Wild, Rodden, Grodd, Ruch - Neural Correlates of Laughter and H.pdf - MA - References - s-abin-a

DOI: 10.1093/brain/awg226

Advanced Access publication August 5, 2003

Brain (2003), 126, 2121±2138

REVIEW ARTICLE

Neural correlates of laughter and humour

Barbara Wild, 1,2, * Frank A. Rodden, 2

Wolfgang Grodd 2

and Willibald Ruch 3

1 Department of Psychiatry, 2 Section of Experimental

Magnetic Resonance of the CNS, Department of

Neuroradiology, University of T È bingen, Germany and

3 Department of Psychology, University of Z È rich,

Switzerland

Correspondence to: Dr Barbara Wild, Psychiatrische

Universit È tsklinik, Osianderstrasse 24, 72076 T È bingen,

Germany

E-mail: bawild@med.uni-tuebingen.de

Summary

Although laughter and humour have been constituents

of humanity for thousands if not millions of years, their

systematic study has begun only recently. Investigations

into their neurological correlates remain fragmentary

and the following review is a ®rst attempt to collate and

evaluate these studies, most of which have been pub-

lished over the last two decades. By employing the clas-

sical methods of neurology, brain regions associated

with symptomatic (pathological) laughter have been

determined and catalogued under other diagnostic signs

and symptoms of such conditions as epilepsy, strokes

and circumspect brain lesions. These observations have

been complemented by newer studies using modern

non-invasive imaging methods. To summarize the

results of many studies, the expression of laughter

seems to depend on two partially independent neuronal

pathways. The ®rst of these, an `involuntary' or `emo-

tionally driven' system, involves the amygdala, thala-

mic/hypo- and subthalamic areas and the dorsal/

tegmental brainstem. The second, `voluntary' system

originates in the premotor/frontal opercular areas and

leads through the motor cortex and pyramidal tract to

the ventral brainstem. These systems and the laughter

response appear to be coordinated by a laughter-coordi-

nating centre in the dorsal upper pons. Analyses of the

cerebral correlates of humour have been impeded by a

lack of consensus among psychologists on exactly what

humour is, and of what essential components it consists.

Within the past two decades, however, suf®cient agree-

ment has been reached that theory-based hypotheses

could be formulated and tested with various non-inva-

sive methods. For the perception of humour (and

depending on the type of humour involved, its mode of

transmission, etc.) the right frontal cortex, the medial

ventral prefrontal cortex, the right and left posterior

(middle and inferior) temporal regions and possibly the

cerebellum seem to be involved to varying degrees. An

attempt has been made to be as thorough as possible in

documenting the foundations upon which these bur-

geoning areas of research have been based up to the

present time.

Keywords: emotion; facial expression; brain physiology; exhilaration; functional anatomy

Abbreviations: ERP = event related potential; PAG = periaqueductal grey; rCBF = regional cerebral blood ¯ow; RF =

reticular formation; SMA = supplementary motor area

Introduction

Abraham called the name of his son who was born to

him, whom Sarah bore him: Isaac (i.e. `he laughs') ¼

and Sarah said, `God has made laughter for me;

everyone who hears will laugh over me'.

Genesis 21:3 and 6

Analysing humour is like dissecting a frog. Few people

are interested and the frog dies of it.

That laughter and humour are integral components of

humanity hardly needs to be documented; they have been

analysed and discussed for over two millennia, traditionally

within the contexts of philosophy, anthropology, psychology,

theology and philology (Martin, 1998; Fry, 2002). Ever since

the 19th century, particularly the pathological variants of

laughter have enjoyed the interest of neurologists (Nothnagel,

1889; Brissaud, 1895). More than 20 years have passed,

E. B. White

2122

B. Wild et al.

however, since the last major review of this ®eld was

published (Poeck, 1985) and most of the present article is a

summary and evaluation of studies on symptomatic laughter

carried out since 1985.

Very recently, however, `normal' laughter has also come

under the purview of neurology (Ozawa et al., 2000; Goel

et al., 2001, Iwase et al., 2002), and with it has comeÐ

somewhat in the role of an uninvited guest at a family

reunion, its awkward companionÐhumour. Normal laughter

can, of course, be caused by elements other than humour:

tickling, social cues and laughing gas come to mind

(McGhee, 1979; Ramachandran, 1998; Provine, 2000). At

present, however, humour is the only element that has been

used to elicit normal laughter in neurological studies. Far

from being a simple stimulus, humour is a phenomenon of

such controversial complexity (particularly with respect to its

cognitive components) that a brief discourse on its nature is

prerequisite for understanding the laughter that it evokes.

