Taber, Redden - Functional Anatomy of H. - Positive Affect.pdf - MA - References - s-abin-a

WINDOWS TO THE BRAIN

Robin A. Hurley, M.D., L. Anne Hayman, M.D., Katherine H. Taber, Ph.D.

Section Editors

Functional Anatomy of Humor: Positive Affect and Chronic Mental Illness

Katherine H. Taber, Ph.D., Maurice Redden, M.D., Robin A. Hurley, M.D.

COVER AND FIGURE 1. The dopamine system is a critical component of the brain reward circuitry, important for both motivation

and reward-associated functions. The majority of dopamine-containing neurons reside in two midbrain nuclei, the substantia nigra (pink)

and the ventral tegmental area (yellow). The dorsal striatum (caudate and putamen) is the major target for the substantia nigra. The

ventral striatum (blue, mostly occupied by nucleus accumbens) is a major target for the ventral tegmental area.

FIGURE 2. Functional imaging agrees

with clinical evidence that the neuroana-

tomical networks supporting voluntary

and humor-evoked smiling are different.

Motor-related areas (e.g. primary motor

cortex, premotor cortex, operculum) are

consistently activated during voluntary

facial movement (left), but not during

humor-evoked smiling (right). Differ-

ences in the areas activated probably re-

late to the different contrasts utilized in

these three studies. 1–3

FIGURE 3. One approach to identifying areas of brain important for later stages of humor processing is to look for areas of activation

in common between two different types of humor (conjunction analysis). 4,5 A study comparing verbally-presented puns and semantic

jokes reported that only an area in medial prefrontal cortex (blue) survived the two step analysis procedure. A study comparing visually-

presented captioned and uncaptioned cartoons reported multiple regions of activation in common (green).

http://neuro.psychiatryonline.org

J Neuropsychiatry Clin Neurosci 19:4, Fall 2007

TABER et al.

sively studied, investigation of positive emotions

is relatively new. 6 An evolutionary perspective on the

value of emotions is potentially illuminating. The adap-

tive value of many negative emotions has been related

to promoting fast and appropriate responding during

high risk situations (ﬁght or ﬂight). 7 Under life-threat-

ening circumstances, a narrowing of response patterns

is necessary for rapid response selection and perfor-

mance. In contrast it has been proposed that the adap-

tive value of humor and positive affect is to promote a

broadening of response. This provides a way to explore

new possibilities in times of safety. 7 In Fredrickson’s

model, general categories of positive emotions have dif-

ferent but complementary adaptive value that build an

individual’s physical, intellectual and social resources.

The emotion of joy (or happiness), for example, is asso-

ciated with imaginative play, which is characterized by

“exploration, invention, and just plain fooling around.” 7

Among other beneﬁts, play promotes the learning of new

skills. The emotion of interest (or wonder) promotes ex-

ploration, leading to a broadening and deepening of

knowledge.

The adaptive value of positive emotions is supported

by their evolutionarily early origins. Both spontaneous

smiling and laughing have been documented in non-

human primate species, most commonly as part of social

play. 8–10 Gervais and Wilson proposed “nonserious so-

cial incongruity” as the common factor for the stimuli

that elicit spontaneous laughter, which include safe sur-

prise (infants), tickling and physical play (apes, human

children), and incongruity-based humor (human adults,

signing apes). 10 The authors note that laughter is both a

behavioral response and a signal. In their formulation,

laughter and humor beneﬁt both the sender and receiver

by spreading positive emotions that promote stability,

decrease negativity, moderate stress, and strengthen

group identity and cohesion.

Positive emotions presumably activate areas of the

brain involved in reward. 11 The dopamine system is a

critical component of the brain reward circuitry, im-

portant for motivation, affect and reward-associated

functions (Figure 1). 12–16 The majority of dopamine-

containing neurons reside in two midbrain nuclei, the

substantia nigra and the ventral tegmental area (VTA).

The dorsal striatum (caudate and putamen) is the ma-

jor target for the substantia nigra (nigro-striatal projec-

tion). The ventral striatum (nucleus accumbens) is a

major target for the VTA. The VTA projects to multiple

areas of both the cerebral cortex (mesocortical projec-

tions) and limbic system (mesolimbic projections).

It is important to distinguish true humor-evoked

laughter and smiling (Duchenne), which are spontane-

ous emotionally positive responses, from laughter and

smiling that are intentionally generated (non Du-

chenne). 8,10 The neurological pathways involved are

clearly different, as indicated by lesion-induced paresis

of voluntary facial expression with preservation of emo-

tionally evoked facial expression and vice versa (double-

dissociation). 8 Volitional facial paresis has been associ-

ated with lesions in primary motor cortex, premotor

areas (including the frontal operculum), and/or along

the course of the corticobulbar motor tracts. Emotional

paresis has been reported in patients with Parkinson’s

disease, and has been associated with lesions in the thal-

amus and striatal structures as well as in the pons (i.e.,

vicinity of the facial nucleus, CN VII). Recent functional

imaging studies have further delineated the cortical ar-

eas involved (Figure 2). 1–3 Activations (as measured by

either positron emission tomography [PET] or func-

tional MRI [fMRI]) were found within primary motor

cortex, supplementary motor cortex, and the frontal

operculum during voluntary smiling. Primary motor ar-

eas were not activated by humor-induced smiling.

