Elsevier

Cortex

Volume 66, May 2015, Pages 134-140
Cortex

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Neural correlates of mirth and laughter: A direct electrical cortical stimulation study

https://doi.org/10.1016/j.cortex.2014.11.008Get rights and content

Abstract

Laughter consists of both motor and emotional aspects. The emotional component, known as mirth, is usually associated with the motor component, namely, bilateral facial movements. Previous electrical cortical stimulation (ES) studies revealed that mirth was associated with the basal temporal cortex, inferior frontal cortex, and medial frontal cortex. Functional neuroimaging implicated a role for the left inferior frontal and bilateral temporal cortices in humor processing. However, the neural origins and pathways linking mirth with facial movements are still unclear. We hereby report two cases with temporal lobe epilepsy undergoing subdural electrode implantation in whom ES of the left basal temporal cortex elicited both mirth and laughter-related facial muscle movements. In one case with normal hippocampus, high-frequency ES consistently caused contralateral facial movement, followed by bilateral facial movements with mirth. In contrast, in another case with hippocampal sclerosis (HS), ES elicited only mirth at low intensity and short duration, and eventually laughter at higher intensity and longer duration. In both cases, the basal temporal language area (BTLA) was located within or adjacent to the cortex where ES produced mirth. In conclusion, the present direct ES study demonstrated that 1) mirth had a close relationship with language function, 2) intact mesial temporal structures were actively engaged in the beginning of facial movements associated with mirth, and 3) these emotion-related facial movements had contralateral dominance.

Introduction

Laughter, an essential part of daily life, consists of motor and emotional components, the latter of which is known as mirth (Arroyo et al., 1993). Indeed, appreciating or enjoying humor is associated with a feeling of mirth. Lesion studies have shown that humor consists of both cognitive and affective processing (Gardner, Ling, Flamm, & Silverman, 1975). Goel and Dolan (2001), in their pioneer functional magnetic resonance imaging (fMRI) study, showed that cognitive processing with semantic components was associated with the left hemisphere (left inferior frontal gyrus and posterior inferior temporal gyrus), while cognitive processing with semantic components involved the bilateral temporal cortices (bilateral posterior middle temporal gyrus and left posterior inferior temporal gyrus), and that affective processing was associated with reward processing system (medial ventral prefrontal cortex) (Goel & Dolan, 2001). This notion was confirmed by several lines of evidence using fMRI in healthy subjects (Amir et al., 2013, Mobbs et al., 2003, Moran et al., 2004, Watson et al., 2007). However, despite centuries of inquiry, the neural origins and pathways linking bilateral facial movements with mirth are still unclear.

Unilateral lower facial motor weakness (contralesional “mimetic palsy” or emotional facial paresis), which manifests during spontaneous smiling and weeping but not at all during voluntary muscle contraction, has been reported in patients with lesions involving mesial temporal structures (amygdala and hippocampus) (Hopf, Muller-Forell, & Hopf, 1992). This suggests that impairment of contralateral functional connections originating in mesial temporal structures leads to asymmetric emotional facial movements.

We report two patients with temporal lobe epilepsy who underwent subdural electrode implantation, and in whom electrical cortical stimulation (ES) of the cortices of the left basal temporal lobe elicited mirth, followed by laughter. By analyzing the features common to the two cases, we postulated that mesial temporal structures directly bridged mirth and laughter.

Section snippets

Subjects

We enrolled 13 consecutive patients with medically intractable left temporal lobe epilepsy who underwent chronic subdural electrode implantation over the basal part of the temporal lobe for presurgical evaluation between March 2000 and December 2013. All the patients showed language dominance in the left hemisphere as assessed by the Wada test (Takayama et al., 2004), with the exception of one who demonstrated bilateral language representation. We systematically performed high-frequency ES at

Results

In both patients, mirth was elicited by high-frequency ES at a very restricted area in the left basal temporal cortex [Fig. 1: a white circle (monopolar stimulation) in Patient 1 and black circles (bipolar stimulation) in Patient 2]. In Patient 1, high-frequency ES at low intensity (5 mA, 5 sec) consistently caused lifting of the right side of the mouth, followed by bilateral facial movements with mirth (Fig. 2). After ES was over, the patient said, “I do not know why, but something amused me

Mirth and language

The neural basis of mirth has been explored by studying humor, classically via brain lesions and more recently with fMRI. Humor can be divided into cognitive and affective processing (Gardner et al., 1975). Cognitive processing, i.e., humor detection, is formed in two stages: 1) a perception of incongruity between the expectation and “punch line”, and 2) resolution of the incongruity (Suls, 1972). A series of fMRI studies of humor indicated that cognitive processing has phonological and

Acknowledgments

We are indebted to Dr. Keiko Usui for providing the patient data. This work was partly supported by Grants-in-Aid for Scientific Research (B) 26282218 (RM), (C) 24592159 (TK), Grant-in-aid for Young Scientists (B) 25861273 (TK) and Exploratory Research 26560465 (RM) from the Ministry of Education, Culture, Sports, Science and Technology of Japan. Department of Epilepsy, Movement Disorders and Physiology, Kyoto University Graduate School of Medicine is an endowment department, supported with

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