Under what conditions can laughter and humour be separated

from one another? Under what conditions can they be

dissected into sensory, cognitive, emotional and expressive

components? When and how are these factors related? Recent

studies addressing these questions, based on `normal laugh-

ter', are discussed and a framework for the neural correlates

of laughter and humour is formulated on the basis of the

studies on laboratory animals, neurological patients and

normal subjects that are reviewed here.

Duchenne, who ®rst described how this pattern distinguished

smiles of enjoyment from other kinds of smiling). The

Duchenne display refers to the simultaneous contraction of

the zygomatic major and orbicularis oculi muscles (which

pull the corners of the lips backwards and upwards and

narrow the eyes, causing wrinkles). During laughter, add-

itional facial, respiratory and laryngeal muscles are activated

(Bachorowski and Smoski, 2001; Ruch and Ekman, 2001).

Smiling and laughing may occur spontaneously (in response

to humour or to appropriate emotional or sociological

stimuli), and can also be elicited upon command (voluntary,

contrived or `faked' smiling/laughter). The neural pathways

involved in these different displays have been partially

elucidated on the basis of information derived from studies of

subjects with brain lesions (see below).

Pathological laughter

As mentioned above, the study of symptomatic laughter

antedates that of normal laughter by decades. The following

sections describe various forms of symptomatic laughter in

patients with brain lesions. Most (but not all) of the studies

cited here date from the past 18 years, i.e. since Poeck's

(1969) widely quoted review.

At the outset of this discussion, it must be noted that at

present there is neither a uniform nomenclature nor a

consistent nosology with regard to neurological disturbances

involving laughter. What follows must be considered a

summary of the state of the art. Inasmuch as laughter is such a

ubiquitous component of human behaviour, the notion of

`pathological' laughter can refer to anything from laughter at

politically incorrect jokes to laughter as a manifestation of

chromosomal aberrations in the Angelman syndrome. In

those conditions in which pathological laughter is part of a

global behaviour pattern (i.e. in which the laughter is

congruent with a feeling of exhilaration), issues of causality

are, at present, simply too complex for analysis and will not

be further discussed in this review. Such conditions include

mania, schizophrenia, mood disorders, Alzheimer's syn-

drome and the genetic disorder of Angelman syndrome

(Askenasy, 1987; Laan et al., 1996).

Despite certain shortcomings (see below), the most widely

acknowledged classi®cation scheme for symptomatic laugh-

ter is that of Poeck (1969, 1985). With respect to

neuropathology, he differentiated among symptomatic laugh-

ter deriving from: (i) motor neuron disease, vascular

pseudobulbar paralysis and extrapyramidal motor disorders;

(ii) fou rire prodromique; and (iii) epileptic seizures. In the

following sections, we use Poeck's classi®cation but have

added sections on voluntary/emotional dissociation, laughter,

mirth and brain stimulation, functional imaging in healthy

subjects and studies of non-human laughter-like vocaliza-

tions. For heuristic reasons, the various forms of pathological

laughter are described in an order different from Poeck's. A

summary of pathological ®ndings (included here only if they

Laughter and the brain

Laughter: origins

It would be remarkable if such a loud, ubiquitous, relatively

uniform but somewhat incapacitating behaviour such as

laughter had no survival value. In his book The Expression of

the Emotions in Man and Animals, Charles Darwin (1872)

speculated that the evolutionary basis of laughter was its

function as a social expression of happiness, and that this

rendered a cohesive survival advantage to the group. Smiling

and laughter are not unique to humans. The cerebral

organization of laughter has likewise been studied in squirrel

monkeys (JÈrgens, 1986, 1998); furthermore, among juvenile

chimpanzees a `play face' with associated vocalization has

been noted to accompany actions such as play, tickling or

play biting (van Hoof, 1972; Preuschoft, 1995).

In humans, responsive smiling generally develops within

the ®rst 5 weeks of extrauterine life (Kraemer et al., 1999).

Laughter emerges later, around the fourth month (Ruch and

Ekman, 2001). Although more than 16 different types of

smiles have been distinguished at the morphological level

(Ekman, 1997), it is interesting that the various types of

laughter (at humorous situations, but also scornful, mocking,

social, faked, etc.) remain relatively undesignated (Ruch and

Ekman, 2001). The smile occurring in response to humour is

the facial con®guration designated (Ekman et al., 1990) the

`Duchenne display' (in honour of the neurologist, G. B.

Neural correlates of humour and laughter

2123

were determined either by neuroradiology or post-mortem)

associated with symptomatic laughter is presented in Table 1.

again, the temporal regions (Molinuevo and Arroyo, 1998).

Epileptic laughter has also been reported in patients with

generalized tuberous sclerosis (Striano et al., 1999).

