The neuropsychology of facial expression: A review of the neurological and psychological mechanisms for producing facial expressions

Abstract

Describes the facial musculature and its lower motor neuron innervation. Upper motor neuron innervation from pyramidal and extrapyramidal circuits is explored, with special attention to the respective roles of these systems in voluntary vs emotional facial movements. Also discussed are the evolution of volitional and emotional motor systems, the behavioral and neurological differences between the upper and lower face, the mechanisms of proprioceptive feedback from the face, and asymmetry in facial expression. (117 ref) (PsycINFO Database Record (c) 2012 APA, all rights reserved)

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Neuropsychology of Facial Expression William E. Rinn 1
Psychological Bulletin
1984, Vol. 95, No. 1,52-77
Copyright 1984 by the
American Psychological Association, Inc.
The Neuropsychology of Facial Expression: A Review of
the Neurological and Psychological Mechanisms
for Producing Facial Expressions
William E. Rinn
State University of New York at Stony Brook
This report examines the neuromotor and behavioral aspects of facial expressions.
It begins with an exploration of methodological considerations. This is followed
by a detailed description of the facial musculature and the lower motor neuron
innervation of this musculature. Upper motor neuron innervation from pyramidal
and extrapyramidal circuits is explored, with special attention given to the respective
roles of these two systems in voluntary versus emotional facial movements. Also
discussed are the evolution of volitional and emotional motor systems, the behavioral
and neurological differences between the upper and lower face, the mechanisms of
proprioceptive feedback from the face, and asymmetry in facial expression.
Facial expressions are principally the result
of stereotyped movements of facial skin and
fascia (connective tissue) due to contraction
of the facial muscles in certain combinations.
Such contractions create folds, lines, and
wrinkles in the skin and cause movement of
facial landmarks such as mouth corners and
eyebrows. Although such factors as skin coloration
and perspiration may contribute to a
few expressions, the most salient aspects of
most expressions are the direct result of muscle
action.
The face muscles are not the only muscles
that respond to emotion. The striate muscles
in the neck, back, arms, and so forth, also
contract in response to emotion, as do the
smooth muscles of the blood vessels and alimentary
tract. Nowhere in the body, however,
are the emotions so clearly differentiated from
each other as in the pattern of facial muscle
tension.
This should not be surprising given the role
of the face in communication and the role of
emotional communication in social exchange.
The communication of emotion is central to
early social experience in humans and other
mammals and has been described as lying at
the core of the social process (Engel, 1963;
Hamburg, 1963). Some authorities have even
mammals and has been described as lying at the
core of the social process (Angle, 1963;
Hamburg, 1963). Some authorities have even
suggested that this social-communicative
function of emotion has played a central role
in shaping the evolution of human facial
expression (Andrew, 1965).
So powerful is the communicative impact
of the face that it is difficult to separate the
message from the medium. We tend to describe
facial behaviors not in anatomical terms but
in terms of the emotions portrayed. This tendency
has been a pronounced impact on recent
research.
Objective Description and Measurement
of Facial Expression
Most methods used in research to describe
and quantify facial expressions rely heavily on
the subjective impressions of an observer.
Campbell (1978), for example, asked raters to
gauge which of two faces "looked happier."
Sackiem and Gur (1978) had raters judge the
"intensity" of emotional expressions. There
are several problems with this approach. To
begin with, constructs such as "happiness" and
"intensity" of emotion refer to internal states
that are not directly observable. Most such
studies employ multiple raters, thereby
increasing the reliability of the impression, but
it is not clear that all raters used the same
criteria in arriving at their judgments (e.g.,
brightness of the eyes, movements of the brows,
I wish to express my appreciation to Carroll Izard and Joan Borod
for their very helpful suggestions concerning this manuscript.
Requests for reprints should be sent to William Rinn,
who is now at the Spaulding Rehabilitation Hospital, 125 Nashua Street,
Boston, MA 02114. email: Rinn.William@MGH.Harvard.edu

Neuropsychology of Facial Expression William E. Rinn 2
position of mouth corners, skin coloration,
etc.). Subjective inferences about the internal
states of others can easily become influenced
by idiosyncracies of the raters and their relation
to the poser (e.g., prejudices, sex role
expectations, raters' mood, and social perceptiveness,
etc.). Although the findings of studies
using such methods are by no means invalid
(e.g., Sackiem & Gur, 1978), such methods
add substantially to error variance and make
statistically significant findings more difficult
to obtain.
The development of objective measures of
facial expression has come about mainly
through a de-emphasis on inferring the
"meaning" of the expression and an increase
in emphasis on direct description. One can
objectively describe facial expressions by simply
listing the position and movements of various
lines, wrinkles, folds, and facial landmarks
(see Figure 1) without-regard to the semantic
or emotional meaning expressed.
The measurement system described by
Blurton-Jones (1971) illustrates this approach.
In this system the expression is divided into
nine anatomical components (e.g., brow position,
mouth shape, lip position, eye openness,
tongue position, eye direction, lip separation,
teeth showing, and other miscellaneous). For
each component, a choice of descriptors is
provided for the rater to select among. For eye
openness, for example, the choices are (a) wide,
(b) bit wide, (c) normal, (d) bit narrow, (e)
very narrow, and (f) upper lid down. Detailed
descriptions are provided of the changes that
occur in the appearance of various facial landmarks
during each possible movement.
Another way to objectively describe a facial
expression is in terms of the particular facial
muscles that produce it. Although the muscles
are not directly visible, the facial musculature
underlying various movements of .the skin is
well established (Darwin, 1872/1965; Ekman
& Friesen, 1978). (See Figures 1 and 2.)
Description in terms of muscles has much
to recommend it. It is, first of all, a more direct
reflection of the actions of the nervous system
than is movement of the skin. Second, it allows
a more revealing description of the behavior
than is permitted by accounts of skin movement.
For example, when a person attempts
to mask a sorrowful expression with a smile,
two opposing muscles are brought into play:
Figure 1. Principle landmarks of the face.
the zygomatic major (see Figure 2), which
raises the mouth corners, and the depressor
anguli oris, which lowers them (Oster & Ekman,
1978). The resultant expression could
be described in terms of the emotion it seems
to portray, (e.g., a "brave smile" or an "ironic
smile"), or it could be described strictly in
terms of skin movement. But these approaches
miss the most essential feature of this expression:
the competition between two antagonistic
muscle groups for control of the expression.
Description in terms of muscles also generally
produces a more detailed account of the
event than systems based solely on external
facial features. The "eye openness" component
of Blurton- Jones's protocol (described above)
is a case in point. That system allows descrip
Figure 2. Principle muscles of facial expression.

