In the vignette, A holds a true first order belief and B holds a false second order belief. Each belief is associated with an emotional state—in each scenario one of the emotional states has a positive valence and the other a negative valence see Supplementary data.
Participants are asked, in a random order, questions designed to assess their understanding of the two conflicting beliefs and conflicting emotional states. Control questions testing memory for the story and inference making are included. This index thus expressed the difference in performance arising from the content of the task, adjusted for a measure of overall accuracy.
There were no significant differences on the basic neuropsychological measures between the clinical groups, who were, however, significantly impaired relative to healthy comparison subjects on most measures. Demographic variables were similar for all the groups. Although the age of onset of habitual seizures was lower in the early amygdala damage than the late amygdala damage group, this did not reach statistical significance Table 2. No subject made errors on the first order false belief questions Table 3.
Four subjects with early amygdala damage and one late amygdala subject made errors on the second order false belief task, although the group difference in total number of errors did not reach significance. For results, see Table 3. The results Table 3 were highly skewed as subjects in late amygdala damage and comparison groups made no errors. There was no effect of group on comprehension of metaphor. There were no group differences in the scores on control questions with all groups displaying near perfect scores.
There was a significant effect of group on the total number of correct detections and epistemic attributions, but not in affective attributions. Errors in the epistemic attributions all involved assuming that the faux pas had been made intentionally with the aim of upsetting the other protagonist in the vignette. One subject in the late amygdala damage and one in the early amygdala group failed to complete the test. There was no significant difference between the groups in the memory and inference questions.
Performance on the first order true belief component was nearly at ceiling in all groups, and a Kruskal—Wallis test showed no effect of group see Table 3. All but four subjects made more errors in emotional than belief attributions.
There was a significant group difference in the number of correct emotional attributions associated with both first and second order beliefs. A cumulative score reflecting in equal measure the scores on the four tests was calculated Table 4. All clinical groups were substantially impaired relative to the healthy comparison group. There were modest positive correlations within each group between these variables and the overall measure of performance on ToM tests, but no significant interactions between these covariates and the measure of overall performance in each group.
We thus reanalysed the data with these measures as covariates. However, the significant difference between the late amygdala damage group and clinical controls in overall performance in ToM tests did not remain after adjustment for differences in executive function, memory and IQ between the groups.
For results see Table 5. An index of content specificity was calculated to give a measure of the relative performance on epistemic versus affective ToM reasoning. As can be seen from Table 6 , there were no significant gender differences within each group, although in the early and late amygdala damage group and the healthy control group, females tended to perform slightly better.
Collapsing the results for the cumulative index across all groups, females had a marginally higher score than males female mean As discussed earlier, the age of damage for the early amygdala group can be taken to be the age of onset of seizures which arise from the lesion.
The age of damage to the amygdala in the late onset group is the age at which the patient underwent its surgical excision. Figure 2 illustrates this correlation, with the overall score expressed as number of standard deviations from the mean of the healthy comparison group. Four of the six patients who had a DNET associated with adult onset of seizures were less impaired falling within 2 SDs of the healthy comparison group. Turning to the late amygdala damage group, only two of the 11 subjects scored 2 SDs below the healthy comparison group.
Thus it is unlikely that an early age of onset of seizures per se , regardless of the location of the epilpetogenic focus, leads to deficits in ToM reasoning. The study demonstrated deficits in advanced tests of reasoning about the mental states of others among subjects with lesions of the amygdala arising early in development, particularly if associated with childhood onset of seizures. In contrast, subjects with lesions of the amygdala acquired in adult life showed no significant impairment in ToM tasks relative to a clinical comparison group of subjects with lesions which spared the amygdala.
There was no effect of side of damage or gender on overall performance. There was also no evidence of an interaction between the side of amygdala damage and impairment on specific types of mental state attribution epistemic versus affective. In the primary analyses, the developmental stage of amygdala damage was defined pathologically; early amygdala damage subjects had a presumed DNET and late amygdala damage subjects had a histologically normal amygdala excised in adulthood.
Given the uncertainly about the exact age at which DNETs arise, we include a complementary method of dating the age of the amygdala lesions, i. In contrast, only two subjects with damage to the amygdala which arose in adult life due to surgery showed marked ToM impairments.
This raises the possibility of a sensitive period in development of ToM reasoning which extends to late childhood, during which damage to the amygdala leads to impairments, particularly if the damage is so severe as to be clinically and neurophysiologically apparent. Deficits in the early amygdala damage group are only apparent in the developmentally advanced tests of ToM such as the faux pas , implying that such damage is associated with a degree of developmental delay, rather than developmental arrest.
