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MORITO, Masako

ODAGIRI, Sanae

IWADO, Momoka

MIYAZAKI, Hisashi

MIKAMI, Fumiaki

NAMBA, Tomoko

NAMIKAWA, Kyoko

TAKEI, Yuko

Development of YOUCHART the Information Sharing System for Linking Children with Autism Spectrum Disorder, Their Families and Supporters

OBAMA, Naoya

TANEMURA, Jun

135
Kawasaki Journal of Medical Welfare Vol. 26,  No. 2,  2021 135-140
Original Paper
＊1 Department of Speech-Language pathology and Audiology, Faculty of Rehabilitation,
    Kawasaki University of Medical Welfare, Kurashiki, 701-0193, Japan
    E-Mail: obama@mw.kawasaki-m.ac.jp
A Study on Neuropsychological Characteristics 
and the Lesion Site of Right Hemisphere Damaged 
Patients with Indifference Reaction
Naoya OBAMA＊1 and Jun TANEMURA＊1
(Accepted November 4, 2020)
Key words: indifference reaction, right hemisphere, emotion, attention, unilateral spatial neglect
Abstract
　The relationship between indifference reaction and neuropsychological symptoms in right 
hemisphere damaged patients (RHD) was investigated. 78 patients with RHD were included in this 
study. According to the lesion site, the subjects were classified into six groups as follows: extensive 
cortical lesion, anterior cortical lesion, posterior cortical lesion, extensive basal ganglia lesion, limited 
basal ganglia lesion, and thalamic lesion groups. The Neuropsychiatric Inventory (NPI) was used to 
evaluate indifference reactions. The subjects showed neuropsychological symptoms that included 
anosognosia, attention disorder, unilateral spatial neglect, amnesia, dysexecutive syndrome, apraxia, 
and agnosia. Subjects with extensive cortical lesions and extensive basal ganglia lesions showed 
high NPI scores, whereas subjects with anterior cortical lesions and limited basal ganglia lesions 
showed low NPI scores. Multiple logistic regression analysis was applied to assess the factors 
that influenced indifference reaction, and the attention disorder was significantly correlated with 
indifference reaction. Hence, lesions in the right hemisphere might cause indifference reaction due 
to inability to perceive external stimuli caused by attention disorder.
1. Introduction
　Gainotti1,2) first evaluated the emotional behavior of patients with unilateral brain damage. He showed 
that patients with right hemisphere damage (RHD) were more likely to present indifference and euphoric 
reactions than those with left hemisphere damage (LHD). Babinski3) first reported indifference reaction in 
RHD. Then, Goldstein4) revealed that indifference reaction is an abnormal reaction associated with denial 
of disability in RHD. Moreover, Ohigashi5) recently revealed that indifference reaction was not commonly 
included to apathy-like symptoms in RHD. Although indifference reaction has been observed in patients 
with RHD for a long time, its symptoms and mechanism are still unknown. After the study of Gainotti1,2), 
no research has assessed indifference reactions in RHD in detail. As shown by Gainotti1,2), patients with 
RHD predominantly presented the indifference reaction. Less serious symptoms could be classified into 
four groups as follows: indifference to surroundings, tendency to joke, lack of awareness to their disability, 
and evaluating their disability as mild state. The indifference reaction was significantly correlated with 
136 Naoya Obama and Jun Tanemura
unilateral spatial neglect. Therefore, this study aimed to examine the lesion sites in the right hemisphere 
and incidence of neuropsychological symptoms in patients with and without indifference reaction. Then 
factors influencing indifference reaction were assessed.
2. Methods
2.1 Participants
　Patients with RHD who were admitted for 5 years in the convalescent rehabilitation ward at Kurashiki 
Kinen Hospital were enrolled in this study. The participants were right-handed and did not have a history 
of previous strokes. And they had stable symptoms and did not show confusion at 3 months from the 
onset of their stroke. The exclusion criteria were consciousness disorder, lesion under tent, head trauma, 
subarachnoid hemorrhage, subdural hemorrhage and psychiatric disorders including depression. 78 patients 
with RHD were finally included. 
2.2 Procedures
　We assessed the site of the lesion, severity of indifference reaction, and neuropsychological symptoms. 
Four speech therapists who were in charge of the subjects evaluated the above mentioned items. The 
assessment sheet was distributed to all evaluators in advance, and the researcher explained the evaluation 
method. 
2.2.1 Evaluation of lesion site
