patients and normal controls. Physiological arousal was studied in response to both nonspecific and cognitively meaningful stimuli. Pure tones were used as nonspecific stimuli to examine the integrity of the arousal system, while the slides comprised a class of stimuli designed to elicit the autonomic component of the emotional response. Since the emotional content of the slide rather than its physical intensity mediates the emotional response [6], these stimuli were considered specific elicitors of emotional autonomic arousal. The importance of incorporating both of these paradigms in the same study was to assess the generality of the hypothesis 1241 that RHD patients have lower phasic arousal relative to LHD patients and controls. The autonomic components studied were skin conductance responses (SCRs) and heart rate (HR) changes. The cognitive component to emotion was assessed by requiring the subjects to identify the content of the slide and to rate the slides on a scale from very pleasant to very unpleasant.

DlSSOClATlON

OF AUTONOMIC

AYI,

SUBJECTIVE

RESPONSES

TO

EMOTIOKAL

849

SLIDES

METHODS Forty-six subjects participated in the study. The 21 patients with vascular lesions were inpatients and outpatients from the Neurology and Stroke Services of the New England Medical Center, Boston, MA. Twelve patients had right hemisphere lesions (RHD) and nine patients had left hemisphere lesions (LHD). Only patients with a single unilateral vascular event confined to one hemisphere as indicated by neurological and radiographic studies were included in the hemisphere damaged groups. Twenty-five normal controls (CON) with no history of neurological disease were recruited from the community by advertising in local newsletters. The normal control group (CON) included twice the number of subjects compared to the experimental groups in order to assess potential sex ditferences. All subjects were right-handed. There were no age, sex ratio or time since disease onset differences between groups, however. there were significant differences between groups on education, with the RHD patients having had less years of schooling compared to the CON group. Table I shows the subject characteristics for the three groups. Table

1. Subject characteristics. Data are presented as means (standard deviations) variables age, education, onset and as sex ratio (male.!female) RHD

Age (years) Sex (M;F) Education (years) Onset (months) *P < 0.05 compared

63.2 (10.37) 51’7 11.0 (1.35)* 19.5 (15.39)

LHD 64.6 (11.56) 4;5 12.4 (3.97) 22.5 (19.90)

for the

CON 55.8 (11.88) 12113 14.3 (2.59)

to CON

The number of ischemic strokes due to vessel occlusion or hemorrhage was similar between the two lesion groups. Only two patients had a hemorrhagic stroke, they were both in the LHD group. Radiographs (CT or MRI scans) here available for all subjects and were read blindly. The distribution of lesion location, cortical and subcortical areas infarcted, and size of the lesion are presented in Table 2 for the two hemisphere damaged groups. The size of the lesion was classified as small if less than 10% of the hemisphere was infarcted, medium if 1(&30X was infarcted and large if greater than 30% 1431. There were no differences between the hemisphere damaged groups on relative size (x2 =0.30; d.f. = 2; PcO.86) or intrahemispheric location of lesion (z*=O.O4: d.f. = 2; PcO.98). Participation in the study required adequate language comprehension. Accordingly, all subjects performed above the cutoff for aphasia on the word discrimination and reading sentences and paragraphs subtests from the Boston Diagnostic Aphasia Examination [20]. Medications were recorded for each subject since tonic skin conductance levels (SCL) are under the influence of the cholinergic and adrenergic systems [ 141. Seven out of 12 of the RHD and 4 out of 9 of the LHD patients were taking these medications at the time of testing. This difference was not statistically significant. Only two subjects in the control group were taking similar medications. Drugs which act as alpha and beta adrenergic antagonists, cholinergic antagonists, calcium channel blockers and drugs wtth significant antichohnergic side effects may decrease tonic skin conductance levels [lS]. However. while drugs with anticholinergic side effects may influence tonic SCLs, they do not appear to affect the SCR 121. The study was approved by the Tufts-New England Medical Center Institutional Review Board. Prior to participation, the study was explained to the subject and each subject signed an informed consent. Most subjects were paid $10.00 to cover transportation costs to the Medical Center.