We can speculate about the possible cognitive origins of this delay. The amygdala appears to be a pivotal structure in supporting some of the earliest precursors of ToM reasoning. By disrupting such precursors of ToM reasoning, early damage to the amygdala may thus slow the trajectory of the development of ToM, in many cases preventing subjects reaching the most advanced stages of the skill. This may explain the pattern of deficits found in the early amygdala damage group of generally intact, but not perfect, basic ToM function, and impaired, qualitatively anomalous performance on the more complex tasks of ToM such as the faux pas and comprehension of irony.
This explanation links the role of the amygdala in emotional perception with a role in ToM reasoning. Early damage to the amygdala has been linked explicitly to the later development of autism, which arguably has impaired ToM reasoning as its core neurocognitive deficit. Similarly, participants with early amygdala damage frequently made inappropriate affective attributions in the conflicting belief and emotion test, even when they made the correct epistemic attributions.
There are several possible interpretations of the lack of deficits in the late amygdala damage group. First, it could be argued that the amygdala may be necessary for the performance of ToM reasoning and that just one intact amygdala is sufficient for this processing.
There are several instances of functional reduplication within the brain whereby the loss of one structure is readily compensated for by the presence of its homologue. If this were the case, then deficits in ToM reasoning would be present in subjects with late acquired damage only if both amygdalae were affected, such as that found in subjects described by Stone et al.
This position would also explain the functional imaging reports of amygdala activation during putative ToM reasoning tasks.
However, these lesion and functional imaging studies are open to criticism. First, two of the bilateral subjects S. One of the subjects D. Turning to the functional imaging studies, Frith and Frith have noted that the tasks which report amygdala activation use stimuli such as the human face and eye region, which may recruit the amygdala even in the absence of a clear ToM component. None of the tasks which we employed which more clearly assess ToM reasoning has demonstrated amygdala activation during fMRI.
In other domains of social cognition such as moral reasoning, a similar relationship between impairments and the age of acquisition of a lesion has been reported.
A comparison of the effects of early and late acquisition of lesions to the prefrontal cortex found more pervasive impairments in moral reasoning among subjects with early compared with late prefrontal cortex damage Anderson et al. Several important cautions must be considered in this study. First, the impairment demonstrated by the early amygdala damage group might not be considered severe: the majority of subjects passed the standard first and second false belief ToM tests and were mostly intact in the detection of irony which is in essence a test of second order ToM reasoning.
Deficits were only apparent in the more advanced tests of ToM, and even in these tests the deficits in absolute terms were not great. It would therefore be important to place these impairments in the context of other groups who are also thought to exhibit ToM deficits. Equally, the impairments in the subjects with early amygdala DNETs are not as severe as those found among most people who have autism, emphasizing the fact that we view early amygdala damage as only one of the contributors to a delay in the development of ToM reasoning.
A second important caveat is the presence of almost entirely normal ToM function in some of the subjects in the early amygdala group. Why were these subjects unimpaired? First, there is the possibility of a type 1 error, although the probability of this is low given the effect sizes reported.
Secondly, the presence of intact performance in the face of amygdala damage raises the possibility that the amygdala may not be a core component of the development of ToM reasoning and may provide instead domain general support for ToM reasoning. By this reasoning, compensation for early damage to the amygdala may occur more readily as it is not a core component of ToM reasoning, and thus subjects with amygdala damage may not always demonstrate clear ToM impairments.
If this were so, deficits would only be evident in tests which relied on the domain general functions of the amygdala e. However, the case for a core contribution of the amygdala would be strengthened by the demonstration of deficits on a wider battery of tests, less reliant on verbal processing and comprehension than those used in the current study. Finally, it is notable that all the unimpaired subjects with amygdala lesions had an adult onset of epilepsy see Fig.
This may reflect the presence of a lesion which is less disruptive to amygdalar neuronal integrity leading both to a later age of onset of epilepsy and less impairment in the development of ToM. Thus patients who have a clinically silent DNET throughout early childhood may have been better able to compensate for the presence of an early focal lesion of the amygdala.
We would, however, predict that such compensation may often not be complete, which would account for the deficits found in subjects with early amygdala lesions who have an adult onset of seizures. Additionally, we might expect that on more subtle measures of ToM processing such as reaction times or the quality of responses, differences may be apparent. As the age of onset of habitual seizures was not significantly correlated with the degree of impairment in ToM reasoning in the late amygdala and clinical comparison groups whose epileptogenic lesions lie outside the amygdala , it is unlikely that an early age of onset of seizures per se , regardless of the location of the epileptogenic focus, accounts for the deficits in ToM reasoning.