　Computed tomography scan images (CT) and magnetic resonance imaging (MRI) of the head were 
investigated based on the diagnosis of the attending physician. According to lesion location, the patients 
were classified into six groups, which were as follows: extensive cortical lesion (frontal and parietal, 
temporal, or occipital lobe lesion), anterior cortical lesion, posterior cortical lesion, extensive basal ganglia 
lesion, limited basal ganglia lesion, and thalamic lesion. 
2.2.2 Evaluation of indifference reaction
　The items in the Neuropsychiatric Inventory (NPI) Japan version6) for indifference reaction were used. 
The NPI score ranged from 0 to 12 points, and a higher score indicated more severe symptoms. 
2.2.3 Evaluation of neuropsychological symptoms
　Neuropsychological symptoms were evaluated based on the Bisiach scale for anosognosia, the Clinical 
Assessment of Attention Deficit was used for evaluating attention disorders, the Behavioral Inattention Test 
for unilateral spatial neglect, the Wechsler Memory Scale-Revised for amnesia, the Behavioral Assessment 
of the Dysexecutive Syndrome for disexecutive syndrome, the Standard Performance Test of Apraxia for 
apraxia, and the Visual Perception Test of Agnosia for agnosia was also used for the evaluation. Based on 
the cutoff scores for each evaluation method, each symptom was evaluated as present (1) and not present 
(0). If the test did not reach the cutoff score, a lower score than the other evaluation items was evaluated as 
present (1), otherwise as not present (0). 
2.3 Statistical analysis
　We used Excel (Bell Curve for Excel) version 2.02 for the statistical analysis. The Mann-Whitney U test 
was used to assess the differences in score between two samples, and a multivariate analysis of variance 
was used for three or more samples. The Steel-Dwass test was applied in multiple comparison correction 
analysis. A multiple logistic regression analysis was applied to assess factors influencing indifference 
reaction. The significance level in all analyses was set at <5%.
2.4 Research ethics
　This study was approved by the Medical Welfare Ethics Committee of Kawasaki University of Medical 
Welfare (approval number: 18-050) and the Ethics Committee of Kurashiki Kinen Hospital (approval number: 
30-1). 
137Examination of Related Factors in Indifference Reaction
3. Results
3.1 Severity of indifference reaction according to the site of damage
　There were no statistically significant differences in terms of number of subjects, age, and Mini-Mental 
State Examination (MMSE) scores among the groups of lesion sites (Table 1). To validate the severity of 
indifference reaction in patients with right hemisphere lesions, the differences in NPI scores were evaluated 
using the Kruskal-Wallis test. Results showed that there was a significant difference in the scores (p < 0.01) 
among the groups. Based on the multiple comparison correction analysis, the NPI score was significantly 
higher in the extensive cortical lesion group than in the anterior cortex lesion group (p < 0.01) and the 
restricted basal ganglia lesion group (p = 0.01). And the score was significantly higher in the extensive basal 
ganglia lesion group than in the anterior cortical lesion group (p < 0.01). 
Table 1　Median score of age, MMSE and NPI of respective lesion sites in right hemisphere damaged patients
ext cortex ant cortex pos cortex ext ganglia lim ganglia thalamus p value analysis
male 13 9 5 6 8 8
0.82 *
female 4 7 4 4 6 4
age 64 (60-67) 67.5 (60.2-75) 67 (63-73) 62 (68.7-64.5) 66.5 (63.2-70.7) 68 (60.7-72) 0.66 **
total points of MMSE 23 (18-26) 21.5 (14.5-28) 25 (15-28) 20.5 (13.2-26.7) 23.5 (18.7-26.7) 21 (18-24.2) 0.93 **
total points of NPI <0.01 **
ext cortex VS ant cortex <0.01 ***
ext cortex VS pos cortex 0.43 ***
ext cortex VS ext ganglia 0.99 ***
ext cortex VS lim ganglia 0.01 ***
ext cortex VS thalamus 0.79 ***
ant cortex VS pos cortex 0.27 ***
ant cortex VS ext ganglia
8 (4-12) 0 0 (0-8) 12 (4.2-12) 0 (0-3.7) 5 (0-8)
<0.01 ***
ant cortex VS lim cortex 0.44 ***
ant cortex VS thalamus 0.05 ***
pos cortex VS ext ganglia 0.36 ***
pos cortex VS lim ganglia 0.96 ***
pos cortex VS thalamus 0.99 ***
ext ganglia VS lim ganglia 0.05 ***
ext ganglia VS thalamus 0.62 ***
lim ganglia VS thalamus 0.49 ***
Statistical analysis: *chi-squared test, **Kruskal-Wallis test, ***Steel-Dwass test
3.2 Comparison of neuropsychological symptoms in patients with and without indifference reaction
　Based on the NPI score, the participants were divided into two groups according to whether they 
have indifference reaction or not. There was no statistically significant difference in terms of number 