Humor is a complex construct, with several stages of

processing. Although multiple theories of humor exist,

the most accepted is the Incongruity Theory postulated

by Sols. 8,17 He proposed that humor occurs in two

stages. The ﬁrst involves the listener’s expectation of the

joke being disconﬁrmed by the end; the listener encoun-

ters an incongruity (i.e., the punch-line). In the second

stage the listener engages in a form of problem solving

to resolve the incongruity between the punch-line and

the expectation shaped by the joke. This has also been

described as “surprise” and “coherence,” a similar for-

mulation to that of “nonserious social incongruity” (see

above). A third stage has been proposed: detecting that

From the Veterans Affairs Mid Atlantic Mental Illness Research, Edu-

cation, and Clinical Center (K.H.T., R.A.H.); the Mental Health Ser-

vice Line, Salisbury Veterans Affairs Medical Center, Salisbury, NC

(K.H.T., R.A.H.); the Division of Biomedical Sciences, Virginia School

of Osteopathic Medicine, Blacksburg, VA (K.H.T.); the Department

of Physical Medicine and Rehabilitation, Baylor College of Medicine,

Houston, TX (K.H.T); Department of Psychiatry, Wake Forest Uni-

versity School of Medicine, Winston-Salem, NC (M.R.., R.A.H.); De-

partment of Radiology, Wake Forest University School of Medicine,

Winston-Salem, NC (R.A.H.); and the Menninger Department of Psy-

chiatry and Behavioral Sciences, Baylor College of Medicine, Hous-

ton, TX (R.A.H.). Address correspondence to Dr. Robin Hurley, Hef-

ner VA Medical Center, 1601 Brenner Ave., Salisbury, NC 28144;

Robin.Hurley@med.va.gov (e-mail).

J Neuropsychiatry Clin Neurosci 19:4, Fall 2007

http://neuro.psychiatryonline.org

359

W hile negative emotional states have been exten-

2007 American Psychiatric Publishing, Inc.

FUNCTIONAL ANATOMY OF HUMOR

what actually makes sense is pleasant nonsense (appre-

ciation). 8

Functional imaging provides a way to identify areas

of brain involved in different types of humor and stages

of processing. A common approach has been to look for

areas in which activation correlates with a measure of

amusement intensity (funniness). 1–5,18,19 Results can be

complex to interpret. Such activations may be due mul-

tiple processes including solving the incongruity in or-

der to understand the joke and appreciation of the hu-

mor. Results may also be inﬂuenced by how the degree

of funniness is determined. For example, a study that

used the intensity of smiling (as measured by electro-

myography) found activity correlated with smiling only

in medial prefrontal cortex (BA 6) and putamen, both

motor-related areas. 1 Studies that have used subject rat-

ings of funniness, on the other hand, have generally

found much more widespread activations.

Two studies have used conjunction analysis in order

to identify areas of common activation between two

types of humor (Figure 3). 4,5 One study reported a single

area (medial prefrontal cortex, BA 10/11) survived the

two step analysis procedure when comparing two types

of verbally presented humor (puns and semantic jokes). 4

The other study compared two types of visually pre-

sented humor (captioned and uncaptioned cartoons). 5

Multiple regions of activation were found, including

posterior temporal cortex, inferior frontal cortex, hip-

pocampus and parahippocampal cortex, amygdala, nu-

cleus accumbens and midbrain.

Given the adaptive value of humor in promoting posi-

tive emotions, the brain areas activated during the ﬁnal

stage (appreciation) are of particular interest. 20 One in-

triguing study has used event-related fMRI during pre-

sentation of humorous ﬁlms (with and without a laugh

track) to compare the areas activated just prior to laugh-

ter (humor detection) to those active during laughter

(humor appreciation). 21 Humor detection was associ-

ated with activation in the inferior frontal and posterior

temporal cortices for both types of ﬁlm. Humor appre-

ciation was associated with activation in the insular cor-

tex and amygdala. These results are consistent with pre-

vious studies, and support the importance of the

posterior temporal and inferior frontal regions in resolv-

ing the incongruity. The authors of the study also noted

that activation of insular cortex and amygdala is consis-

tent with the visceral and emotional aspects of humor

appreciation. The involvement of the amygdala may

also relate to its role in memory formation, as humorous

material is more easily remembered than material that

is not.

