- Email: [email protected]
Is “reading mind in the eyes” impaired in Parkinson’s disease?
Parkinsonism and Related Disorders 17 (2011) 246e248
Contents lists available at ScienceDirect
Parkinsonism and Related Disorders journal homepage: www.elsevier.com/locate/parkreldis
Is “reading mind in the eyes” impaired in Parkinson’s disease?q Natsuko Tsuruya a, Mutsutaka Kobayakawa a, b, Mitsuru Kawamura a, * a b
Department of Neurology, Showa University School of Medicine, 1-5-8 Hatanodai, Shinagawa-ku, Tokyo, Japan Brain Science Institute, Tamagawa University, Tokyo, Japan
a r t i c l e i n f o
a b s t r a c t
Article history: Received 12 July 2010 Received in revised form 4 September 2010 Accepted 8 September 2010
Theory of mind (ToM) is the specific cognitive ability to understand other people’s mental states. Several studies have examined ToM ability in patients with Parkinson’s disease (PD), using the “reading mind in the eyes” test (RMET). However, there has been no agreement as to whether or not ToM ability in this task is affected by PD. In order to obtain conclusive evidence regarding ToM ability in PD, we examined RMET-related performance in nondemented PD patients; we also used the semantic discrimination task to exclude the possibility that PD patients had difficulty in distinguishing emotional adjectives. Results indicated that ToM ability in the RMET is impaired in PD patients, and that this finding was not attributable to the visual processing of faces or the verbal comprehension of emotional adjectives. Thus, the affective aspects of ToM can be impaired in PD patients. Ó 2010 Elsevier Ltd. All rights reserved.
Keywords: Theory of mind Reading mind in the eyes Social cognition Parkinson’s disease
1. Introduction Theory of mind (ToM) is the specific cognitive ability to perceive others’ mental states. In recent years, ToM ability has been increasingly investigated in various neurological diseases, and several studies have shown that ToM ability is affected by Parkinson’s disease (PD) [1,2]. One of the most popular means of assessing ToM ability is the “Reading mind in the eyes” test (RMET). In the RMET, subjects must infer the mental states of a person in a photograph that shows only the subject’s eye region. In the current literature, there is no agreement as to whether or not RMET performance is impaired by PD. Two studies report that PD patients could correctly recognize what others were thinking, from their eye gaze [3,4]. On the other hand, 3 studies, including ours, have reported that PD patients show impairment in the RMET [5,6]. Bodden et al. showed that in relatively advanced stages of PD, patients exhibited impairment in the RMET [7]. Our previous study showed the presence of RMET impairment in PD patients by using the 2-choice version of the RMET. Additionally, 1 study showed that PD patients had difficulty in the RMET, but only after undergoing subthalamic nucleus-deepbrain surgery [8]. Thus far, there is no specific evidence that PD patients, especially those in the early stages of PD, exhibit RMET impairment.
In the present study, we aimed to obtain conclusive evidence regarding mind-reading ability in early PD. First, we recruited nondemented PD patients because in order to infer the mental states of others, several cognitive processes other than ToM ability must be intact. Second, we included the semantic discrimination task as a control task. The RMET involves not only the visual processing of faces but also the ability to discriminate similar emotional adjectives. In most of the previous studies, faceperception ability was determined using the gender-discrimination task; the ability to discriminate emotional adjectives, however, was not determined. Because the RMET uses comparatively unfamiliar words as the target and foils, lexical ability should first be guaranteed through an appropriate task. Third, we recruited patients who were in the earlier stages of PD than those recruited by previous studies. As mentioned above, there is no specific evidence that early PD patients exhibit RMET impairment. Because the RMET is believed to assess the affective aspect of the ToM ability, defective performances in the RMET would indicate the dysfunctions in emotional processing in PD patients. This would support the notion that in the early course of PD, pathological changes are found in the emotional system such as the limbic areas, including the amygdala [9]. 2. Methods 2.1. Subjects
q The review of this paper was entirely handled by an Associate Editor, Eng-King Tan. * Corresponding author. Tel./fax: þ81 3 3784 8710. E-mail address: [email protected] (M. Kawamura). 1353-8020/$ e see front matter Ó 2010 Elsevier Ltd. All rights reserved. doi:10.1016/j.parkreldis.2010.09.001
Twenty PD patients were recruited from among outpatients diagnosed and under treatment at Showa University Hospital (Table 1). All patients were being treated with levodopa or a dopamine agonist, and the experiment was conducted during the “on” state of medication. None of the patients had a history of impulse
N. Tsuruya et al. / Parkinsonism and Related Disorders 17 (2011) 246e248
247
Table 1 Summary of study participants. PD
NC
Mean
SD
Mean
SD
PD vs. NC (significance)
N Men Women Age (y) Years of education HoehneYahr stage Disease duration (y) MMSE WCST category achievement SDS ReyeOsterrieth Complex Figure test LD daily dose (mg) DA daily dose (mg)
11 9
11 9
70.5 14.8 1.5 5.1 28.3 5.1 34.0 34.5
8.6 2.8 0.7 0.7 1.6 1.3 8.4 1.2
265.0 192.0
122.6 163.4
e e
Total LEDD
457.0
207.7
e
67.7 13.7 e e 28.6 3.6a 32.1 34.4
n.s. 4.5 2.2
n.s. n.s.
