Thursday, December 25, 2014

Eliciting Mirth and Laughter via Cortical Stimulation

Ho ho ho!

“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.”

-Yamao et al. (2014)

The subject of laughter has been under an increasing amount of scientific scrutiny.  A recent review by Dr. Sophie Scott and colleagues (Scott et al., 2014) emphasized that laughter is a social emotion. During conversations, voluntary laughter by the speaker is a communicative act. This contrasts with involuntary laughter, which is elicited by external events like jokes and funny behavior.

One basic idea about the neural systems involved in the production of laughter relies on this dual process theme:
The coordination of human laughter involves the periaqueductal grey [PAG] and the reticular formation [RF], with inputs from cortex, the basal ganglia, and the hypothalamus. The hypothalamus is more active during reactive laughter than during voluntary laughter. Motor and premotor cortices are involved in the inhibition of the brainstem laughter centres and are more active when suppressing laughter than when producing it.


Figure 1 (Scott et al., 2014). Voluntary and involuntary laughter in the brain.


An earlier paper on laughter and humor focused on neurological conditions such as pathological laughter and gelastic epilepsy (Wild et al., 2003). In gelastic epilepsy, laughter is the major symptom of a seizure. These gelastic (“laughing”) seizures usually originate from the temporal poles, the frontal poles, or from benign tumors in the hypothalamus (Wild et al., 2003). Some patients experience these seizures as pleasant (even mirthful), while others do not:
During gelastic seizures, some patients report pleasant feelings which include exhilaration or mirth. Other patients experience the attacks of laughter as inappropriate and feel no positive emotions during their laughter. It has been claimed that gelastic seizures originating in the temporal regions involve mirth but that those originating in the hypothalamus do not. This claim has been called into question, however...

In their extensive review of the literature, Wild et al. (2003) concluded that the “laughter‐coordinating centre” must lie in the dorsal midbrain, with intimate connections to PAG and RF. Together, this system may comprise the “final common pathway” for laughter (i.e., coordinating changes in facial muscles, respiration, and vocalizations). During emotional reactions, prefrontal cortex, basal temporal cortex, the hypothalamus, and the basal ganglia transmit excitatory inputs to PAG and RF, which in turn generates laughter.


Can direct cortical stimulation produce laughter and mirth?

It turns out that the basal temporal cortex (wearing a Santa hat above) plays a surprising role in the generation of mirth, at least according to a recent paper by Yamao et al., (2014). Over a period of 13 years, they recorded neural activity from the cortical surface of epilepsy patients undergoing seizure monitoring, with the purpose of localizing the aberrant epileptogenic tissue. They enrolled 13 patients with implanted subdural grids to monitor for left temporal lobe seizures, and identified induced feelings of mirth in two patients (resulting from electrical stimulation in specific regions).

Obviously, this is not the typical way we feel amusement and utter guffaws of delight, but direct stimulation of the cortical surface goes back to Wilder Penfield as a way for neurosurgeons to map the behavioral functions of the brain. Of particular interest is the localization of language-related cortex that should be spared from surgical removal if at all possible.

The mirth-inducing region (Yamao et al., 2014) encompasses what is known as the basal temporal language area (BTLA), first identified by Lüders and colleagues in 1986. The region includes the left fusiform gyrus, about 3-7 cm from the tip of the temporal lobe. Stimulation at high intensities produces total speech arrest (inability to speak) and global language comprehension problems. Low stimulation intensity produces severe anomia, an inability to name things (or places or people). Remarkably, however, Lüders et al. (1991) found that “Surgical resection of the basal temporal language area produces no lasting language deficit.”

With this background in mind, let's look at the results from the mirthful patients. The location of induced-mirth (shown below) is the white circle in Patient 1 and the black circles in Patient 2.  In comparison, the locations of stimulation-induced language impairment are shown in diamonds. Note, however, that mirth was co-localized with language impairment in Patient 2.