The subject’s hands were washed prior to the procedures with mild soap and water. Bilateral skin conductance was measured by bipolar Ag.‘AgCI electrodes (0.64 cm*) placed on the hypothenar and thenar eminences of the right and left palms; physiological saline in Unibase cream at a 0.05 molar concentration was used as the conducting medium. Heart rate was measured with commercially available AgAgCI disposable electrodes (2 active, I ground) placed on the left and right forearms. The subjects were requested to limit movement as much as posstble and a pillow was placed on their lap so as to limit any lower arm motor responses. The temperature of the testing room was maintained at 70+2-F. These procedures and recording parameters conform to suggested guidelines for psychophysiological research in humans [ 17,401. A constant voltage of 0.166 V was applied across the skin and SCLs [range @ 50 siemens (FS); sensitivity=0.02 &S] were obtained using a J & J Enterprises Physiological Monitor (model I-330) and software program interfaced to a Dell 200 personal computer. HR was digitized from the raw waveform using the same computer-based system. The system converted the time interval from the peak ofone pulse waveform to the peak of the next to a voltage representing 0 to 200 beats per min (BPM).

M.-E. Mra~mws

850

and R. F. KAPLAN

Table 2. Radiological Subject

R;L

x 9

I0 II 12 13 14 1s 16 17 18 IY 20 21 Abbreviattons:

data Size

Location

R R R R R R R R R R R R L L L L L L L L L

FrontalIBG Posterior limb IC/WM Parietal Frontal/Central Frontal.!Parietal Temporal BG.IC Posterior limb IC Frontal Parietal Caudatc Frontal;Parictal Frontal;‘CV InsulaWM Parictal;Temporal Posterior limb IC TemporalOccipital Frontal Parielal Temporal;Parietal:WM Frontal

Both Subcortical Cortical Cortical Cortical Cortical Subcortical Subcortical Cortical Cortical Subcortical Both Cortical Subcortical Cortical Subcortical Cortical Cortical Cortical Both Cortical

BG = Basal Ganglia;

IC = Internal

Capsule:

WM = White Matter:

Large Small Medium Medium Large Medium Large Small Small Small Small Medium Small Small Medium Small Large Medium Medium Large NA

NA = Not Available

Subjects were seated comfortably in a dimly lit room with a projection screen 4 feet in front of them. The room used for testing was a standard examining room with no extraneous distracters in the subject’s visual field. The experimenter and equipment were located behind the subject. There was a 10 min acclimation period after briefing the subjects on the experimental procedures. Autlitor~ huhifuarion. Following the acclimation period. earphones were placed over the subject’s ears and I4 tones (1000 Hz, 100 dB, 1000 msec) were presented binaurally over the course of6 min. The intertone intervals were randomly varied with a range of I t&25 set (mean = 16.5 set: S.D. =4.6) and the intervals were the same for each subject. Subjects were told to sit back, relax and to try to ignore the tones. The presentation of the tones was synchronized to the computer and SCLs (/tS) were obtained just prior to and immediately after the presentation of the tone for 10 sec. Five data points were sampled and recorded per second and the mean. standard deviation, maximum and minimum calculated. Pictoriul slides. One practice slide was shown of neutral content in order to acchmatc the subjects to the procedures. Twenty-four slides were then presented in a pseudo-random order (I6 scenic neutral; 8 emotional) with a random IO-~15 set interstimulus interval. The shdes shown were either unpleasant (i.e. a starving child) or neutral (i.e. a scenic landscape). The unpleasant slides w’ere previously effective in a study ofeliciting facial expressions 161. A I:2 ratio ofemotional:neutral slides was utilized in order to increase the probability ofan autonomic response to the emotional slides. As the slide was presented on the screen SCL and HR were recorded for 10 set in a manner identical to that discussed above and the subjects were instructed to remain quiet until instructed to respond. After the IO set recording period the subjects wcrc required to identify the content of the slide and rate it on a rating scale from I&very plcasant to Y-very unpleasant as to how it made them feel. The rating acalc was a Likcrt-type scale printed on an 8.5” x I I” sheet of paper placed on a music stand in a vertical orientation to the front and side of the subject. The interstimulus interval began after the subject identified and rated the slide.