Neuropsychology of Facial Expression William E. Rinn 3
tion of the eyes only in terms of the height of
the eye opening. This distance, however, can
be influenced by a number of different muscles—
each of which produces a strikingly different
facial appearance. The eyes can become
"narrowed" because the upper lid is drooping
due to relaxation of the levator palpebrae, or
because the inner ring of the orbicularis oculi
is contracted causing a slight elevation of the
lower lid. (This is often seen in anger expressions.)
The eyes can also narrow because the
outer ring of the orbicularis oculi is contracted,
producing a squint, or even because the zygomatic
muscle is contracted, elevating the
check and producing a secondary elevation of
the lower eye lid. All of these distinctions are
missed by Blurton-Jones's system, but would
be picked up by a system based purely on
muscle activity.
Since the muscles are not directly visible,
in order to describe their actions, one needs
a method of translating skin movement into
the muscle patterns that produce them. The
most elaborate instrument for this purpose is
the Facial Action Coding System (FACS; Ekman
& Friesen, 1978). The FACS is a catalog
of all perceptible "action units" (AUs) that the
face is capable of producing and the muscular
basis of these AUs. Action units are not facial
gestalts but discrete movements of some part
of the face. For example, action unit number
5 (AU 5) = upper eyelids raised; AU 4 = brows
lowered and drawn together.
Some AUs can be performed by more than
one muscle. Indeed, some groups of muscles
always act as a unit. For example, the corrugator,
the procerus, and the depressor supercilii
(part of the orbicularis oculi) all act
to draw the brows medially and downward.
Conversely, some muscles are capable of
performing more than one action unit. The medial
and lateral aspects of the frontalis muscle,
for example, can contract independently and
raise the nasal and temporal aspects of the
eyebrows, respectively. Therefore, action units
do not correspond precisely to specific facial
muscles. They are defined strictly in terms of
observable movements of the facial skin.
However, the muscular basis of each AU is
well established, and the FACS permits reliable
inferences about the muscles involved in any
expression.
Reducing the expression to its simplest elements
for objective description does not, of
course, preclude observations regarding combinations
of movements that frequently appear
together. Indeed, the FACS manual lists the
most frequently observed combinations of AUs
for each of six common emotional expressions.
However, the reduction of the expression to a
list of AUs has the advantage of providing a
means of describing any facial configuration,
even one that does not readily fit into a preconceived
category.
Another muscularly based facial coding
system is Izard's (1979) Maximally Discriminative
Facial Movement Coding System
(Max). Unlike the FACS, the Max is not a
comprehensive catalog of all possible facial
movements. Appearance changes that do not
discriminate between different emotions are
not dealt with. The Max manual describes nine
fundamental emotional expressions (those
posited by Izard's Differential Emotion Theory)
in terms of appearance changes detectable
by the Max. Although somewhat less detailed
than the FACS, the Max is easier to use and
may be preferred when one is interested particularly
in examining emotion-based facial
movements. For the study of nonemotional
facial movements (e.g., brow and lip movements
related to speech), or when a highly
detailed description of facial behavior is desired,
a more comprehensive system such as
the FACS is required.
Affectograms
Izard recommends organizing facial expression
data in a format he calls an affectogram
(Izard & Dougherty, 1982). An affectogram is
a graphic representation that illustrates the sequence
and duration of expressions occurring
on a subject's face over a given period of time.
The expressions are represented by various
symbols, with time of occurrence represented
along the abscissa. (See Figure 3.)
The affectogram is an extremely useful way
to organize data on facial behavior. It can facilitate
a detailed comparison of the emotional
reactions of different individuals (e.g., brain
damaged vs. normal) to a given emotion evoking
incident. With repeated measures, it
allows one to analyze maturational changes in
emotional reactions of infants or children to
specific emotion-evoking stimuli. By representing
other neurologically relevant events
(e.g., speech, speech related brow movements,

Neuropsychology of Facial Expression William E. Rinn 4
Figure 3. Individual affectograms. (Two 4-month-old white male infants' affect expressions in response to
the pain of inoculation. From "Two complementary systems for measuring facial expressions in infants and
children" by C. E. Izard and L. M. Dougherty, in C. E. Izard (Ed.), Measuring emotions in infants and
children. Cambridge, England: Cambridge University Press, 1982. Copyright 1982 by Cambridge University
Press. Reprinted by permission.)
gestures, blinks, gaze shifts, physiological
measures, etc.) along the same time line, one
can readily recognize and quantify the rela-
tionships between these variables and various
facial behaviors. Affectograms are simple to
construct and permit a highly detailed description
of a great deal of data in a very succinct
format. (For a discussion of other uses
of affectograms and statistical treatment of
affectogram data, see Izard & Dougherty, 1982.)
Electromyograph (EMG)
It is clear that not all emotional states are
visibly reflected in the facial expression. It has
been shown, however, that the face muscles
often respond to such states even in the
absence of movement of the facial skin.
Using electromyographic (EMG) measures
of electrical potentials in muscles, Schwartz,
Fair, Salt, Mandel, and Klerman (1976a,
1976b) have demonstrated that various
patterns of facial muscle activity reliably
accompany the experience of different
emotional states. For example,
following instructions to imagine a
"happy" situation, increases are seen in the
zygomatic, depressor angular oris, and mentalis
muscles compared with resting baseline,
whereas corrugator activity decreases slightly.
Sad imagery produces increased activity
principally in the corrugators. Angry imagery
produces increases most predominantly in
depressor angular oris activity. With EMG
measures, these patterns are detectable even
When there is little or no movement of the facial
skin (Schwartz, 1982).
Because of this extreme sensitivity, facial
EMG recording may eventually have clinical
utility. A study by Schwartz et al. (1976a),
for example, found that in clinically
depressed patients, the facial muscle response
to happy imagery showed the same patterns
as for nondepressed subjects but in markedly
attenuated form. Conversely, sad imagery
produced a comparatively exaggerated
version of the normal sad pattern.
Additionally, normals and depressives
responded differently when asked to
simply imagine a "typical day." Normals

