Background
Social cognition is defined as the process that modulates behaviour in response to conspecifics and, in particular, to the higher cognitive processes that subserve the extremely diverse and flexible social behaviours that are observed in primates [
1]. A core component of social cognition is the capacity to attribute independent mental states to others or to predict other people’s behaviour based on their mental states, a capacity that is known as theory of mind (ToM) [
2]. It can enable us to interact in complex social environments and to engage in the activities that we value most, such as family, friendship, love, and cooperation. Accordingly, impairments in ToM can have a serious negative effect on interpersonal relationships, employment, and social interactions [
3,
4].
Previous studies showed that traumatic brain injury [
5] and various psychiatric disorders, including autism [
6] and depression [
7], are accompanied by deficits in ToM. Human lesion [
5,
8] and neuroimaging studies [
1,
9,
10] have been pivotal in attempts to explore the neural substrate of aspects of ToM, such as the ability to recognize the emotional expressions and the reasons underlying the mental states of others. Evidence from several studies performed in both primates and humans suggested that the temporal lobe is involved in ToM and the recognition of emotion [
11‐
14]. One of the first studies of higher-order ToM, which was reported by Schacher, found that patients with mesial temporal lobe epilepsy (MTLE) have impairments in their ability to recognize a faux pas, which is an advanced ToM task [
15]. That study indicated that patients with MTLE, both pre- and postoperatively, performed significantly worse on the Faux pas test compared with patients with extramesiotemporal lobe epilepsy and healthy controls (HC), suggesting that MTLE is a specific aetiology of deficits in higher-order social cognition. Regarding the recognition of emotions, patients with anterior temporal lobectomy have deficits in emotion recognition [
16]. Similarly, a few studies showed that patients with temporal lobe epilepsy had deficits in the ability to recognise emotions, ToM, and decision making [
11,
17‐
19]. These studies confirmed that widespread deficits in social cognition are common in MTLE. Moreover, a growing body of neuroimaging evidence has shown that the temporal pole was activated by a variety of stimuli: moral judgments, socio-emotional stories and sounds evoking a social scene [
9,
20,
21]. Although many neuropsychological studies [
11,
18,
19] examined ToM in individuals with MTLE, and functional neuroimaging studies [
9,
21] demonstrated that the temporal lobe was involved in ToM, fewer studies have explored the effects of temporal lobe cerebral infarction (TLCI) on ToM [
22]. A study performed by Happe et al. [
22] showed that people with right hemisphere (including the temporal lobe) stoke exhibited specific impairments in understanding stories and cartoons that require mental-state attribution. In addition, Weed et al. [
23] reported on patients with right hemisphere stroke who had difficulty discriminating between film categories and a bias toward reduced mental-state ascription in the ToM condition. However, the location of the lesion in those patients was not limited to the right temporal lobe, and results from previous studies have not provided any conclusive evidence regarding the involvement of the temporal lobes in ToM.
Hence, based on the results of previous studies, the aim of the present study was to investigate ToM in patients with TLCI using a variety of tests, including the Recognition of faux pas and the Reading the Mind in the Eyes (RME) tasks. One Study from Pellicano et al. [
24] showed that ToM development relied on executive function in children. Carlson et al. [
25] implicated that inhibition control and working memory might be central to the relation between executive function and false belief understanding. Saxe and colleagues [
26] have identified both separated and overlapping brain structures involved in ToM and executive function, suggesting that both domain general and domain specific cognitive resources are involved in ToM. In contrast, some lesion studies showed that ToM impairment was independent of executive function in adults [
27,
28]. Previous studies have shown that executive function might play an important role in ToM emergence during childhood, but mature theory of mind ability might not rely on executive functions [
26]. However, a relationship between ToM and executive function or memory function has not been reported in patients with TLCI. Thus, we tested the relationship between other cognition functions and ToM in patients with TLCI.
Discussion
This study examined the nature of mentalizing deficits presented by patients with TLCI, especially with medial temporal lobes lesions. Our results showed that the TLCI group had impaired ToM compared with the HC group. Consistent with previous literatures [
11,
13], our findings implied that the temporal lobe was involved in ToM.
The results from this study showed that the TLCI group had impaired performances on the total faux-pas–related test and the RME test compared with the HC group,while its performances on control question and gender recognition task were relatively normal. ToM ability can be further divided into 2 subcomponents: ‘cognitive ToM’ and ‘affective ToM’. Since the RME test is regarded as a classical task to measure affective ToM based on eye expression, the results of the current study indicate that affective ToM may be impaired in patients with temporal lobe infarction. In addition to this observation, our findings partially confirmed that the impaired performance on the faux pas test observed in the TLCI group was mostly related to a significantly worse performance on the question regarding understanding of the mental states of the speakers and listeners, and not to identifying the faux pas. Performing a social faux pas task may involve at least two levels of difficulty in cognitve loading processes: the identification and the understanding of a social faux pas. Identification of a social faux pas with questions 1 and 2 that merely ask whether the participants noted that there was a faux-pas at all and relied on the cognitive ToM ability. Understanding of a social faux pas maybe more requires, in addition, an empathic appreciation of the speaker’s and listener’s emotional state (knowledge about emotions). Following this line of thought, the poor performance on Questions 3 and 4 in patients with TLCI may be related to an increase of the ability to make affective representations of others’ mental states relative to Questions 1 and 2. The present study indicated that the TLCI group have a specific affective ToM deficit, which represented the deficit with the integration of emotional information for ToM. In social interactions, deficits in affective ToM may limit the TLCI patients’ abilities of understanding the intention of individuals to hurt the feelings of others. Subsequently, their social behaviours which are affected by misinterpretation of the intention to hurt possibly have an impact on the quality of social interactions and relationships [
39].
