NoteNeural correlates of mirth and laughter: A direct electrical cortical stimulation study
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
References (35)
- et al.
Hemispherical asymmetry in human SMA during voluntary simple unilateral movements. An fMRI study
Cortex
(2003) - et al.
Susceptibility-induced loss of signal: comparing PET and fMRI on a semantic task
NeuroImage
(2000) - et al.
Asymmetric bilateral effect of the supplementary motor area proper in the human motor system
Clinical Neurophysiology
(2012) - et al.
Left anterior temporal cortex actively engages in speech perception: a direct cortical stimulation study
Neuropsychologia
(2011) - et al.
Humor modulates the mesolimbic reward centers
Neuron
(2003) - et al.
Neural correlates of humor detection and appreciation
NeuroImage
(2004) - et al.
Laughter and the mesial and lateral premotor cortex
Epilepsy Behaviour
(2006) - et al.
The inferior, anterior temporal lobes and semantic memory clarified: novel evidence from distortion-corrected fMRI
Neuropsychologia
(2010) - et al.
Ha Ha! Versus Aha! A direct comparison of humor to nonhumorous insight for determining the neural correlates of mirth
Cerebral Cortex
(2013) - et al.
Mirth, laughter and gelastic seizures
Brain
(1993)
The ventral and inferolateral aspects of the anterior temporal lobe are crucial in semantic memory: evidence from a novel direct comparison of distortion-corrected fMRI, rTMS, and semantic dementia
Cerebral Cortex
Mirth and laughter elicited during brain stimulation
Epileptic Disorders
Electric current stimulates laughter
Nature
Comprehension and appreciation of humorous material following brain damage
Brain
The functional anatomy of humor: segregating cognitive and affective components
Nature Neuroscience
Localization of emotional and volitional facial paresis
Neurology
Role of primary sensorimotor cortices in generating inhibitory motor response in humans
Brain
Cited by (39)
Semantic Space Theory: A Computational Approach to Emotion
2021, Trends in Cognitive SciencesMirroring other's laughter. Cingulate, opercular and temporal contributions to laughter expression and observation
2020, CortexCitation Excerpt :In the present study, laughter and smiling were elicited by ES of specific cingulate, opercular and temporal sites. While these localizations are fully in line with previous reports from our and other groups (Caruana et al., 2016, 2018, 2015; Arroyo et al., 1993; Bijanki et al., 2019; Fernández-Baca Vaca et al., 2011; Satow et al., 2003; Sperli et al., 2006; Yamao et al., 2015), the precise localization of these sites is telling of their possible contribution to emotional behavior. The cingulate sites involved in laughter production are localized in the caudal sector of the pACC.
Pathways for smiling, disgust and fear recognition in blindsight patients
2019, NeuropsychologiaGelastic seizures caused by subtle focal cortical dysplasia in the inferior frontal gyrus: Three case reports
2017, Journal of the Neurological SciencesSmile and laughter elicited by electrical stimulation of the frontal operculum
2016, NeuropsychologiaCitation Excerpt :Reports of laughter elicited by ES of the basal temporal lobe showed a left lateralization in all cases (Arroyo et al., 1993; Satow et al., 2003; Yamao et al., 2015), and stimulated sites were typically located adjacent to the basal temporal language area. Taken together, these evidences leaded to the hypothesis that laughter and language processing have a very close relationship, and that laughter can be elicited mainly in the dominant hemisphere and in close spatial proximity to language (Fernandez-Baca Vaca et al., 2011; Yamao et al., 2015). Nevertheless, laughter was also elicited from the right supplementary motor area in one patient (Schmitt et al., 2006) and, more recently, from the pregenual anterior cingulate area (pACC) in seven out of eleven stimulation sites (Caruana et al., 2015), questioning this hypothesis.