2.0 2.1 8.5 2.1
n.s. e n.s. n.s.
PD, Parkinson’s disease; NC, normal control; SD, standard deviation; n.s., not significant; MMSE, Mini-Mental State Examination; WCST, Wisconsin Card-Sorting Test; SDS, Self-rating Depression Scale; LD, levodopa; DA, dopamine agonist; LEDD, levodopa equivalent daily dose. a Mimura et al. [5]. control disorder or other psychiatric symptoms. Disease severity corresponded to HoehneYahr stages IeIII (stage I, 13 patients; stage II, 5 patients; stage III, 2 patients) [10]. Global cognitive function was evaluated using the Mini-Mental State Examination (MMSE) [11], and severity of depression was assessed using the Zung Selfrating Depression Scale (SDS) [12]. Visuoperceptual ability was assessed using the ReyeOsterrieth Complex Figure test [13]. The Wisconsin Card-Sorting Test [14] was conducted to assess executive function. We also recruited 20 healthy subjects who were matched for age, gender, and educational background (Table 1). They were enlisted through an agency working with senior citizens and were financially compensated for their participation. None of the normal control (NC) subjects had a history of neurological or psychiatric disorders; their global cognitive functions were evaluated using the MMSE, and the presence of depression was measured using the SDS. Visuoperceptual ability was assessed using the ReyeOsterrieth Complex Figure test [13]. All PD patients and NC subjects were Japanese. Written informed consent was obtained from all participants, and the study protocols were approved by the Showa University Ethics Committee. 2.2. “Reading the mind in the eyes” test To examine participants’ ability to infer the mental states of others, we developed a Japanese adaptation of the revised version of the RMET [15]. The task comprised 20 photographs of the eye region of the faces of Japanese actors, each printed on a separate paper. Four adjectives corresponding to complex mental state descriptors (e.g., “hateful,” “panicked”) were printed on each paper. One of four words (the target word) correctly described the mental state of the person in the photograph. The “correct” word was decided in the pilot study, under the criterion that at least 5 out of 8 judges agreed that the word was the most suitable for each picture. Participants were required to decide which of the 4 words best described what the individual in the photograph was thinking or feeling. There was no time limit for responses. As a control task, we assessed subjects’ lexical ability to understand the meanings of target and foil words (i.e., semantic discrimination task). The participants were required to choose which of 4 words was the most similar in meaning to the target word. The participants also judged the gender of the person shown in the photograph (i.e., gender attribution task), because general deficits in facial perception can affect the main task. The participants were required to judge the gender of the person shown in the photographs used in the RMET. 2.3. Statistical analysis Data are expressed as means (standard deviation [SD]) for the continuous variables. Intergroup differences (PD vs. NC) in demographic and clinical data and in cognitive and behavioral characteristics were analyzed using independent sample t tests. Associations between the scores on the RMET and the demographics, clinical data, and cognitive variables were analyzed with Spearman’s rank correlations.
3. Results The scores of the basic neuropsychological tests of the PD patients were within the normal range (Table 1).
Fig. 1. Performances in the “reading mind in the eyes” test and control tasks. In the RMET, the performances of PD patients were worse than those of NC subjects. Meanwhile, there were no significant differences between the 2 groups in terms of performance in either the semantic discrimination task or the gender attribution task.