of subjects and age between the two groups. However, the MMSE score was significantly lower in the 
group with indifference reaction than in the group without indifference reaction (Table 2). To validate the 
neuropsychological symptoms based on the presence of indifference reaction, the difference in the incidence 
of neuropsychological symptoms between the two groups was assessed using the Mann-Whitney U test. 
Results showed that the proportion of patients with anosognosia, attention disorder, unilateral spatial 
neglect, and amnesia was significantly higher in the group with indifference reaction than in the group 
without indifference reaction (p < 0.01; Table 3). 
138 Naoya Obama and Jun Tanemura
3.3 Factors affecting indifference reaction
　A multiple logistic regression analysis was applied to identify the factors influencing indifference reaction. 
The dependent variable was the presence of indifferent reaction based on NPI scores. To assess differences 
in the incidence of neuropsychological symptoms in patients with or without indifference reaction, 
explanatory variables such as anosognosia, attention disorder, unilateral spatial neglect, and amnesia were 
used. Results showed the following values for each independent variable: anosognosia, 3.59; attention deficit 
disorder, 15.98; unilateral spatial neglect, 5.55; and amnesia, 0.63 (Figure 1). 
Table 2　Median score of age and MMSE in patients with and without indifference reactions
with indifference
reaction
without indifference
reaction p value analysis
male 27 22
0.95 *
female 15 14
age 66 (61.25-70) 65.5 (60-65.5) 0.75 **
total points of MMSE 20.5 (15.25-24.75) 24 (17.75-28) 0.02 **
Statistical analysis: *chi-squared test, **Mann-Whitney U test
Table 3　 Incidence of neuropsychological symptoms in patients with and without 
indifference reactions
with indifference
reaction
wituout indifference
reaction p value
Anosognosia 0.64 0 <0.01
Attention 0.75 0.19 <0.01
Unilateral neglect 0.41 0.05 <0.01
Amnesia 0.52 0.14 <0.01
Disexecutive 0.26 0.15 0.08
Apraxia 0.15 0.09 0.25
Agnosia 0.1 0.02 0.05
Statistical analysis: Mann-Whitney U test
Figure 1　Factors affecting indifference reaction
139Examination of Related Factors in Indifference Reaction
4. Discussion
4.1 Relationship between indifference reaction and site of brain lesion
　Based on the severity of indifference reaction according to the site of RHD, the extensive cortex 
and extensive basal ganglia lesion groups had severe indifference reaction, and the anterior cortex and 
restricted basal ganglia lesion groups had mild indifference reaction. Gainotti1,2) showed a significant 
correlation between RHD and indifference reaction. However, no studies have assessed the relationship 
between severity of indifference reaction and right hemisphere lesions. As Gainotti2) pointed out, the 
exclusion criteria for brain damage were not established, and patients with head trauma were included in 
the previous study. Hence, the risk of diffuse axonal or bilateral hemisphere damage could not be ruled out. 
The present study is significantly different from those of previous studies. That is, the etiology of subjects 
was limited to cerebrovascular disease in the right hemisphere, and those with head trauma, under tent 
lesions, subarachnoid hemorrhage, and subdural hemorrhage were excluded. 
4.2 Relationship between indifference reaction and neuropsychological symptoms
　Gainotti2) evaluated the emotional behavior of patients with unilateral hemisphere damage. Results 
showed a relationship between LHD and catastrophic reaction and RHD and indifference reaction. 
Moreover, there was a significant correlation between catastrophic reactions and aphasia in LHD and 
between indifference reaction and unilateral spatial neglect in RHD. However, Gainotti2) examined the 
relationship between catastrophic reaction and aphasia as well as indifference reaction and unilateral spatial 
neglect. However, the relationship between emotional behavior and other neuropsychological symptoms 
was not evaluated. In the current study, the proportion of patients with cognitive disorder, anosognosia, 
attention disorder, unilateral spatial neglect, and amnesia was significantly higher in the subjects with 
indifference reaction than in the subjects without indifference reaction. Hence, in RHD, indifference reaction 
is characterized by not only unilateral spatial neglect but also various right hemisphere symptoms. This 
result matches with those of studies showing that cortex and basal ganglia lesions are associated with 
severe indifference reaction. And the indifference reaction to the surroundings is thought to be one of right 