Previous studies also showed the temporal lobe was involved in social emotional functions [
40], such as in the perception of affective empathy of others [
41], understanding of sarcasm [
42], emotional expressions [
43], and gaze direction [
44,
45]. A neuropsychological study also revealed that patients with atrophy in the temporal pole region [
46] and patients with temporal lobe epilepsy [
47,
48] impaired in emotion recognition. One study performed in normal subjects using blood oxygen level-dependent functional MRI showed that areas including the temporoparietal junction, the superior temporal lobe, and the temporal pole were activated in affective empathy [
14]. Our results may provide new evidence in support of the relationship between the temporal lobe and affective ToM.
Furthermore, the results obtained here also indicate that the deficit in the faux pas test observed in the TLCI group is similar to that of patients with dorsolateral prefrontal cortex lesions described in a previous study [
5]. A functional neuroimaging study showed that the ToM task activated the right dorsolateral prefrontal cortex, the bilateral temporoparietal junction and the right inferior parietal lobule more than the non-ToM condition did [
10]. Schilbach et al. [
49] reported that not only the left medial basotemporal and right superior temporal cortex, but also the prefrontal lobe, were activated when participants viewed socially relevant clips. However, the deficit in the faux pas test observed in the TLCI group was different from that of patients with orbitofrontal cortex damage [
8]. Patients with orbitofrontal cortex damage made errors in detecting faux pas by giving the answer that nothing awkward was said in the story [
8]. Of course, the prefrontal cortex, together with areas of the temporal cortex, has been established as a part of the complex network underlying ToM, i.e., the ability to understand that others have beliefs, desires, and intentions that are different from one’s own [
50,
51]. In the present study the results indicated that the TLCI group could identify the occurrence of a faux pas in the story,but they could not correctly make inferences about the mental state of others. Therefore, it is conceivable that the deficits in ToM observed in the TLCI group were due to a disturbance in the connections of frontotemporal networks. Temporal lobe stroke may have an effect on higher-order social behaviour by altering afferents to frontal regions.
In addition, this study showed that patients with TLCI exhibited impairment not only in ToM, but also in executive-function subcomponents and memory. Within the TLCI group, the total faux-pas–related scores were correlated with RAVLT trial 5, indicating that memory impairment was associated with ToM. We did not find any correlation between the RME test or the faux pas test scores and other cognitive tasks. The results of this study indicated that the deficit of faux pas with the TLCI group might be related to auditory verbal memory impairment. Moreover, a neuroimaging study confirmed the existence of areas of activity that were common to autobiographical episodic memory and ToM within the frontal and posterior/medial temporal lobe regions [
52]. However, we did not find that the correlation between the RME task and RAVLT in the patient group. The social faux pas task features verbal material and it requires participants to hold a large amount of verbal material in working memory in recognition of faux pas, while the RME task is thought to reflect a visual affective subcomponent of ToM [
53]. The results from this study indicated that performance on the RAVLT 5 correlates with the faux pas task might be due to the verbal material of this task. We found that there was no correlation between ToM and neuropsychological testing including executive-function subcomponents and memory in the HC group. Previous studies have demonstrated development of ToM depends largely on the normal functioning of executive function memory systems in childhoods [
54]. And some evidences have emerged to show that the ability of ToM seemed to be independent of a more cognitive or executive in normal adults [
27,
55]. The results from the study indicated that the ToM ability of the normal adults maybe not relied on executive or memory function. Moreover, the study also indicated that the RME test not correlated with the scores from the faux pas. Shamay-Tsoory et al. [
56] have identified that the performance in affective ToM tasks was positively related to their empathic ability, indicating that the ability to make affective representations of others’ mental states is associated with the ability to empathize. The faux pas recognition test is thought to reflect both the cognitive and affective subcomponents of ToM. A rational explanation for this would be that performance of the RME test requires less empathic processing than is needed for the appreciation of a faux pas.
There are some limitations of our study. First, we could not use executive-function subcomponents and memory as covariates for analyses of the differences in ToM performance between groups because the data of the faux pas or RME was not normally distributed. Another limitation of the present study was that patients with unilateral lesions were not tested for hemispheric specialization for ToM because of the small sample of patient with left temporal lobe cerebral infarction in our study, although some researchers pointed out the role of right temporal lobe structures in social cognition [
44,
57] and impaired emotion processing and ToM ability in patients with right hemispheric stroke [
23,
58]. Moreover, previous studies indicated the presence of gender differences in social cognition [
59]. Unfortunately, the sample size of the female patients with TLCI was too small to reach any conclusions of this nature.
Competing interests
None of the authors have any competing financial interests.
Authors’ contributions
CZ, YW, and KW designed the experiments. CX YZ DS and KW conducted the experiments. CX YZ and DS analyzed the data. CX, YW, and KW drafted the manuscript. All authors read and approved the final manuscript.