Neuropsychology of Facial Expression William E. Rinn 5
produced patterns similar to their patterns for
"happy" imagery but in attenuated form. De-
pressives produced an attenuated version of
their "sad" pattern.
Video
Although most observers would agree that
facial behavior plays an important role in
communication, few appreciate the immense
complexity and richness of the messages conveyed.
It is virtually impossible to apprehend
all of it in a single exposure. For this reason,
with the possible exception of EMG studies,
there is no substitute for video recording of
facial behavior.
On reviewing a videotape of a conversation,
the first thing one is struck with is the surprising
frequency of facial gestures. For many
subjects, the face and head are almost constantly
generating expressions and gestures.
These expressive movements are generally
missed in casual conversation. Some expressions
are of very low amplitude and cause only
subtle changes in the overall expression. Many
of these are the results of highly controlled,
skillful suppression of the facial reaction to
emotion. A second reason why many facial
behaviors are missed is that their duration is
too short or too long. Some expressions endure
for as little as 40 msec (Ekman & Friesen,
1975). Others go undetected because they are
virtually constant. It is not uncommon, for
example, for persons to keep their eyebrows
elevated (frontalis muscle) or knitted (corrugators)
for several minutes at a time while engaged
in conversation or mental effort. These
patterns of muscle tension may become visible
only when the face is subsequently relaxed.
Video recording is also necessary to ensure
reliability in observations. Correct descriptions
generally require considerable scrutiny. Ekman
(1980) suggests that the tape be reviewed twice:
once to look for activity in the upper face (eyes
and forehead), and once for the lower face.
Additionally, all movements that are questionable
should be confirmed by reviewing the
relevant segments. It is best to have more than
one judge to establish the reliability of the
observation. Additionally, when viewing the
monitor, it is essential that the observer sit
directly in front of the screen. When multiple
observers are used, they should crowd close
together in front of the monitor. Viewing angles
of more than a few degrees can produce very
convincing illusions of asymmetry in expression.
Artifactual Asymmetry
Studies of asymmetry in facial behavior that
use subjective measures such as intensity of
the emotion displayed must control for certain
perceptual artifacts. It is now well established
that the right hemisphere is superior to the
left in the processing of faces and emotional
expressions (Benton, 1980; Landis, Assal, &
Ferret, 1979; Ley & Bryden, 1979; Patterson
& Bradshaw, 1975; Rizzolatti, Umilta, & Berlucchi,
1971; Suberi & McKeever, 1977). This
is presumably due to the right hemisphere's
greater facility in dealing with visual-spatial
stimuli.
Stimuli in the left side of one's visual field
(everything to the left of fixation) are processed
initially in the right hemisphere. When an observer
looks directly at a poser, the right side
of the poser's face appears in the left visual
field and thus is processed initially by the right
hemisphere. Thus, unless controlled for, the
right hemisphere superiority for processing
faces can lead to the incorrect judgment that
the right face dominates the facial appearance.
(Of course, left visual field information eventually
becomes available to the left hemisphere
because of transmission through the corpus
callosum, but not until considerable right
hemisphere processing and probably some signal
decay have taken place.) Early studies,
which did not control for this artifact, uniformly
found right face dominance in most
subjects (Lindzey, Prince, & Wright, 1952;
McCurdy, 1949; Wolff, 1933). When these artifacts
are controlled for, right face dominance
is much less common (Gilbert & Bakan, 1973).
In fact, recent studies, nearly all of which have
controlled for perceptual asymmetries, have
generally found that the left face dominates
the emotional expression.
Studies using more objective measures such
as facial EMG or anatomically based scoring
of facial movements, without interpretations
of the emotional "message" or "intensity" of
the expression, eliminate these artifacts. The
right hemisphere (left visual field) superiority
is for processing facial gestalts. Neither hemi-

Neuropsychology of Facial Expression William E. Rinn 6
sphere is known to be superior to the other at
detecting movement or estimating distance.
The Muscles of the Face
The muscles of the face may be divided into
two groups according to the function they
serve. Most of the facial muscles attach to the
facial skin or fascia (a subcutaneous sheet of
fibrous material) and manipulate the facial
features into meaningful expressions. However,
on each side of the face, there are four muscles
that attach to bone and ligament and move
these skeletal structures around. These are the
temporalis, the masseter, and the internal and
external pterygoid muscles. These muscles do
respond to emotion, as do the muscles of the
neck and back, and they may even have a
minor effect on facial expression. However,
their primary function is not the communication
of affect. Essentially, these muscles are
responsible for chewing movements of the
jaws. These two groups of muscles (mastication
muscles and expressive or "mimitic" muscles)
use different nerve tracts and have somewhat
different evolutionary origins.
Phylogeny and Ontogeny
Nowhere is the principle that ontogeny re-
capitulates phylogeny better exemplified than
in the facial muscles. The muscles of facial
expression have their evolutionary origin in
the muscles of the breathing apparatus (the
gill arches) of vertebrate fish. Although these
muscles have a striate appearance, their func-
tion in fish is respiratory, and some of the
autonomic connections to these muscles
(through the facial nerve) remain intact in hu-
mans. Because of this, many anatomists classify
the face muscles as viscera (Crelin, 1981;
Noback & Demarest, 1975).
In submammalian land-dwelling animals,
these gill muscles become the sphincter colli
muscle that encircles the neck. In mammals,
the muscles take their place on the head and
form investments in the freely moveable facial
skin and fascia. The mammalian face is, there-
fore, flexible and expressive, whereas the
submammalian face presents a rigid mask (Huber,
1931).
In the human embryo, vestigial gill arches
(called the branchial arches) are present in the
first few weeks of life. The muscles of facial
expression arise from the second of the five
branchial arches, which is located in the site
of the future neck. The muscles of mastication
arise from the first branchial arch, which
corresponds to the jaws in fish. Both sets of
muscles are present by the 5th week of
development. Gradually, the arches develop into
other structures, and the muscles migrate to new
locations, carrying their nerve tracts with
them, so that by the 8th week they have arrived
at their final positions—that is, around the
mouth, nose, and eyes for the muscles of
expression; on the side of the head for the
muscles of mastication (Crelin, 1981).
Behavior
Ekman and Friesen (1975) divide the face
into three regions: (a) the brows and forehead,
(b) the eyes, lids, and root of the nose, and (c)
the lower face, including the cheeks, mouth,
lower nose, and chin. This division is based
on the fact that these regions are largely
motorically independent of each other and make
somewhat independent contributions to the
facial message. Their roles in language illustrate
this point. The lower face participates in
language by articulating the lips, while the upper
face participates by adding a kind of visual
punctuation of the speech, reflecting semantic
emphasis and/or pitch and stress contours of
intonation (Ekman & Friesen, 1975).
Additionally, Darwin (1872/1965) has suggested
that the brows are involved in attention/
concentration and mental effort, frequently being
held high (frontalis) while listening intently to
conversation and drawn down and together
(corrugator) during mental effort, such as
calculation, pondering, and so forth.
The lower and upper face also differ in the
degree of fine motor control. The oral region
is manipulated by many small muscles and
can be moved in almost any direction. The
brows are manipulated by fewer muscles and
can move only up, down, and together (i.e.,
medially).
The lower face also shows considerable lateral
independent of action; that is, one can
unilaterally retract one corner of the mouth
while the other remains relatively still. Few
people have this degree of unilateral movement
in the brows or forehead. Rather the muscles