Although the beneﬁcial effects of humor and laughter

have been part of “common wisdom” for many centu-

ries, there is comparatively little solid scientiﬁc research

in this potentially quite important area. 22,23 As noted

above, humor is a complex construct. In research studies

humor has been deﬁned in many ways including a stim-

ulus (e.g., viewing a cartoon or humorous ﬁlm), a re-

sponse (e.g., laughter), a personality trait (e.g., positive

affect), a cognitive process (e.g., resolving the contradic-

tion to understand a joke) and a therapeutic intervention

(e.g., humor therapy). The time frame examined has var-

ied from a few minutes to years, depending upon the

aspect of humor under investigation. The group sizes

range from fewer than 10 individuals to cohorts num-

bering in the thousands.

Studies that focus on the physiological effects of

laughter suggest positive effects on many aspects in-

cluding immunity and pain tolerance, although some

have been criticized on methodological grounds. 22 A

more recent review using the broader deﬁnition of posi-

tive affect (e.g., feelings that reﬂect a level of pleasurable

engagement with the environment) evaluated studies of

physical health. 23 The authors differentiated studies of

trait positive affect (a stable disposition) and state posi-

tive affect (short-term bout), noting that the former

would be more likely to inﬂuence chronic disease pro-

cesses, while the latter would be more likely to inﬂu-

ence occurrence of sudden events. They found that

both prospective and cross-sectional studies support

an association between trait positive affect and better

health, with lower morbidity in a wide range of con-

ditions (e.g., stroke, accident, common cold). This did

not hold for all diseases, particularly those with a high

short-term mortality rate (e.g., melanoma). Laboratory

studies utilizing induction of state positive affect dem-

onstrated generally positive results (e.g., decreased

pain sensitivity/increased pain tolerance, improved

immune response). Laboratory studies of the effect on

stress responses (as indicated by cortisol level) were less

consistent in showing a positive effect. The authors of

this review emphasized that there are multiple ways in

which positive affect might inﬂuence health, some direct

(e.g., changes in health practices) and some indirect

(e.g., susceptibility to disease, sensitivity to stress).

Humor has been integrated into the practice of med-

icine in multiple ways. 24–26 Perhaps the most common

use of humor is to decrease the sense of isolation that is

360

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J Neuropsychiatry Clin Neurosci 19:4, Fall 2007

TABER et al.

often felt by patients, families, and health care workers.

Appropriate use of humor can promote communication

and strengthen relationships. Humor must be used with

care, however, as poorly timed or ill-chosen humor can

be detrimental. Clowns have been used in medicine for

about two decades. A recent study compared anxiety

levels between children accompanied only by parents

and children accompanied by both parents and clowns

during the preoperative period prior to minor surgery. 27

The presence of clowns was associated with signiﬁ-

cantly lower preoperative anxiety, supporting a thera-

peutic beneﬁt. Interestingly, surveys completed by the

medical staff indicated both perception of the beneﬁt to

the child and widespread opposition to continuing the

program.

Two recent studies have explored the effect of very

different humor-centered activities on the behavior of

hospitalized psychiatric patients. 28,29 In one, twice-

weekly clown-lead sessions were provided on an acute

psychiatric ward. 28 Sessions were varied, and included

games, psychomotor expression exercises and activities

based on imaginary situations. Disruptive behaviors

during the intervention period were compared to the

same period of time (83 days) prior to the intervention.

Although there were more patients admitted during in-

tervention period, (101 versus 83) disruptive behaviors

decreased in both absolute and relative terms. Of par-

ticular interest, the most signiﬁcantly reduced behaviors

were attempted elopements, self-injury and ﬁghting.

This change is not likely to be due to differences in the

patient populations, as the distribution by diagnosis

was quite similar during the two time periods. The au-

thors of the study note that most of the treatment plan-

ning in psychiatry is directed toward psychotherapeutic

and pharmacotherapeutic inteventions. There has been

relatively little focus on the therapeutic milieu. In the

second study, movies were provided on two chronic

psychiatric wards 5 days per week for 3 months. 29 One

group viewed only humorous ﬁlms. The other group

viewed a mixture of ﬁlm types, with only 15% being

humorous. The patients were primarily diagnosed with

chronic schizophrenia. A signiﬁcant reduction in clini-

cally rated negative symptoms, anxiety, and depression

was found only in the group that viewed humorous

movies. In addition, self-reported anger was decreased

and social competence was improved. No changes were

found in positive symptoms, activities of daily living,

treatment insight, or therapeutic alliance. The authors of

the study noted that humorous movies appeared to gen-

erate active social exchanges not seen following the non-

humorous (e.g., action adventure) movies. Although

these studies must be considered preliminary, they both

suggest that humor-based interventions can be quite

beneﬁcial to patients with chronic mental illness.

Recently, there has been an increasing emphasis on

recovery-oriented care in the treatment of chronic men-

tal illness. A review of research in this area identiﬁed

multiple mechanisms by which pleasure, play and posi-

tive life events help to develop and strengthen a pa-

tient’s ability to take an active role in promoting recov-

ery. 30 These insights support the need for further study

of the functional anatomy of positive emotions.

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