RESLJLTS Baseline

ps~~choplzysiological

lecels

Baseline measures of skin conductance levels (SCLs) and HR were obtained from a 10 see period just prior to the auditory habituation series. A 3 x 2 analysis of variance (ANOVA) [27] with side of recording as the within subjects factor showed no differences for group; however, a significant sex difference on this measure was obtained [F (1, 39)= 19.53; P < O.OOl] with the males having higher SCLs compared to the females. There was no group

by sex interaction. There was also a within subjects effect for side of recording [F (1, 39)= 8.01; P
x52

M-E.

MI.AI)OWS and R. F. KAPLAY

[F (I, 38)= 778.62; P
RHD W El

LHD

CON

Emotional Neutral

The mean responses of the SCRs to both slide types arc shown in Fig. 2. An ANOVA with group and sex as the between subject factors and slide type and side of recording as the within subject factors showed significant main effects for group [F (2, 37)=4.66; P-cO.031and within subject main effects for slide type [F (1, 37) = 4.99: P < 0.031 and a slide type by group interaction [F(2, 37)=4.30; P
0.6

0.0 RHD

LHD

CON

n Emotional PI

Neutral

Fig. 2. Mean SC‘Rs for the three groups to the emotional and neutral pictorial slides

DISSOCIATION

OF AUTONOMIC

AND

SUBJECTIVE

RESPONSES TO EMOTIONAL

SLIDES

853

Difference r-tests, showed that all three groups differed on both the emotional and neutral slides. For the emotional slides, the RHD group had significantly (P
DISCUSSION Whereas RHD patients showed appropriate cognitive labeling of emotionally charged slides, their SCRs were lower in comparison to both LHD patients and normal controls. Moreover, this was not reflective of a general state of decreased arousal because there were no comparable differences in baseline SCL, orienting and habituation among the three groups. All three groups appropriately identified the slides and did not differ in their affective ratings of these photographs. Other studies have also shown that RHD patients are able to appropriately infer affective judgments [3,4, lo]. What differentiates these tasks from tasks in which the RHD patient misperceives the emotional content of the stimulus? Using a level of processing analysis, we know the RHD patients correctly recognized the information in each slide because they did not differ from normals in the labeling of the slide. We propose that in this task, rating the information required minimal additional processing since once the slide was identified its affective interpretation was unambiguous. For example, the picture of a burnt baby, by definition, is unpleasant. Thus, as Blonder et al. demonstrated, RHD patients are capable of emotionally processing denotative information [3]. Although our RHD patients correctly labeled the affect associated with the slides, they showed reduced electrodermal responding to both the emotional and neutrai slides. Electrodermal activity can be elicited by three central pathways: a premotor cortico-spinal system, a limbo-hypothalamic system and a system within the reticular formation [14]. Although the limbic-hypothalamic pathway probably mediates the electrodermal response to emotional stimuli [14], when the SCR is driven by visual stimuli, i.e. emotional slides, we can assume this pathway comes under cortical control [42]. The activation of this system would most likely occur through the polymodal association cortex in the parietal lobes which have extensive connections to limbic structures [30], including the cingulate gyrus and

854

M.-E.MLWOWS and R. F. KAPLAN

the amygdala. The limbic system regulates electrodermal activity via both hypothalamic and reticular activating system connections to the sympathetic nervous system [ 18]. Feedback from the autonomic nervous system would in turn contribute to the physiological component of the emotional experience 126, 28, 371. In their classic paper, SCHACTER and SINGER[37] proposed that emotional states needed to be defined in terms of the state of physiological arousal and a cognition appropriate to that arousal state. In this context, the RHD patient remains capable of assigning the appropriate cognitive label but they are neither generating nor receiving the appropriate autonomic responses and feedback inherent in normal emotion. Similarly, individuals with spinal cord lesions, which result in a reduction in sympathetic nervous system feedback, reported emotional feelings but also reported that the intensity of their feelings were reduced [25]. Although our RHD patients had lower SCRs to the emotional slides, their orienting response to loud tones was comparable to that of the LHD and CON groups. Z~CC~L~TTIet al. 1441 observed a similar phenomena in that their RHD patients responded to the initial slide, independent of content, but not subsequent slides. While these data support the role of the right hemisphere in mediating arousal 123,241, they suggest that this role may be limited to arousal associated with higher cortical functioning. PAVLOV [34]referred to the orienting response as the “what is it reflex” because it occurred in response to the slightest change in the environment. However, arousal to an orienting stimulus does not necessarily involve cortical pathways [35]. The acoustic startle response in the rat, for example, is mediated by a lower brain stem neuronal pathway [ 131. Our data suggests that physiological arousal associated with the orienting response can be differentiated from the physiological arousal associated with the construct of cerebral activation [l 1] and that only the latter is affected by right hemisphere damage. Our three groups also showed comparable habituation curves to the series of loud tones. These data differed from the data of DAVIDSON et al. [12] who reported more rapid habituation in their right temporal lobectomy patients. However, direct comparisons are difficult because of differences in the location and type of brain lesion as well as differences in stimulus intensity, 100 vs 60 db. While this and previous studies [7, 3 1,441 have consistently shown lower SCRs in RHD patients to stimuli conveying negative affect, our results with regard to the LHD patients appear discordant with those of previous studies. Both MORROW et al.[31] and CALTACIRONE et ul. [7] reported that their LHD patients showed greater SCRs to the emotional stimuli relative to the neutral stimuli; a finding we did not replicate. Like other studies [7, 311, we found that SCRs in LHD patients were lower compared to controls with respect to the emotional slides, however, there were no differences in this group between slide type. In fact only our normal control group showed a pattern of autonomic differentiation between the two slide types. We think this was interesting finding since it demonstrated that both LHD and RHD patients failed to show autonomic discrimination between the emotional and neutral slides. At this point, however, an explanation for the discrepancy between our results and those discussed above with respect to the LHD patients is not apparent. Nevertheless, it is important to note that all these studies showed that lesions to either hemisphere resulted in a pattern of autonomic dysregulation. To our knowledge, only one other study [7] examined heart rate changes in hemispheric damaged patients in response to emotionally charged material. These investigators showed that RHD patients had less of a HR deceleration compared to LHD patients and controls during a negative film. In contrast, we found a significant HR deceleration to the emotional

“lSSOC,AT,ON

OF AUTONOMIC

ANO

SUBJECTIVE

RESPONSESTO LMOTlO&ALSLII1FS

855

slides compared to the neutral slides but no group differences. It is important to note, that despite the group differences reported by CALTAGIR~NE [7], the magnitude of heart rate deceleration for their RHD group was considerably greater than any of our groups. This may be related to differences in our sampling times. We sampled heart rate changes for a 5-set after stimulus onset, whereas CALTAGIRONEet al. used a 20-set sampling period. It is possible that our shorter sampling period obscured the HR differences between the groups. In conclusion, the findings suggest that the paucity of emotion in RHD patients may be related to an inability to generate the normal autonomic arousal associated with an emotional event rather than an inability to recognize the emotional content of that event. Moreover, the arousal deficit is not ubiquitous and may only encompass arousal that is cortically mediated. Ackno~clrdSrments-Supported in part by BRSG S07-RR05598-21

awarded by the Biomedical Research Support Program, Division of Research Resources, National Institutes of Health. The authors would like to thank Drs Harold Goodglass, Mieke Verfaellie, Louis Caplan, Marlene Oscar-Berman, Jacqueline Liederman and Samuel Sokol for their suggestions and criticisms. We would also like to thank Dr Louis Caplan for reading the radiographs and for patient referrals, and Drs Michael Pessin and L. Dana Dewitt for patient referrals.

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