Neuropsychology of Facial Expression William E. Rinn 7
of the left forehead are neurologically yoked
to those of the right so that independent voluntary
movement is extremely difficult
(DeMyer, 1980;Cf.,Ekman&Friesen, 1978).
These behavioral differences between the
upper and lower face are the result of important
differences in neural innervation of these
two facial regions. These differences will be
discussed later in this report.
Neural Innervation of the Face
Neurons through which the brain innervates
muscles are called motor neurons and are dis-
tinguished from those called sensory neurons,
which bring information to the brain from
sense receptors. Motor neuron circuits have
two parts. Upper motor neurons (UMNs)
carry motor impulses from motor centers in
the brain to the brain stem or spinal cord.
Lower motor neurons (LMNs) carry the impulses
from the brain stem or cord to the muscle
itself. The LMN tract that innervates the
muscles of facial expression is called the seventh
cranial nerve, or simply, the facial nerve.
Another LMN tract that innervates certain
facial muscles is the fifth cranial nerve—the
trigeminal nerve. The functions of these two
nerves differ markedly. The trigeminal nerve
innervates the temporalis, masseter, and the
internal and external pterygoid muscles. As
noted above, these muscles manipulate the
mandibles in chewing movements. By contrast,
the muscles innervated by the facial nerve do
not move any skeletal structures at all. In humans,
the primary function of the facial nerve
is not to perform operations on the environment
but to arrange the facial features in
meaningful configurations. That is, it is specialized for
communication.
Course and Functions of the Facial Nerve
In all, three brain stem nuclei contribute
fibers to the facial nerve tract. Fibers from the
superior salivatory nucleus innervate the lacrimal
and salivary glands in the face. The nucleus
solitarius contributes sensory fibers that
carry taste information from the anterior two
thirds of the tongue. These sensory and autonomic
functions are served by a particular
group of fibers within the facial nerve, called
the nervus intermedius. Although the fibers of
the nervus intermedius share a fiber bundle
with the facial nerve, their functions are
essentially independent. The fibers innervating
the muscles of expression all begin in a small
cluster of cell bodies, the motor nucleus of the
facial nerve, located in the brain stem at the
level of the pons.
The LMN tract of the left face is completely
independent of that of the right face, and their
respective nuclei in the pons are symmetrically
paired and likewise independent. Thus, when
the left and right side of the face behave more
or less identically, it is because more or less
identical signals have been sent to both LMN
nuclei; that is, the integration is accomplished
by UMN circuits. Additionally, when parts of
the face are described as contralaterally or
bilaterally innervated, this means that UMN
fibers from either the opposite (contralateral)
or both (bilateral) hemispheres supply impulses
to the LMN nucleus. The final common
pathway (the LMN) supplies the muscles of
only one side of the face.
The intracranial course of the facial nerve
is well established. Fibers leaving the motor
nucleus loop around the nucleus of the sixth
cranial nerve (involved with eye movements),
then leave the pons, and are joined by fibers
from nuclei salivary and solitarius. The first
major branch given off by the facial nerve
proper is the stapedius branch, which innervates
the stapedius muscle in the middle ear.
The function of the stapedius muscle is to
damp vibrations of the ossicles in the middle
ear. A lesion of this branch will produce a loss
of this damping and cause an oversensitivity
to sound (hyperacusis).
The organization of the peripheral portions
of the facial nerve shows considerable variability
between individuals, both in the course
of its branches and in the specific muscles
innervated by each branch. Five major branches
are usually present, but the adjacent branches
communicate with each other through a network
called the pes anserinus or parotid plexus.
Thus, the precise innervation of any given
muscle in any individual cannot be stated with
certainty (Marker & McCabe, 1977). Figure 4
represents a composite impression of the facial
nerve, based on drawings in Gray (1977),
DeJong (1979), Chusid & McDonald (1962),
and Borland's Medical Dictionary (1974). The
organization depicted in Figure 4 is fairly typical,
but by no means universal.

Neuropsychology of Facial Expression William E. Rinn 8
Figure 4, The five main peripheral branches of the facial
nerve and the muscles innervated by each branch.
In nearly all humans, and in most mammals,
the main trunk divides into an upper
and lower division (the temporofacial and
cervicofacial divisions, respectively) shortly after
emerging onto the face just in front of the ear
through a hole in the skull known as the
stylomastoid foramen. The cervicofacial division
gives rise to the cervical branch, the mandibular
branch, and the buccal branch, all of
which supply muscles of the lower face, as
shown in Figure 4. The temporofacial division
gives off the zygomatic and temporal branches,
which innervate the muscles in the middle
and upper face, respectively. Numerous
smaller branches exist, but these five are
responsible for most visible facial expressions.
The temporofacial division differs from the
cervicofacial division in that the latter carries
impulses from only the contralateral hemisphere
of the brain, while the temporofacial
division—especially the temporal branch —
carries impulses originating in either hemisphere.
This will be explained more fully in
the ensuing discussion of the corticobulbar
pathways. '
The Facial Nerve Nucleus
The motor nucleus of the facial nerve is a
column of cell bodies, about 4 mm long, situated
in the brain stem, about one-third of
the way up from the base of the pons. It is the
largest of the cranial nerve motor nuclei and
contains some 7,000 to 10,000 nerve cells plus
numerous glial cells, (Brodal, 1981; Courville,
1966b). Different anatomists have described
different numbers of cell body groups within
the nucleus. Figure 5 is a schematic representation
of these cell groups and is based on
drawings from five independent studies that
were presented by Courville (1966b).
It is now clear that the various cell groups
in the nucleus map to specific peripheral
branches of the facial nerve: Note in Figure
5 that the various peripheral branches of the
nerve are topographically represented in the
organization of the laterally situated cell
groups. The ventromedial group contains the
cell bodies of the neurons that innervate the
platysma muscle of the neck. The ventrolateral
group contains cell bodies of fibers innervating
muscles that move the lower lip. The lateral
group maps to muscles moving the upper lip.
The dorsolateral (or "intermediate") group
supplies the muscles of the upper face, including
some of the auricular muscles of the
external ear. The dorsomedial and medial
groups innervate the stapedius muscles of the
middle ear and the rest of the auricular muscles
of the external ear.
Some authorities have reported that the facial
muscles map onto the nucleus in a rostral-
caudal (up-down) organization; that is, that
the muscles of the lower face are represented
in the most rostral (highest) regions of the nucleus,
and the upper face muscles map to the
caudal (lower) portion. These reports seem to
be based on the findings of a single study
(Szentagothai, 1948). Courville (1966b) failed
to replicate this finding and attributed the
original discovery to inappropriate methodology.
Figure 5 is based on studies conducted on
lower animals (rabbits, dogs, cats). Similar
groupings of cell bodies are present in the facial
nucleus in humans. Almost certainly, the basic
mapping of face muscles onto the nucleus is
the same as in these other mammals (Vraa-
Jensen, 1942). However, the human facial nucleus
differs from that of lower mammals in
two important respects. First, the laterally situated
groups of cell bodies are much larger in
humans than in other animals, and the
differentiation of various muscles is much finer
(Brodal, 1981; Vraa-Jensen, 1942). This is
especially true of those groups concerned with
movements of the mouth and lower face. This
probably relates to superior fine motor control