Although the focus of the study was on the amygdala, some participants had damage to other structures which are held to mediate ToM reasoning, such as the temporal poles which are activated in fMRI studies tapping this domain Frith and Frith, However, as can be seen from the individual results in Table 3 , the subjects with early developmental, combined amygdala and temporal pole damage showed a range of scores spanning from the most impaired individual to subjects performing at average levels for the amygdala damage group.
Subjects who acquired temporal pole damage as part of a temporal lobectomy were unimpaired compared with clinical controls.
Only one subject in this study had a lesion in this region a DNET and she made relatively few errors on the tasks, performing at the mean level for the clinical control group. Future work will examine more systematically the effects of lesions in these specific areas.
There were no significant gender differences within or across groups. This was a surprising finding as we might have expected males to compensate less readily for amygdala damage given the male predominance in developmental disorders with ToM impairments as a core feature. However, the lack of a significant correlation between measures of general intellectual ability, executive function and ToM performance and the intact performance on the comprehension and inference conditions in the tests makes an explanation in these terms unlikely.
Additionally, the vignettes for assessing the comprehension of irony and metaphor were structurally identical, yet deficits were only present in the interpretation of irony, which relies on intact ToM reasoning.
In conclusion, we found that lesions of the amygdala which arise early in development and act as epileptogenic foci in childhood were associated with deficits in ToM reasoning. Subjects who sustained surgical damage to a previously normal amygdala in adult life were intact in most tests of ToM relative to a clinical comparison group. These impairments cannot be reduced to executive dysfunction, which was not marked in the subjects with amygdala lesions and which did correlate strongly with overall performance.
Although the findings were statistically robust and large effect sizes were observed, a minority of subjects had essentially normal ToM reasoning in the face of an amygdala DNET. All such subjects had an adult onset of epilepsy, perhaps reflecting a less aggressive amygdala lesion which may have also been less disruptive to the development of ToM reasoning. However, the presence of these intact subjects emphasizes the need for replication of these findings using complementary measures of ToM reasoning.
The study provides initial evidence compatible with the postulation of the amygdala as part of the neural system which supports the development of ToM reasoning. Pearson correlations between ToM tests overall score and IQ, logical memory and executive function. The possibility of different forms of theory of mind impairment in psychiatric and developmental disorders.
Psychol Med ; 30 : —8. Adolphs R. Neural systems for recognizing emotion. Curr Opin Neurobiol ; 12 : — Cognitive neuroscience of human social behaviour. Nature Rev Neurosci ; 4 : — The human amygdala in social judgment.
Impairment of social and moral behavior related to early damage in human prefrontal cortex. Nature Neurosci ; 2 : —7.
Neurology ; 53 : — Theory of mind: independence of executive function and the role of the frontal cortex in acquired brain injury.
Cogn Neuropsychiatry ; 5 : — A clinicopathological study of autism. Brain ; : — J Child Psychol Psychiatry ; 30 : — Do people with autism understand what causes emotion? Child Dev ; 62 : — Cognition ; 21 : 37 — J Autism Dev Disord a; 29 : — Social intelligence in the normal and autistic brain: an fMRI study. Eur J Neurosci b; 11 : —8. Amygdala is well known to play an important role in human emotions, especially fear and anxiety and its respective resulting behavior.
Stimulation of the amygdala in the human, produces a feeling of fear and anger. This is because, this structure is located near the brainstem, where the sympathetic pathway is located, to produce all physiological reflexes when we are angry or scared. Apart from this, the extreme proximity of amygdala and hippocampus makes us to believe that amygdala has some form of memory functions too. And in fact, it has memory functions too.
However, it is more towards the memory of producing anxiety and fear. Amygdala is also important for sexual function by vomeronasal organ-detected pheromones. Sex-related hormone is secreted by the hypothalamus in respond to the amygdala. Moreover, amygdala, also has a role in the reward system, where positive emotion is elicited.
Now, what happens if amygdala is damaged? In case of monkeys, the bilateral both, there is one left and one right amygdala lesion of amygdala demonstrated that there is a massive reduction of fear and aggression and the monkeys became more friendly, sexually and also non-sexually towards other monkeys. Then, what is the case in humans? Thanks for reading Scientific American. Create your free account or Sign in to continue. See Subscription Options.
Go Paperless with Digital. Get smart. Sign up for our email newsletter. Sign Up. Support science journalism. Knowledge awaits. See Subscription Options Already a subscriber? Create Account See Subscription Options. Continue reading with a Scientific American subscription. Subscribe Now You may cancel at any time.
0コメント