Fig. 1 (modified from Yamao et al., 2014). The results of high-frequency electrical cortical stimulation. “Mirth” (circles) and “language” (diamonds) electrodes are shown in white and black colors for Patients 1 and 2, respectively. Note that mirth was elicited at or adjacent to the electrode associated with language impairment.  R = right side. The view is of the bottom of the brain.


How do the authors interpret this finding?
...the ratio of electrodes eliciting language impairment was higher for the mirth electrodes than in no-mirth electrodes, suggesting an association between mirth and language function. Since the BTLA is actively involved in semantic processing (Shimotake et al., 2014 and Usui et al., 2003), this semantic/language area was likely involved in the semantic aspect of humor detection in our cases.

Except there was no external humor to detect, as the laughter and feelings of mirth were spontaneous. After high-frequency stimulation, one patient reported, “I do not know why, but something amused me and I laughed.” The other patient said, “A familiar melody that I had heard in a television program in my childhood came to mind; its tune sounded funny and amused me.”

The latter description sounds like memory-induced nostalgia or reminiscence, which can occur with electrical stimulation of the temporal lobe (or TL seizures). But most of the relevant stimulation sites for those déjà vu-like experiences are not in the fusiform gyrus, which has been mostly linked to higher-level visual processing.

The authors also found that stimulation of the left hippocampus consistently caused contralateral (right-sided) facial movement that led to laughter.

I might have missed it, but one thing we don't know is whether stimulation of the right fusiform gyrus would have produced similar effects. Another thing to keep in mind is that these little circles are only one part of a larger system (see Scott et al. figure above). Presumably, the stimulated BTLA sites send excitatory projections to PAG and RF, which initiate laughter. But where is mirth actually represented, if you can feel amused and laugh for no apparent reason? By bypassing higher-order regions1, laughter can be a surprising and puzzling experience.


Footnote

1 Like, IDK, maybe ventromedial PFC, other places in both frontal lobes, hypothalamus, basal ganglia, and more "classically" semantic areas in the left temporal lobe...


link originally via @Neuro_Skeptic:



References

LÜDERS, H., LESSER, R., HAHN, J., DINNER, D., MORRIS, H., WYLLIE, E., & GODOY, J. (1991). BASAL TEMPORAL LANGUAGE AREA Brain, 114 (2), 743-754 DOI: 10.1093/brain/114.2.743

Scott, S., Lavan, N., Chen, S., & McGettigan, C. (2014). The social life of laughter Trends in Cognitive Sciences, 18 (12), 618-620 DOI: 10.1016/j.tics.2014.09.002

Wild, B., & et al. (2003). Neural correlates of laughter and humour Brain, 126 (10), 2121-2138 DOI: 10.1093/brain/awg226

Yamao, Y., Matsumoto, R., Kunieda, T., Shibata, S., Shimotake, A., Kikuchi, T., Satow, T., Mikuni, N., Fukuyama, H., Ikeda, A., & Miyamoto, S. (2014). Neural correlates of mirth and laughter: A direct electrical cortical stimulation study Cortex DOI: 10.1016/j.cortex.2014.11.008



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4 Comments:

At December 26, 2014 3:48 AM, Anonymous David J. Littleboy said...

Somewhat off topic, but when is someone going to notice that cortical stimulation studies of epileptic patients is unethical, amoral, and like, really obnoxious?

 
At December 26, 2014 8:07 AM, Anonymous Catherine Caldwell-Harris said...

Great article. Neurocritics, congrats on your mention in New Yorkef Nov 30 article (Neuroscience Fiction).

 
At December 26, 2014 5:42 PM, Blogger The Neurocritic said...

David - I can see your concern, but neurosurgeons perform cortical stimulation whether or not there is a research study involved. And if the patient does participate in research, it is approved by an ethics board, and the patient signs a consent form.

Catherine - Thanks! That New Yorker article has enjoyed a resurgence in popularity for some reason. It was actually published in 2012!

 
At February 11, 2015 2:10 AM, Anonymous Anonymous said...

Its tremendous :)

 

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