On the RMET, PD patients performed significantly worse than the NC subjects (13.5 [2.6] vs. 15.5 [1.6], t(32) ¼ 2.92, P < 0.01; Fig. 1). Meanwhile, performances in the semantic discrimination and gender attribution tasks were not significantly different between PD patients and NC subjects (19.2 [1.2] vs. 19.6 [0.8], t (32) ¼ 1.44, P > 0.1; 18.5 [2.0] vs. 18.5 [1.7], t(38) ¼ 0, P > 0.1, respectively). In order to investigate if early PD influences performance on the RMET test, we analyzed the data limited to patients with Hoehn & Yahr stage I (N ¼ 13). The result showed the same pattern; PD patients performed worse than NC subjects in the RMET test (13.2 [2.7] vs. 15.5 [1.6], t(31) ¼ 3.11, P < 0.01), but not in the semantic discrimination and gender attribution tasks (19.1 [1.4] vs. 19.6 [0.8], t(16.7) ¼ 1.25, P > 0.1; 18.7 [1.7] vs. 18.5 [1.7], t(31) ¼ 0.31, P > 0.1, respectively). There were no significant correlations between the RMET scores and other demographic variables, such as age, gender, or education level. Neither was there any correlation between the RMET scores and other cognitive tasks. 4. Discussion and conclusion PD patients showed impairment in the RMET, but they could perform as well as NC subjects in the semantic discrimination and gender attribution tasks. This result indicated that the ability to infer the mental states of others was impaired in PD patients and that this impairment was not attributable to a failure to discriminate emotional adjectives or to perceptual problems in visually analyzing the eye-gaze region. Moreover, we could find no correlation between the RMET scores and the clinical or demographic data, or the other cognitive tasks. This would imply that the impairment revealed by the RMET is specific to a ToM component in our PD patients, rather than a secondary consequence of other cognitive deficits. ToM ability can be divided into 2 subcomponents: “cognitive ToM” and “affective ToM.” Cognitive ToM is thought to require cognitive understanding of another’s mental state, while affective ToM requires an empathic appreciation of the listener’s emotional state [2]. The RMET is considered to measure affective ToM. In order to investigate the affective side of ToM ability, we should exclude the influences of cognitive factors as much as possible. To date, reported RMET studies have differed in several ways, including the languages and stimuli used and the number of trials involved. Although the general procedure is identical, several factors could bring about differences in RMET results. Therefore, it is important
248
N. Tsuruya et al. / Parkinsonism and Related Disorders 17 (2011) 246e248
to verify the basic cognitive abilities of PD patients. We introduced the semantic discrimination task to examine the participants’ lexical ability to distinguish emotional adjectives. The task sensitivity for ToM ability may decrease if the choices in the RMET are lexically too difficult to distinguish. Some of the previous studies used a glossary to which participants referred when they did not understand the meaning of the choices. However, we consider this insufficient, as participants might not have referred to the glossary when they misunderstood the meanings of the choices. We believe that using the semantic discrimination task is a direct way of controlling and assessing the participants’ lexical ability. The present result indicated that affective ToM could be impaired in PD patients. The ToM network includes the medial prefrontal cortex, superior temporal sulcus region, temporoparietal junction, temporal pole, and amygdala [2]. Pathological changes in PD can result in dysfunction in the affective ToM network. For example, dysfunctions in the mesocorticolimbic dopaminergic pathwaydwhich projects from the ventral tegmental area to the nucleus accumbens, amygdala, and medial prefrontal cortexdis associated with emotional impairment in PD patients [16]. Accumulations of Lewy bodies could also be a possible cause of limbic dysfunction; they are found in the amygdala and surrounding limbic structures as early as the presymptomatic stage of PD [9]. In conclusion, the present result indicated that ToM deficits could be observed in PD patients lacking cognitive deterioration. These results are consistent with the notion that limbic lesions and emotional impairment are observed in patients with early PD [1,9].
Acknowledgements This study was supported by a grant from the Tamagawa University Center of Excellence under the Ministry of Education, Culture, Sports, Science, and Technology (MEXT); a Grant-in-Aid for Scientific Research (No. 20591031, 21700295) from MEXT; a Grantin-Aid for Scientific Research on Innovative Areas, “Face perception and recognition” from MEXT (No. 21119518); a Grant-in-Aid for Scientific Research on Priority AreasdSystem Study on Higherorder Brain Functions from MEXT (No. 20020026); a Showa University Grant-in-Aid for Innovative Collaborative Research
Projects; and a Special Research Grant-in-Aid for the Development of Characteristic Education from MEXT.
References [1] Kawamura M, Kobayakawa M. Emotional impairment in Parkinson’s disease. Parkinsonism Relat Disord 2009;15(Suppl. 1):S47e52. [2] Bodden ME, Dodel R, Kalbe E. Theory of mind in Parkinson’s disease and related basal ganglia disorders: a systematic review. Mov Disord 2010;25:13e27. [3] Peron J, Vicente S, Leray E, Drapier S, Drapier D, Cohen R, et al. Are dopaminergic pathways involved in theory of mind? A study in Parkinson’s disease. Neuropsychologia 2009;47:406e14. [4] Euteneuer F, Schaefer F, Stuermer R, Boucsein W, Timmermann L, Barbe MT, et al. Dissociation of decision-making under ambiguity and decision-making under risk in patients with Parkinson’s disease: a neuropsychological and psychophysiological study. Neuropsychologia 2009;47:2882e90. [5] Mimura M, Oeda R, Kawamura M. Impaired decision-making in Parkinson’s disease. Parkinsonism Relat Disord 2006;12:169e75. [6] Rossi M, Gerschcovich ER, de Achaval D, Perez-Lloret S, Cerquetti D, Cammarota A, et al. Decision-making in Parkinson’s disease patients with and without pathological gambling. Eur J Neurol 2010;17:97e102. [7] Bodden ME, Mollenhauer B, Trenkwalder C, Cabanel N, Eggert KM, Unger MM, et al. Affective and cognitive theory of mind in patients with parkinson’s disease. Parkinsonism Relat Disord 2010;16(7):466e70. [8] Peron J, Le Jeune F, Haegelen C, Dondaine T, Drapier D, Sauleau P, et al. Subthalamic nucleus stimulation affects theory of mind network: a PET study in Parkinson’s disease. PLoS One 2010;5:e9919. [9] Braak H, Bohl JR, Muller CM, Rub U, de Vos RA, Del Tredici K. Stanley Fahn Lecture 2005: The staging procedure for the inclusion body pathology associated with sporadic Parkinson's disease reconsidered. Mov Disord 2006;21 (12):2042e51. [10] Hoehn MM, Yahr MD. Parkinsonism: onset, progression and mortality. Neurology 1967;17:427e42. [11] Folstein MF, Folstein SE, McHugh PR. “Mini-mental state”. A practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res 1975;12:189e98. [12] Zung WW, Richards CB, Short MJ. Self-rating depression scale in an outpatient clinic. Further validation of the SDS. Arch Gen Psychiatry 1965;13:508e15. [13] Osterrieth P. Le test de copie d’une figure complexe; contribution à l’étude de la perception et de la mémoire. Arch Psychol 1944;30:206e356. [14] Berg EA. A simple objective technique for measuring flexibility in thinking. J Gen Psychol 1948;39:15e22. [15] Baron-Cohen S, Wheelwright S, Hill J, Raste Y, Plumb I. The “Reading the Mind in the Eyes” Test revised version: a study with normal adults, and adults with Asperger syndrome or high-functioning autism. J Child Psychol Psychiatry 2001;42:241e51. [16] Yoshimura N, Yokochi M, Kan Y, Koyama S, Kawamura M. Relatively spared mesocorticolimbic dopaminergic system in juvenile parkinsonism. Parkinsonism Relat Disord 2007;13:483e8.
Contents lists available at ScienceDirect
Parkinsonism and Related Disorders journal homepage: www.elsevier.com/locate/parkreldis
Is “reading mind in the eyes” impaired in Parkinson’s disease?q Natsuko Tsuruya a, Mutsutaka Kobayakawa a, b, Mitsuru Kawamura a, * a b
Department of Neurology, Showa University School of Medicine, 1-5-8 Hatanodai, Shinagawa-ku, Tokyo, Japan Brain Science Institute, Tamagawa University, Tokyo, Japan
a r t i c l e i n f o
a b s t r a c t
Article history: Received 12 July 2010 Received in revised form 4 September 2010 Accepted 8 September 2010
Theory of mind (ToM) is the specific cognitive ability to understand other people’s mental states. Several studies have examined ToM ability in patients with Parkinson’s disease (PD), using the “reading mind in the eyes” test (RMET). However, there has been no agreement as to whether or not ToM ability in this task is affected by PD. In order to obtain conclusive evidence regarding ToM ability in PD, we examined RMET-related performance in nondemented PD patients; we also used the semantic discrimination task to exclude the possibility that PD patients had difficulty in distinguishing emotional adjectives. Results indicated that ToM ability in the RMET is impaired in PD patients, and that this finding was not attributable to the visual processing of faces or the verbal comprehension of emotional adjectives. Thus, the affective aspects of ToM can be impaired in PD patients. Ó 2010 Elsevier Ltd. All rights reserved.
Keywords: Theory of mind Reading mind in the eyes Social cognition Parkinson’s disease
1. Introduction Theory of mind (ToM) is the specific cognitive ability to perceive others’ mental states. In recent years, ToM ability has been increasingly investigated in various neurological diseases, and several studies have shown that ToM ability is affected by Parkinson’s disease (PD) [1,2]. One of the most popular means of assessing ToM ability is the “Reading mind in the eyes” test (RMET). In the RMET, subjects must infer the mental states of a person in a photograph that shows only the subject’s eye region. In the current literature, there is no agreement as to whether or not RMET performance is impaired by PD. Two studies report that PD patients could correctly recognize what others were thinking, from their eye gaze [3,4]. On the other hand, 3 studies, including ours, have reported that PD patients show impairment in the RMET [5,6]. Bodden et al. showed that in relatively advanced stages of PD, patients exhibited impairment in the RMET [7]. Our previous study showed the presence of RMET impairment in PD patients by using the 2-choice version of the RMET. Additionally, 1 study showed that PD patients had difficulty in the RMET, but only after undergoing subthalamic nucleus-deepbrain surgery [8]. Thus far, there is no specific evidence that PD patients, especially those in the early stages of PD, exhibit RMET impairment.
In the present study, we aimed to obtain conclusive evidence regarding mind-reading ability in early PD. First, we recruited nondemented PD patients because in order to infer the mental states of others, several cognitive processes other than ToM ability must be intact. Second, we included the semantic discrimination task as a control task. The RMET involves not only the visual processing of faces but also the ability to discriminate similar emotional adjectives. In most of the previous studies, faceperception ability was determined using the gender-discrimination task; the ability to discriminate emotional adjectives, however, was not determined. Because the RMET uses comparatively unfamiliar words as the target and foils, lexical ability should first be guaranteed through an appropriate task. Third, we recruited patients who were in the earlier stages of PD than those recruited by previous studies. As mentioned above, there is no specific evidence that early PD patients exhibit RMET impairment. Because the RMET is believed to assess the affective aspect of the ToM ability, defective performances in the RMET would indicate the dysfunctions in emotional processing in PD patients. This would support the notion that in the early course of PD, pathological changes are found in the emotional system such as the limbic areas, including the amygdala [9]. 2. Methods 2.1. Subjects
q The review of this paper was entirely handled by an Associate Editor, Eng-King Tan. * Corresponding author. Tel./fax: þ81 3 3784 8710. E-mail address: [email protected] (M. Kawamura). 1353-8020/$ e see front matter Ó 2010 Elsevier Ltd. All rights reserved. doi:10.1016/j.parkreldis.2010.09.001
Twenty PD patients were recruited from among outpatients diagnosed and under treatment at Showa University Hospital (Table 1). All patients were being treated with levodopa or a dopamine agonist, and the experiment was conducted during the “on” state of medication. None of the patients had a history of impulse
N. Tsuruya et al. / Parkinsonism and Related Disorders 17 (2011) 246e248
247
Table 1 Summary of study participants. PD
NC
Mean
SD
Mean
SD
PD vs. NC (significance)
N Men Women Age (y) Years of education HoehneYahr stage Disease duration (y) MMSE WCST category achievement SDS ReyeOsterrieth Complex Figure test LD daily dose (mg) DA daily dose (mg)
11 9
11 9
70.5 14.8 1.5 5.1 28.3 5.1 34.0 34.5
8.6 2.8 0.7 0.7 1.6 1.3 8.4 1.2
265.0 192.0
122.6 163.4
e e
Total LEDD
457.0
207.7
e
67.7 13.7 e e 28.6 3.6a 32.1 34.4
n.s. 4.5 2.2
n.s. n.s.
2.0 2.1 8.5 2.1
n.s. e n.s. n.s.
PD, Parkinson’s disease; NC, normal control; SD, standard deviation; n.s., not significant; MMSE, Mini-Mental State Examination; WCST, Wisconsin Card-Sorting Test; SDS, Self-rating Depression Scale; LD, levodopa; DA, dopamine agonist; LEDD, levodopa equivalent daily dose. a Mimura et al. [5]. control disorder or other psychiatric symptoms. Disease severity corresponded to HoehneYahr stages IeIII (stage I, 13 patients; stage II, 5 patients; stage III, 2 patients) [10]. Global cognitive function was evaluated using the Mini-Mental State Examination (MMSE) [11], and severity of depression was assessed using the Zung Selfrating Depression Scale (SDS) [12]. Visuoperceptual ability was assessed using the ReyeOsterrieth Complex Figure test [13]. The Wisconsin Card-Sorting Test [14] was conducted to assess executive function. We also recruited 20 healthy subjects who were matched for age, gender, and educational background (Table 1). They were enlisted through an agency working with senior citizens and were financially compensated for their participation. None of the normal control (NC) subjects had a history of neurological or psychiatric disorders; their global cognitive functions were evaluated using the MMSE, and the presence of depression was measured using the SDS. Visuoperceptual ability was assessed using the ReyeOsterrieth Complex Figure test [13]. All PD patients and NC subjects were Japanese. Written informed consent was obtained from all participants, and the study protocols were approved by the Showa University Ethics Committee. 2.2. “Reading the mind in the eyes” test To examine participants’ ability to infer the mental states of others, we developed a Japanese adaptation of the revised version of the RMET [15]. The task comprised 20 photographs of the eye region of the faces of Japanese actors, each printed on a separate paper. Four adjectives corresponding to complex mental state descriptors (e.g., “hateful,” “panicked”) were printed on each paper. One of four words (the target word) correctly described the mental state of the person in the photograph. The “correct” word was decided in the pilot study, under the criterion that at least 5 out of 8 judges agreed that the word was the most suitable for each picture. Participants were required to decide which of the 4 words best described what the individual in the photograph was thinking or feeling. There was no time limit for responses. As a control task, we assessed subjects’ lexical ability to understand the meanings of target and foil words (i.e., semantic discrimination task). The participants were required to choose which of 4 words was the most similar in meaning to the target word. The participants also judged the gender of the person shown in the photograph (i.e., gender attribution task), because general deficits in facial perception can affect the main task. The participants were required to judge the gender of the person shown in the photographs used in the RMET. 2.3. Statistical analysis Data are expressed as means (standard deviation [SD]) for the continuous variables. Intergroup differences (PD vs. NC) in demographic and clinical data and in cognitive and behavioral characteristics were analyzed using independent sample t tests. Associations between the scores on the RMET and the demographics, clinical data, and cognitive variables were analyzed with Spearman’s rank correlations.
3. Results The scores of the basic neuropsychological tests of the PD patients were within the normal range (Table 1).
Fig. 1. Performances in the “reading mind in the eyes” test and control tasks. In the RMET, the performances of PD patients were worse than those of NC subjects. Meanwhile, there were no significant differences between the 2 groups in terms of performance in either the semantic discrimination task or the gender attribution task.
On the RMET, PD patients performed significantly worse than the NC subjects (13.5 [2.6] vs. 15.5 [1.6], t(32) ¼ 2.92, P < 0.01; Fig. 1). Meanwhile, performances in the semantic discrimination and gender attribution tasks were not significantly different between PD patients and NC subjects (19.2 [1.2] vs. 19.6 [0.8], t (32) ¼ 1.44, P > 0.1; 18.5 [2.0] vs. 18.5 [1.7], t(38) ¼ 0, P > 0.1, respectively). In order to investigate if early PD influences performance on the RMET test, we analyzed the data limited to patients with Hoehn & Yahr stage I (N ¼ 13). The result showed the same pattern; PD patients performed worse than NC subjects in the RMET test (13.2 [2.7] vs. 15.5 [1.6], t(31) ¼ 3.11, P < 0.01), but not in the semantic discrimination and gender attribution tasks (19.1 [1.4] vs. 19.6 [0.8], t(16.7) ¼ 1.25, P > 0.1; 18.7 [1.7] vs. 18.5 [1.7], t(31) ¼ 0.31, P > 0.1, respectively). There were no significant correlations between the RMET scores and other demographic variables, such as age, gender, or education level. Neither was there any correlation between the RMET scores and other cognitive tasks. 4. Discussion and conclusion PD patients showed impairment in the RMET, but they could perform as well as NC subjects in the semantic discrimination and gender attribution tasks. This result indicated that the ability to infer the mental states of others was impaired in PD patients and that this impairment was not attributable to a failure to discriminate emotional adjectives or to perceptual problems in visually analyzing the eye-gaze region. Moreover, we could find no correlation between the RMET scores and the clinical or demographic data, or the other cognitive tasks. This would imply that the impairment revealed by the RMET is specific to a ToM component in our PD patients, rather than a secondary consequence of other cognitive deficits. ToM ability can be divided into 2 subcomponents: “cognitive ToM” and “affective ToM.” Cognitive ToM is thought to require cognitive understanding of another’s mental state, while affective ToM requires an empathic appreciation of the listener’s emotional state [2]. The RMET is considered to measure affective ToM. In order to investigate the affective side of ToM ability, we should exclude the influences of cognitive factors as much as possible. To date, reported RMET studies have differed in several ways, including the languages and stimuli used and the number of trials involved. Although the general procedure is identical, several factors could bring about differences in RMET results. Therefore, it is important
248
N. Tsuruya et al. / Parkinsonism and Related Disorders 17 (2011) 246e248
to verify the basic cognitive abilities of PD patients. We introduced the semantic discrimination task to examine the participants’ lexical ability to distinguish emotional adjectives. The task sensitivity for ToM ability may decrease if the choices in the RMET are lexically too difficult to distinguish. Some of the previous studies used a glossary to which participants referred when they did not understand the meaning of the choices. However, we consider this insufficient, as participants might not have referred to the glossary when they misunderstood the meanings of the choices. We believe that using the semantic discrimination task is a direct way of controlling and assessing the participants’ lexical ability. The present result indicated that affective ToM could be impaired in PD patients. The ToM network includes the medial prefrontal cortex, superior temporal sulcus region, temporoparietal junction, temporal pole, and amygdala [2]. Pathological changes in PD can result in dysfunction in the affective ToM network. For example, dysfunctions in the mesocorticolimbic dopaminergic pathwaydwhich projects from the ventral tegmental area to the nucleus accumbens, amygdala, and medial prefrontal cortexdis associated with emotional impairment in PD patients [16]. Accumulations of Lewy bodies could also be a possible cause of limbic dysfunction; they are found in the amygdala and surrounding limbic structures as early as the presymptomatic stage of PD [9]. In conclusion, the present result indicated that ToM deficits could be observed in PD patients lacking cognitive deterioration. These results are consistent with the notion that limbic lesions and emotional impairment are observed in patients with early PD [1,9].
Acknowledgements This study was supported by a grant from the Tamagawa University Center of Excellence under the Ministry of Education, Culture, Sports, Science, and Technology (MEXT); a Grant-in-Aid for Scientific Research (No. 20591031, 21700295) from MEXT; a Grantin-Aid for Scientific Research on Innovative Areas, “Face perception and recognition” from MEXT (No. 21119518); a Grant-in-Aid for Scientific Research on Priority AreasdSystem Study on Higherorder Brain Functions from MEXT (No. 20020026); a Showa University Grant-in-Aid for Innovative Collaborative Research
Projects; and a Special Research Grant-in-Aid for the Development of Characteristic Education from MEXT.
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