Of all these lesions, it is the hypothalamic hamartomas

that have been studied most extensively. Their intra-ictal

epileptic activity has been characterized not only by surface

electrodes but also with intracerebral recordings (Munari

et al., 1995). A study employing single photon emission

computed tomography has demonstrated a condition of

hyperperfusion (Arroyo et al., 1997) in these tumours during

gelastic seizures. Hypothalamic and pituitary hormones have

been found to be secreted during the seizures (Arroyo et al.,

1997; Tinuper et al., 1997; Cerullo et al., 1998). The

supposition that the hypothalamus per se is responsible for

the production of these seizures (as opposed to the hypothesis

that the pathological activity observed in the hypothalamus is

the result of temporal or frontal processes essential for seizure

generation) has been strengthened by three observations.

First, electrical stimulation of the hamartomas themselves

produces typical seizures (Kuzniecky et al., 1997). Secondly,

with respect to the biochemistry of hypothalamic hamarto-

mas, magnetic resonance spectroscopy has shown a reduction

in the N-acetyl aspartic acid/creatine ratio in the area of the

tumour itself but not in adjoining brain areas (Tasch et al.,

1998; Martin et al., 2003). Although a decreased peak of

N-acetyl aspartic acid is regarded as a sign of neuronal

degeneration, it does not necessarily indicate pathological

changes. It may merely re¯ect the variability of the spectral

pattern between different anatomical formations due to the

heterogeneity of their histomorphology. Thirdly, surgical

removal of the tumour can reduce the incidence of seizures

(Nishio et al., 1994; Valdueza et al., 1994; Kuzniecky et al.,

1997; Parrent, 1999; Unger et al., 2000).

It seems plausible that these tumours have excitatory

effects, with abnormal electrical activity spreading rostrally

and dorsally to areas in the neighbouring limbic system and

caudally to the brainstem to produce the physiological and

psychophysiological manifestations of the `laugh attacks'

(Kuzniecky et al., 1997).

Gelastic epilepsy

Laughter can occur within the framework of any epileptic

seizure. The term `gelastic epilepsy' (from the Greek gelos,

laughter) refers exclusively to those relatively rare seizures in

which laughter is the cardinal symptom. These seizures can

consist exclusively of laughing but often occur in association

with general autonomic arousal and automatisms of move-

ment and/or disturbed states of consciousness (Wilson, 1924;

Berkovic et al., 1988; Cascino et al., 1993; Valdueza et al.,

1994; Cerullo et al., 1998; Striano et al., 1999). Other

symptoms accompanying this ictal laughter, such as peram-

bulation (Jandolo et al., 1977) and micturition (Tasch et al.,

1998), have been reported occasionally and are less frequent.

Despite its stereotypic nature, the laughter produced by

patients during gelastic seizures can appear normal and even

be contagious; one such patient even won a `happy baby'

contest (Berkovic et al., 1988). More typically, however, ictal

laughter appears mechanical and unnatural (Berkovic et al.,

1988; Tasch et al., 1998).

During gelastic seizures, some patients report pleasant

feelings which include exhilaration or mirth (Jacome et al.,

1980; Arroyo et al., 1993; Sturm et al., 2000). Other patients

experience the attacks of laughter as inappropriate and feel no

positive emotions during their laughter (Assal et al., 1993;

Munari et al., 1995; Berkovic et al., 1997; Iannetti et al.,

1997; Kuzniecky et al., 1997; Cerullo et al., 1998;

Georgakoulias et al., 1998; Tasch et al., 1998; Striano et al.,

1999). 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, by investigators who have documented

feelings of mirth in some patients during seizures arising from

hamartomas of the hypothalamus (Arroyo et al., 1993; Sturm

et al., 2000).

Older studies of gelastic epilepsy were based exclusively

on ®ndings using surface EEG electrodes; such arrays do not

allow the exact intracranial localization of epileptogenic foci.

The only studies discussed below are those based on data

con®rmed by CT/MRI localization of abnormalities or by

intracranial recordings of epileptic activity.

The brain areas most frequently found to have been

harbouring pathological ®ndings in patients suffering from

gelastic epilepsy are: (i) the hypothalamus, most commonly

in the form of hypothalamic hamartomas, which are non-

neoplastic malformations composed of hyperplastic neuronal

tissue resembling grey matter (Cascino et al., 1993; Valdueza

et al., 1994; Munari et al., 1995; Kuzniecky et al., 1997;

Georgakoulias et al., 1998; Unger et al., 2000); (ii) the frontal

poles (Arroyo et al., 1993; Iannetti et al., 1997; Unger et al.,

2000); and (iii) the temporal poles (Coria et al., 2000). Ictal

smiling (without laughter) has been observed in patients with

epileptic foci in the parieto-occipital, hippocampal and,

Fou rire prodromique

The fou rire prodromique (FÂrÂ, 1903) is a very rare condition

in which unmotivated, inappropriate laughter occurs as the

®rst symptom of cerebral ischaemia. This laughter, which

seems to be utterly uncontrollable, may be followed by

giggling (Wali, 1993) or crying (Badt, 1927), and is then

replaced by more typical symptoms of a stroke: hemiparesis

or aphasia, for example (Poeck, 1969). The laughter of fou

rire prodromique has been described as `loud and hearty'