Neuropsychology of Facial Expression William E. Rinn 9
Figure 5. The facial nerve nucleus. (This is a schematic composite drawing of a cross section of the facial
nerve motor nucleus, based loosely on five such drawings culled from various studies and appearing in
Courville, 1966a. I have indicated the peripheral branches of the facial nerve that map to each grouping
of cell bodies within the nucleus.)
in this region in humans and our ability to
convey messages through subtle manipulations
of these muscles, both in speech and in facial
expression.
Second, the medial and dorsal medial groups
of cell bodies, which are quite large in lower
mammals, are insignificant in humans. Fibers
from these cells innervate the upper face and
auricular muscles, which move the external
ear in lower mammals as part of the orienting
response. In humans, the auriculars serve the
far less vital function of enabling us to wiggle
the ears.
The Cerebral Cortex
The frontal lobes of the brain are separated
from the parietal lobes by the central sulcus.
The anterior lip of this sulcus is known as the
motor strip and contains a topographical map
of the muscles of the body (see Figure 6). In
general, muscles of the left side of the body
are mapped onto the right motor strip, whereas
the right side of the body is mapped onto the
left motor strip. In each motor strip, the contra-
lateral lower extremity, from the knee down,
is represented on the medial aspects of the
hemisphere. The rest of the musculature is
systematically laid out on the superior and
lateral surface in an organization that
corresponds to the layout of these muscles in the
body.
Neural fibers from each region of the motor
strip follow a systematic course through the
internal capsule and brain stem and form
synapses with brain stem and spinal cord motor
nuclei. Impulses emanating from the motor
strip travel through these pathways to the
LMNs and finally to the muscles themselves.
Electrical stimulation of any given region of
the motor strip will produce contractions of
the muscles represented. In humans, surgical
ablation of any given region of the motor strip
will usually lead to a paralysis of the muscles
represented.
The face representation is on the lateral
aspects of the motor strip. Note in Figure 6 that
the face representation is "upside down" with
respect to the rest of the motor strip. That is,
if one examines the organization of the motor

Neuropsychology of Facial Expression William E. Rinn 10
Figure 6. The primary motor strip of the cerebral cortex. (The diagram schematically shows a front view
of a cross section of the left frontal lobe, cut just anterior to the Rolandic fissure. The relative proportion
of cortical tissue controlling the muscles of various body parts is illustrated by the caricature, as well as by
the length of the dark lines adjacent to the caricature. (From The Cerebral Cortex of Man, by W. Penfield
and T. Rasmussen, New \fork: Macmillan, 1950. Copyright 1950 by MacMillan Publishing Co., Inc., renewed
1978 by Theodore Rasmussen. Reprinted by permission.)
strip, beginning in the median fissure, and follows
its course along the curvature of the
brain's surface, it can be seen that successively
higher (more rostral) body regions are represented
as one progresses toward the temporal
lobe (e.g., toes, calves, thighs, buttocks, stomach,
chest, arms, fingers, neck). The motor
representation of the face reverses this trend
so that the progression is neck, upper face,
middle face, lower face, tongue, larynx. This
reversal is probably due to the fact that the
motor strip emerged very early in mammalian
evolution. Note that in most lower mammals,
the ears and upper face are adjacent to the
neck, whereas the lips and snout are further
rostral.
Note also that the motor strip representations
of the face and hands are disproportionately
large compared with the trunk and legs.
In general, the size of the motor strip
representation reflects the degree of fine motor
control of the region in question (Guyton, 1976).
In this regard, note that the lower face, and
particularly the region representing the lip
area, is disproportionately larger than the upper
face representation. This almost certainly
reflects the relative importance of fine movements
of the lower face in communication.
Corticobulbar Connections
The efferent fibers from the motor strip are
generally referred to as the pyramidal tract.
Fibers going to nuclei in the brain stem are
more specifically labeled corticobulbar tracts,
(This term has its origin in the now obsolete

Neuropsychology of Facial Expression William E. Rinn 11
use of the term bulb for the brain stem.) The
specific organization of the corticobulbar
connections to the facial nerve nucleus are
interesting and reflect important functional
differences between the upper and lower face.
Corticobulbar pathways to the facial nucleus
are of two types: direct and indirect (Brodal,
1981; Noback & Demarest, 1975). Direct fibers
synapse directly on the facial nucleus and
topographically map the motor strip face
representation to the face representation in the
facial nerve nucleus. The indirect pathways
convey cortical influences first to interneurons
in the brain stem reticular formation. From
these, relay neurons deliver the impulses to
the facial nerve nucleus.
Of the direct fibers, those synapsing on cell
body groups that innervate the lower half of
the face (i.e., the ventrolatetal and lateral
groups) emanate exclusively from the contralateral
cortex. However, only about 75% of the
direct corticobulbar fibers innervating the nuclear
representation of the orbicularis oculi
muscle (surrounding the eye) are of contralateral
origin. The remaining 25% project from
the ipsilateral cortex. This trend toward bilateral
innervation is even more pronounced
for the upper face. Direct corticobulbar fibers
to the brows/forehead representation in the
nucleus are about evenly divided between those
emanating from the ipsilateral and contralateral
motor strips (Noback & Demarest, 1975;
DeMyer, 1980). Because of this UMN
organization, unilateral lesions of the motor strip
or corticobulbar pathways will cause contralateral
paralysis of the lower face, although the
upper face muscles, with their bilateral cortical
connections, are relatively unaffected.
The significance of the upper face versus
lower face differences in UMN organization
is best illustrated by considering some general
characteristics of contralaterally versus bilat-
erally innervated muscles elsewhere in the
body. Not all of the body's muscles receive
exclusive, direct contralateral innervation.
Indeed, the other major motor nerve of the face,
the trigeminal, is completely bilaterally
innervated (DeJong, 1979), In general, muscles
of the most distal aspects of the extremities
(the fingers and toes) are completely
contralaterally innervated, whereas the axial
muscles (those along the stomach and back)
are bilaterally innervated (Barr, 1974; DeMyer,
1980; Gardner, 1975).
The contralaterally innervated (distal) muscles
are generally bilaterally independent. This
allows the fingers of the left and right hand,
for example, to simultaneously perform very
different behaviors (e.g., as in playing a musical
instrument.) Bilaterally innervated (axial)
muscles are largely yoked to each other. One
cannot generally contract only one half of one's
stomach muscles, for example (DeMyer, 1980).
The muscles of the lower face, like other
contralaterally innervated muscles, are
bilaterally independent in their functioning. All
normal humans can easily perform unilateral
movements of the lips. Muscles higher on the
face (which are increasingly bilaterally supplied)
are increasingly bilaterally yoked. Many
people, for example, have difficulty with
unilateral winking, that is, contraction of the
orbicularis oculi. Many more are incapable of
deliberately raising just one eyebrow (frontalis
muscles). Moreover, when unilateral brow
movements do occur, they probably utilize
only the contralateral pathways. Penfield and
Jasper (1954) found that unilateral electrical
stimulation of the motor strip representation
of the frontalis produced either contralateral
or else bilateral brow movements. Ipsilateral
movements were never seen.
Another difference between contralaterally
and bilaterally innervated muscles concerns
degree of voluntary control. Contralaterally
innervated muscles have the capacity for fine,
discrete, highly controlled movements,
whereas bilaterally innervated muscles perform
only more gross movements (Leukel,
1978). Similarly, the muscles that manipulate
the lips show considerable voluntary control,
whereas the frontalis and corrugator do not
(Cf., Ekman & Friesen, 1978). Instructions to
manipulate the eyebrows up or down, for
example, frequently lead to coarse, jerky
movements, often in the wrong direction, or no
movement at all (Rinn, Friedman, & Meller,
1982).
Perhaps because of this superior degree of
fine motor control, contralaterally innervated
muscles are involved in learned, skilled motor
behaviors much more commonly than are
bilaterally innervated muscles. The participation
of the lower face in articulating speech is an

Neuropsychology of Facial Expression William E. Rinn 12
example of its role in learned, skilled behaviors.
The upper face shows no comparable behavior.
As noted earlier in this report, the participation
of the upper face in language is restricted
to adding "punctuation" and prosody.
Because they are involved in learned
behaviors, highly contralaterally innervated
muscles tend to have disproportionately large
representations in the cortical motor strip.
Bilaterally supplied (axial) muscles are
minimally represented. Hence, the motor strip
representation of the upper face muscles,
although larger than that of other axial structures
such as the stomach muscles, is modest
compared with the very substantial cortical map
of the lower face.
Other UMN Connections to the
Facial Nerve Nucleus
Indirect corticobulbar pathways carry
impulses from the cortex to interneurons in the
brain stem reticular formation which, in turn,
relay the impulses to the facial nucleus. These
interneuron connections presumably do more
than relay cortical influences. Probably, they
provide for subcortical modulation of cortical
influences and carry direct motor impulses
from subcortical motor areas of the brain. Unlike
the direct corticobulbar pathways, these
interneurons carry impulses to both the left
and right facial nuclei. Thus, whereas the direct
corticobulbar paths to the face are contralateral
in origin, indirect paths are bilateral
(Courville, 1966a; Holstege, Kuypers, &
Dekker, 1977). These indirect, bilateral
pathways are more common for the nuclear
representation of the upper than lower face.
In addition to being bilaterally rather than
contralaterally innervated, the upper face has
another neurological feature that distinguishes
it from the lower face. The cell bodies
representing the upper face in the facial nerve
nucleus (i.e., the dorsomedial and intermediate
groups) receive direct fibers from the
contralateral red nucleus. These fibers (called
the rubrofacial pathways) have no connections at
all with the nuclear cell bodies representing
the lower face (Courville, 1966a). Although it
receives fibers from the ipsilateral frontal cortex,
the red nucleus is not simply a cluster of
interneurons from the indirect corticobulbar
pathways. It is a large, well-defined structure
in the brain stem that gets much of its input
from the contralateral cerebellum (Netter,
1977; Noback & Demarest, 1975). The red
nucleus contains a topographical map of the
contralateral muscles of the body and is believed
to play a role in conveying cerebellar
influences to the extremities. These pathways
probably help to modulate reaching movements
of the arms to various points in space
by constantly adjusting the movement to
compensate for slight errors in trajectory or
distance, that is, they help one to motorically
"zero in" on a given point in space.
The fact that the red nucleus sends fibers
to the nuclear representation of the upper face
(and not to that of the lower face) is difficult
to interpret until one considers that, in lower
mammals, this region of the facial nucleus
also controls ear movements. Such ear
movements are part of the orienting response
and help the animal to focus its attention on a
given point in space. Courville (1966a) has
suggested that the red nucleus conveys
cerebellar influences to help the ears motorically
locate targets. The cerebellum is believed to
play a similar role (albeit without the red
nucleus) in regulating targeted saccadic eye
movements (Gardner, 1975).
Volitional Versus Emotional Innervation
of the Face
Volitionally induced movements of the face
use different UMN pathways than those used
for emotionally induced movements. Impulses
for volitionally induced movements emanate
from the cortical motor strip and course to
the facial nucleus through the pyramidal tract
(or more specifically, the corticobulbar
projections). Impulses for emotional facial
movements arise from a phylogenically older
motor system known as the extrapyramidal
motor system. The extrapyramidal "system" is
not actually a unitary system but a group of
highly interactive neural circuits, each of which
contributes its own specialized influences to the
final motor response. Although neuroanatomists
generally include some cells of the frontal
and prefrontal cortex in the extrapyramidal
system, the system involves mostly subcortical
nuclei, and its influences are conveyed to the

Neuropsychology of Facial Expression William E. Rinn 13
Figure 7. Top. Example of volitional facial paralysis. (The
patient shown has a tumor in the face representation of
the right hemisphere's motor strip. On the left, the patient
is shown attempting to retract both mouth corners in
response to a verbal command by the examiner. A marked
left face paresis is evident. On the right, the same patient
is shown exhibiting a genuine emotional smile. In this
condition, the facial movement is bilateral.) Bottom. Example
of unilateral mimitic facial paralysis (i.e., unilateral
masked face syndrome. This patient has a subcortical cerebral
infarction that is impacting on extrapyramidal motor
functions. He can move his face bilaterally to verbal command,
but shows a striking paresis of the left side of the
face [masked left face] during genuine emotional expressions.
The left picture shows the face at rest; the right
shows a spontaneous smile. (From The Neurologic
Examination, by R N. DeJong, New York: Hoeber Medical
Division, Harper & Row, 1967. Reprinted by permission.)
facial nucleus through pathways other than
the pyramidal tract.
The neuroanatomical distinction between
volitional and emotional facial movements is
a well-established principle of clinical neurology
that has been used diagnostically for more
than 50 years (Monrad-Krohn, 1924, 1927;
Karnosh, 1945; DeJong, 979;DeMyer, 1980). It
is supported by several lines of evidence.
The first line of evidence comes from clinical
observations of patients with lesions of the
cortical motor strip or the corticobulbar
projections that leave the face hemiparalyzed.
Typically, such patients cannot retract the
corners of the mouth to command on the side
contralateral to the lesion. However, the same
patients are commonly seen to smile bilaterally
when something strikes them as amusing (see
Figure 7, top). The emotional smile uses the
same muscles that are paralyzed for voluntary
control and is typically just as pronounced on
the paralyzed as on the nonparalyzed side.
Often, in fact, the smile is exaggerated on the
paralyzed side—probably because of an absence
of normal cortical inhibitory influences (Brodal,
1981). The best explanation for the sparing of
emotional facial movements in corticobulbar
paralysis of the face is that motor systems other
than the corticobulbar system are supplying the
facial nerve nucleus. (It should be noted that,
because they are restricted to the upper face and
ear muscles, the rubrofacial projections
discussed earlier are unlikely to be responsible
for the preservation of emotional expressions in
facial paralysis of cortical origin.)
A second line of evidence comes from
observations of patients with brain lesions
compromising the functioning of various nuclei
in the extrapyramidal motor system, especially
the basal ganglia. Such patients commonly
display a "mimitic facial paralysis"—a condition
in which the patient retains the ability to move
the facial muscles to verbal command but loses
all spontaneous emotional movements. This
phenomenon is most clearly seen in Parkinson's
disease, a progressive neurological disorder
affecting the neurotransmitter systems of the
basal ganglia. In the "masked face" syndrome of
Parkinsonism, the patient shows a marked
diminution of expressive gestures of the face,
including brow movements that accompany
speech, and emotional facial expression.
It is important to note that mimitic facial
paralysis is not simply due to depression. Only
about one third of Parkinson patients show
signs of depression (Celesia & Wanamaker,
1972). Severe depression is much less common
(Barcia & Martinez, 1978), and may be related
to the dementia that is often part of the clinical
picture in Parkinsonism. (Depression is a
common feature of dementia.) By contrast,
the masked face is a cardinal sign of the disease
and is often present in the early stages. It is

Neuropsychology of Facial Expression William E. Rinn 14
typically present even in nondepressed
Parkinson patients and is also seen in patients
with strokes, tumors, and traumatic lesions of
the basal ganglia who show no signs of
depression. Additionally, the masked face is
commonly produced on only one side of the
face, a condition compatible with a neurological
motor disorder, but highly uncharacteristic of
depression. (See Figure 7, bottom.) The sparing
of volitional movements in mimitic facial
paralysis suggests separate motor systems for
these two phenomena.
A third line of evidence for separate circuits
for emotional and volitional facial movements
comes from a surgical procedure called facial
nerve anastomosis. This operation is performed
to reanimate a face that is paralyzed
due to a lesion of the facial nerve at some
point prior to its emergence onto the face. In
this procedure, the motor root of the facial
nerve is surgically severed. The central stump
is avulsed to prevent regrowth while the stump
of the distal portion remains raw. A few fibers
are then teased out of another cranial motor
nerve, usually the spinal accessory nerve
(which supplies the muscles that move the
shoulder). These fibers are then "spliced" into
the distal stump of the facial nerve so that
impulses coursing through the spinal accessory
nerve will now innervate the facial muscles as
well as the muscles of the shoulder.
Following the operation, electrical stimulation
of the motor strip representation of the
face yields no responses. The impulses cease
at the stump of the severed facial nerve.
However, stimulation of the representation of
the shoulder will yield movements in both the
shoulder and the face. Gradually, the patient
learns to move the face muscles volitionally—
apparently at first by attempting to move the
shoulder. In time, a good degree of differential
control is achieved and the face can be moved
without shoulder movements. However, even
years after the operation, with return of good
voluntary facial movement, genuine emotional
movements do not occur on the affected side.
For these patients, genuine smiles are sharply
restricted to the unoperated side. Reportedly,
they frequently find this embarrassing and
avoid such expressions (Kahn, 1966; Schemm,
1961; Schemm & Kahn, 1960).,
The most likely explanation for the absence
of emotional movements on the affected side
is that the motor centers for emotional
movements continue to send their impulses to
the now disconnected stump of the facial nerve.
The behavioral plasticity of the cerebral cortex
allows it to learn to use the new pathway
through the cortical shoulder representation
and the spinal accessory nerve. The more
primitive motor centers for emotional movement
do not have this degree of flexibility.
A fourth line of evidence comes from
observations of nonemotional involuntary
laughing and/or weeping often seen in cases
of pseudobulbar palsy. Pseudobulbar palsy
results from lesions of the corticobulbar
pathways and is commonly seen in cases of
multiple sclerosis, amyotrophic lateral sclerosis,
anoxia, and strokes involving the internal
capsule (Horenstein, 1977). About half of all
patients with pseudobulbar palsy commonly find
themselves laughing or crying with only slight
provocation or no provocation at all (Tinley
& Morrison, 1912; Haymaker, 1969). Once
the response is underway, they are largely
unable to inhibit it and must simply wait until
it abates on its own. These episodes are
generally indistinguishable from normal
laughing and weeping (see Figures 8 and 9). The
face muscles contract into convincing smiles or
crying faces, the face reddens, tears flow. The
respiratory and vocal responses are also at least
grossly identical to emotional responses. The
only obvious difference is that these patients
report no emotional experience during these
bouts, or may even report the presence of an
emotion incompatible with the expression
(e.g., anger or pain while laughing; Poeck,
1969). Patients with pseudobulbar palsy
typically also have at least some degree of
voluntary facial paralysis. It appears that the
involuntary expressions stem from an inability
to voluntarily inhibit these motor release
phenomena through normal cortical influences
(Horenstein, 1977; Brodal, 1981).
Thus, a double dissociation between voluntary
and emotional facial movements can
be demonstrated by the fact that either can be
interrupted or disturbed by neurological damage
while the other remains intact. The question
that next suggests itself is why this should
be true. Why are two (or perhaps more) motor
systems required? An answer to this question
is suggested by an analysis of the evolution of
motor systems.

Neuropsychology of Facial Expression William E. Rinn 15
Figure 8. Pathological crying. (This is a 37-year-old
patient with amyotrophic lateral sclerosis, shown here
during an attack of involuntary nonemotional crying.
The first three shots show her struggling
unsuccessfully to suppress the attack. It is full blown
in the final (lower right) shot. Although the attack
was unpleasant to her, the patient reported that she
did not feel sad. From "Pathophysiology of emotional
disorders associated with brain damage" by K. Poeck,
in P. J. Vinken and G. W. Bruyn (Eds.), Handbook
of clinical neurology (Vol. 3). New York: American
Elsevier, 1969. Reprinted by permission.)
The Evolution of Motor Systems and
Emotional Responses
Several authors have suggested that the
patterned bodily reactions of the emotions have
evolved from similar patterned reactions
associated with certain drive-related behaviors
such as feeding, mating, and basic approach-
avoidance responses (Darwin, 1872/1965;
Plutchik, 1962). Anger and fear postures, for
example, appear to be preparatory sets for fight
and flight responses, respectively. Although
actual emotional experience is usually ascribed
only to higher animals, these drive-related
behaviors are present even in very simple
organisms.
In simple organisms, drive-related responses
are handled by simple reflex circuits. These
primitive circuits do not get discarded when
more sophisticated motor mechanisms evolve.
New systems are simply superimposed on
older ones. The more primitive systems continue
to function in situations for which they
are appropriate. In humans, this reflex mode
of responding is retained in certain brain stem
circuits that regulate respiration, heart rate,
and arousal.
In fish, these reflex circuits are supplemented
by a motor system consisting of the
paleostriatum (analogous to the globus pallidus
in man) and the hypothalamus (Truex &
Carpenter, 1969). In birds, the paleostriatum is
elaborated into the corpus striatum, which
plays the major role in organizing complex,
but instinctive and highly stereotyped behaviors
such as locomotion, feeding, courtship rituals,
and defense. These activities are unaffected
by even total destruction of the primitive
cortex in birds, but are obliterated by lesions
of the corpus striatum (Truex & Carpenter,
1969).
In mammals, the corpus striatum becomes
the basal ganglia, and the cerebral cortex is
more completely developed. Although all
mammals have a cerebral cortex, the cortex
is little involved in these stereotyped, instinctive
behaviors. In most mammals, the near total
destruction of the cortex eliminates only
certain discrete motor functions. However,
destruction of the major portion of the basal
ganglia in mammals leaves only a few gross
movements, primarily brain stem reflexes, intact
(Guyton, 1976).
Although the motor systems described thus
far are well suited for managing behaviors that
are directly and immediately in the service of
basic drives, all of these systems have the
disadvantage that they lack plasticity. The output
is almost completely determined by the
immediate input, and is relatively unaltered by
learning. These systems provide a high degree
of certainty that the response, however simple,
will occur consistently whenever the stimulus
is encountered, but they allow little adaptability
to novel situations.
A central function of the cerebral cortex is
to add a measure of adaptability by allowing
learning to influence motor behavior in a
substantial way. The cortical (i.e., pyramidal)