hemisphere symptoms caused by extensive damage in the cortex and basal ganglia. 
4.3 Factors affecting indifference reaction
　A multiple logistic regression analysis was applied to identify factors influencing indifference reaction. 
Results showed that visual attention disorder by unilateral spatial neglect had the strongest effect. Recent 
studies have shown that spatial attention network was considered the mechanism underlying unilateral 
spatial neglect7), and a significant correlation was noted between spatial attention network and unilateral 
spatial neglect. Therefore, we tried to explain the association among indifference reaction, unilateral spatial 
neglect and visual attention disorder which was based on the spatial attention network. Corbetta et al.7,8) 
showed unilateral spatial neglect caused by two spatial attention networks. The dorsal spatial attention 
network consciously directs attention to the target (active attention function), and the frontal lobe of the 
bilateral hemisphere is important for this network. By contrast, the ventral attention network inputs an 
unexpected stimulus from the external environment and we appropriately pay attention to the stimulus 
(passive attention function), and the role of the posterior region of the right hemisphere is important. 
Based on this information, the patients who have the bilateral frontal lobe do not intentionally pay active 
attention to the target. However, damage to the posterior part of the right hemisphere results in difficulties 
in responding passively to external stimuli, and this mechanism causes unilateral spatial neglect8). Based on 
this hypothesis, RHD is associated with an inability to accurately recognize environmental stimuli which 
is caused by decreased passive attention function. And this disorder causes unilateral spatial neglect and 
various inferior hemisphere symptoms. As a result, the indifference reaction is thought to be one of these 
behavioral disorders. This finding was supported by the current study. That is, the anterior lesioned 
subjects had a mild indifference reaction. Therefore, indifference reaction was caused by broad lesions 
including those in the posterior cortex of the right hemisphere.
140 Naoya Obama and Jun Tanemura
4.4 Limitations of the study
　This study showed the relationship among indifference reaction, right hemisphere lesions, attention 
disorder and unilateral spatial neglect. Although indifference reaction was found to be associated with 
passive attention disorder, this study did not examine spatial attention disorder in detail. Moreover, 
indifference and euphoria to disability, which are the characteristics of indifference reaction, cannot 
be explained by perceptual impairment caused by environmental stimuli. And furthermore, this study 
examined only morphological lesions by CT and MRI, without consideration of brain dysfunction. Thus, 
further research on examination of brain dysfunction to clarify related lesions in more detail, and the 
feelings of individuals with indifference reaction should be conducted.
References
1. Gainotti G : Reactions "catastrophiques" et manifestations d’indifference au cours des atteintes cerebrales. 
Neuropsychologia, 7, 195-204, 1969.
2. Gainotti G : Emotional behavior and hemispheric side of lesion. Cortex, 8, 41-55, 1972.
3. Babinski J : Contribution a l’etude des troubles mentaux dans l’hemiplegie organique cerebrale 
(anosognosie). Revue Neurologique, 27, 845-848, 1914.
4. Goldstein K eds : Language and language disturbances: Aphasic symptom complexes and their significance for 
medicine and theory of language. Grune and Stratton, New York, 1948.
5. Ohigashi Y : New way of capturing at spomtaneiety. Committee on education and training Japan Society 
for Higher Brain Dysfunction eds, The neural basis of attention and spontaneity, Shinkoh Igaku Shuppansha, 
Tokyo, 13-26, 2014. (In Japanese, translated by the author of this article)
6. Hirono N, Mori E, Ikejiri Y, Imamura T, Shimomura T, Hashimoto M, Yamashita H and Ikeda M : 
Japanese version of the neuropsychiatric inventory: A scoring system for neuropsychiatric disturbances 
in dementia patients. Brain and Nerve, 49, 266-271, 1997.
7. Corbetta M, Patel G and Shulman G : The reorienting system of the human brain: From environment to 
theory of mind. Neuron, 58, 306-324, 2008.
8. Corbetta M and Shulman G : Spatial neglect and attention networks. Annual Reviews Neuroscience, 34, 569-
599, 2011.


A Study on Neuropsychological Characteristics and the Lesion Site of Right Hemisphere Damaged Patients with Indifference Reaction

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