(Badt, 1927) or as of a `chuckling' nature (Poeck, 1969). It

can last up to 30 min (Wali, 1993). Lesions associated with

fou rire prodromique have been found (i) at the base of the

pons, bilaterally with no involvement of the tegmentum

(Wali, 1993); (ii) in the left parahippocampal gyrus, the left

posterolateral thalamus and adjacent parts of the internal

Table 1 Lesion localization in laughter due to neurological disease

Voluntary facial

paresis without

pathological laughter

Fou rire

prodromique

Gelastic epilepsy

Pathological laughter

With voluntary

paresis

Without

voluntary paresis

Voluntary paresis

unknown

Emotional

paresis/amimia

Ventral

Trepel (1996)

Wali (1993)

Bhatjiwale (2000)

Kataoka (1997)

brainstem

(n =1)

(n =3)

(n =1)

(n =3)

Cantu (1966)

Matsuoka (1993)

(n =1)

Lal (1992)

Shafqat (1998)

(n =1)

Mouton (1994)

(n =1)

Tei (1997)

(n =1)

Tegmental

brainstem

Karnosh (1945)

(n = 12)

Hypothalamus

Many cases, e.g.

Valdueza (1994)

Unger (2000)

Munari (1995)

Kuzniecky (1997)

Georgakoulias (1998)

Cascino (1993)

Frontal cortex

Bilateral opercular

lesions, e.g.

Garg (2000)

(n =1)

Arroyo (1993)

(n =1)

Mendez (1999)

(n =1)

Hopf (1992)

(n =1)

Foix (1926)

Mateos (1995)

Iannetti (1997) n =1

Temporal cortex

Coria (2000)

(n =1)

Striatocapsular

Husain (1997)

Ceccaldi (1994)

Hopf (1992)

(n =1)

(n =3)

(n =1)

Basal ganglia

e.g. Katsikitis

(1991):

Parkinson's

disease)

(n = 21)

Corticobulbar

motor tract

Nishimura (1990):

chronic progressive

spinobulbar spasticity

McCullagh (2000):

ALS

(n =2)

(n =1)

Weller (1990):

progressive

supranuclear motor

system degeneration (n =1)

Table 1 Continued

Voluntary facial

paresis without

pathological laughter

Fou rire

prodromique

Gelastic epilepsy

Pathological laughter

With voluntary

paresis

Without

voluntary paresis

Voluntary paresis

unknown

Emotional

paresis/amimia

Multiple

regions

Gschwend (1978):

occlusion L MCA

with intact

thalamostriatal

arteries in

angiography

(n =1)

Ceccaldi (1994): L

parahippocampal

gyrus + posterolateral

thalamus + adjacent

parts of the internal

capsule, not

hypothalamus,

hippocampus,

amygdala. (n =1)

Parvizi (2001):

pontomesencephalic

junction affecting L

cerebral peduncle +

midline basis pontis

in middle to upper

pons + R middle

cerebellar peduncle

+ R middle cerebellar

peduncle (n =1)

Hopf (1992): Ant.

+ lat. thalamus,

operculum/posterior

or thalamic defect

+ opercular

atrophy/Substantia

nigra + insular

atrophy + mesial

temporal lobe

defect (n = 3)

Hopf (1992): R

MCA

infarction/partial

infarct corona

radiate/large space

occupying lesion

lower frontoparietal

white matter/MS

with large R

frontocentral white

matter lesion (n =4)

Carel (1997): L

lenticular and caudate

nuclei + ant. insula.

(n =1)

Billeth (2000): L

frontotemporoparietal

incl. Wernicke's

area + R anterior

cerebral artery, in

particular precentral

gyrus (n =1)

Lago (1998)

L MCA territory

(n =1)

Bingham (1998):

bilateral perisylvian

microgyria (n = 16)

Other

Molinuevo (1998):

smiling not

laughter (n =20

Hopf (1992):

posterior thalamus

(n =2)

Parieto-occipital

temporal (n =3)

Only reports based on autopsy, angiography, CT or MRI scanning are included. L = left; R = right; MCA = middle cerebral artery; n = number of patients described; MS = multiple

sclerosis; ALS = amytrophic lateral sclerosis.

Wild, Rodden, Grodd, Ruch - Neural Correlates of Laughter and H.pdf

Plik z chomika:

Inne pliki z tego folderu:

Inne foldery tego chomika: