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Mirth and laughter arising from human temporal cortex
  1. T Satow1,
  2. K Usui1,
  3. M Matsuhashi1,
  4. J Yamamoto1,
  5. T Begum1,
  6. H Shibasaki1,
  7. A Ikeda2,
  8. N Mikuni3,
  9. S Miyamoto3,
  10. N Hashimoto3
  1. 1Human Brain Research Centre, Kyoto University Graduate School of Medicine, 54 Kawahara-cho, Shogoin, Sakyo, Kyoto 606-8507, Japan
  2. 2Department of Neurology, Kyoto University Graduate School of Medicine
  3. 3Department of Neurosurgery, Kyoto University Graduate School of Medicine
  1. Correspondence to:
 Dr Hiroshi Shibasaki;
 shib{at}kuhp.kyoto-u.ac.jp

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Laughter and mirth are essential in our enjoyment of daily life and in facilitating communication. Various studies have been done relating to the emotional processing that takes place in the human cerebral cortex, but few have explored the cerebral origins of mirth. Some reports on pathological laughter have implicated the hypothalamus, brain stem, and temporal lobe.1–3

As part of the presurgical evaluation of patients with epilepsy, electric cortical stimulation is used to delineate the functional cortical areas, and sometimes this elicits various emotional responses.4 However, only two stimulation studies2,5 have been conducted with a focus on mirth and laughter. Arroyo et al suggested that the motor act of laughter and the processing of its emotional content were separately represented in, respectively, the anterior cingulate area and the basal temporal area (the fusiform gyrus or parahippocampal gyrus, or both).2 Fried et al suggested not only that laughter and mirth were represented in the presupplementary motor area, but also that there was close linkage between the motor, affective, and cognitive components of laughter.5

We report a patient in whom electric cortical stimulation applied to the inferior temporal gyrus produced mirth alone or laughter preceded by mirth, depending on the intensity of the stimulation.

CASE REPORT

A 24 year old right handed woman with medically intractable complex partial seizures underwent implantation of subdural grid electrodes on the cortical surface of the left temporal cortex and a depth electrode into the right mesial temporal cortex. Long term video/EEG monitoring with scalp electrodes done before this invasive monitoring showed late ictal lateralisation at the left anterior temporal area, and thus a right temporal onset could not completely be excluded. Magnetic resonance imaging showed high intensity and atrophy in the left anterior and right posterior hippocampus. Interictal FDG-PET (fluorodeoxyglucose positron emission tomography) showed hypometabolism in the left temporal lobe. An intracarotid amobarbital test revealed the dominance of language and memory in the left hemisphere.

The seizures started with an epigastric rising sensation, followed by loss of awareness combined with hand and oral automatisms. Laughter or the feeling of mirth was not seen during the patient’s habitual seizures. Video/EEG monitoring showed that the epileptogenic focus was in the left mesial temporal cortex (A1, 2, 9, and 10) (red electrodes in fig 1). Electrical cortical stimulation (50 Hz, alternate polarity of square pulses) was done to delineate the functional areas, with special emphasis on language function.

Figure 1

Brain magnetic resonance imaging showing the arrangement of electrodes on the surface of the left basal temporal cortex. A11 and B1 are overlapping. The electrodes A4 and A12 (yellow) are located on the basal aspect of inferior temporal gyrus where the electric stimulation induced mirth with or without laughter. A1, A2, A9, and A10 (red) were epileptogenic foci and were ultimately resected. Electrical stimulation of blue electrodes disrupted or arrested speech and other language tasks.

Stimulation of the basal aspect of the inferior temporal gyrus between A4 and A12 (yellow electrodes in fig 1) at low intensity and short duration (5 mA, 1 s) consistently produced mirth without laughter, and it was always accompanied by a melody that she had heard in a television programme in her childhood. The duration and intensity of the mirth increased in proportion to the duration and intensity of stimulation (15 mA, 3 s), and she eventually smiled during the latter part of a 5 second stimulation. The patient said that the tune appeared funny to her and made her feel amused, but only during the electrical stimulation, and we were able to confirm this. When maximum intensity at longer duration (15 mA, 5 s) was applied, it disrupted a variety of language tasks, but neither alternating hand and foot movements nor vocalisation was disturbed. During this maximum stimulation condition, the patient felt mirth, but the performance of various language tasks obscured apparent laughter. Stimulation of the adjacent pairs of electrodes (A3–A11, A6–A13, and B2–4) (blue electrodes in fig 1) affected only language tasks but was not consistently accompanied by a feeling of mirth.

COMMENT

Our observations suggest that mirth is represented in a relatively small distinct area in the temporal neocortex (the basal surface of the inferior temporal gyrus), which is in part consistent with the observations of Arroyo et al.2 Our study clearly showed that mirth was represented in the inferior temporal gyrus, and was closely linked with a particular context (a certain tune in this patient). This association with a specific event was not observed in the patients reported by Arroyo et al.2 Because the temporal lobe is involved in memory function in human, it is reasonable that both the context of the mirth and laughter and the induced mirth and laughter are represented. In the present case, we could not identify any site where the electric stimulation elicited laughter without mirth. Importantly, the fact that the stimulation with higher intensity and longer duration elicited mirth with laugher more effectively suggests different thresholds for mirth and laughter, postulating a hierarchical organisation or serial processing of mirth and laughter in the human temporal cortex. Laughter might be situated at a higher order than mirth, at least in the temporal neocortex. It is possible that laughter might be caused by further activation of the frontal motor cortices, including the anterior cingulate gyrus, through corticocortical projections, such that electrical cortical stimulation could elicit laughter without mirth.2

With regard to the characteristics of induced mirth in this patient, the melody which made her feel funny was not amusing by itself in the absence of electrical stimulation, raising the possibility that stimulation changed the internal standard of her amusement through an undetermined process.

Although it should be taken into account that the mirth elicited in the present case might not necessarily have reflected the representation of mirth and laughter in the normal brain, no mirth was seen during the patient’s habitual seizures, and neither electrode A4 nor electrode A12 was included in the epileptogenic foci. Thus this particular area (A4–A12) producing mirth on stimulation can be judged to reflect normal function in this patient.

In the present case, mirth is represented in the temporal lobe and may be stored together with the context inducing mirth in the same area, suggesting a close relation between mirth and memory function. As far as the temporal neocortex in the present patient is concerned, laughter seems to be situated at a hierarchically higher order than mirth.

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