Neuropsychology of Facial Expression William E. Rinn 16
motor system in humans is extremely plastic and
versatile and is capable of executing fine, highly
complex, highly controlled movements. It can
readily modify the behaviors emitted in response
to changes in the environment or in response to
learning.
The motor portion of the cortex is the frontal
lobes. The extent of frontal lobe development
is a good index of the influence of learning
on the organism's behavior. In humans,
these occupy a larger proportion of the brain
than in any other mammal, and they continue
to grow faster than the rest of the brain until
age 7 or so (Luria, 1973). In lower animals,
even in the higher primates, the frontal lobes
constitute a strikingly smaller proportion of
the brain, and the role of the cortical motor
system is correspondingly smaller. Even with
complete bilateral destruction of the cortical
motor tracts, which would cause massive
paralysis in humans, chimpanzees recover the
ability to feed themselves and to execute
walking and climbing movements (Truex &
Carpenter, 1969). Decorticate dogs and cats can
walk, eat, fight, develop rage, engage in sexual
activity, and generally perform all but the most
intricate types of motor behaviors. The most
obvious result of cortical destruction in
mammals is the destruction of the
purposefulness of the action. Decorticate dogs
may ambulate normally but without direction or
they may fail to negotiate a path around
obstructions (Guyton, 1976).
It is remarkable that destruction of the cortex
has such disparate effects on humans versus
other mammals. Almost certainly, the
explanation is that learning plays a more
important role in the development of the
behaviors in question for humans than it does for
other mammals. Humans develop the ability to
walk, feed themselves, and so forth only after
many months or years of practice. For most
other mammals, these behaviors have an
important instinctual component and are
developed very early in life.
Like other motor systems, the cortical motor
system does not replace its predecessors. In
fact, in humans, some of the most primitive
and vital responses are brain stem reflexes (e.g.,
coughing, sneezing, swallowing, gagging, etc.)
or motor release phenomena that are organized
in the brain stem and hypothalamus (e.g.,
laughing and crying). Normally the cortical
motor system plays very little role in these
behaviors. Most of them cannot even be
performed voluntarily (although rough
approximations are possible), and most are
subject to only partial voluntary inhibition.
Discriminating Cortical Versus Subcortical
Features of Behavior
In general, it may be said that cortically
mediated behaviors (e.g., language) are not
present in infancy and must be learned. They
are generally highly flexible and readily
changeable, thus increasing the organism's
adaptability to novel situations. They may also
show considerable cultural variability.
Typically, we have good conscious awareness of
these behaviors, and they can easily be produced
or inhibited on command. By contrast,
behaviors mediated primarily by other motor
Figure 9. Pathologic laughing. (This 61-year-old woman with amyotrophic lateral sclerosis is shown with
face at rest [1], and in successive stages of involuntary nonemotional laughing. The patient reported that
the laughter was painful and that she was struggling to suppress it as these shots were taken. (From
"Pathophysiology of emotional disorders associated with brain damage" by K. Poeck, in P. J. Vinken and
G. W. Bruyn (Eds.), Handbook of clinical neurology (Vol. 3). New York: American Elsevier, 1969.
Reprinted by permission.

Neuropsychology of Facial Expression William E. Rinn 17
systems (e.g., sneezing, heart beat, etc.) are
generally present very early in development,
not substantially influenced by learning, rigidly
stereotyped in topography, inflexible, and show
little cultural variability. In many cases, we
have poor conscious awareness of the behavior.
Generally, they can only be approximated on
command, and are difficult to inhibit when
they occur spontaneously.
The cortical (i.e., pyramidal) motor system
frequently competes with the more primitive
systems for control of our overt behavior. More
commonly, however, they work together, each
contributing certain elements to the final
response. Thus, any given behavior is the
product of both cortical and subcortical
influences, although these influences are not
always equally strong.
One important role of the cortex is in the
social regulation of the face. Ekman and Friesen
(1975) have coined the term display rules
to refer to socially learned prescriptions for
regulating the emotional expressions, that is,
the social etiquette of facial behavior. Display
rules may call for an expression to be amplified,
tempered, feigned, or masked by a different
expression. Examples of display rules
are that males should not show fear, that females
should not show anger, that one should
smile when addressing guests in a reception
line, that one should not giggle at solemn
occasions, and so forth. Additionally, each
individual has his or her own set of idiosyncratic
display rules—a unique catalog of polite smiles
and learned inhibitions.
The influences of display rules are almost
certainly organized cortically. Manifestations
of display rules are not present in infancy.
Although infants can produce nearly all of the
discrete facial movements and most of the
configurations of movement that adults produce
(Izard, Huebner, Risser, McGinnes, &
Dougherty, 1980; Oster & Ekman, 1978),
configurations characteristic of masking one
expression with another are conspicuously
absent in infants (cf. Oster & Ekman, 1978). The
social regulation of the face does not appear
to even begin until late infancy and is not well
developed until at least middle childhood,
when frontal lobe development is complete.
Learning, through reinforcement, punishment,
and modeling, clearly plays a prominent
role in its development (Ekman & Oster, 1979).
Even in adults, these learned social facial
behaviors are not rigidly programmed but
rather are applied flexibly and can be discarded
altogether when they are not adaptive.
Application of display rules depends on a variety
of factors, including one's age, sex,
socioeconomic status, and the eliciting situation,
as well as on the age, sex, and status of the
person being addressed (Ekman & Friesen,
1975; Oster & Ekman, 1978).
Ekman (1972) and Friesen (1972) have
demonstrated cultural variability in display
rules. In one study, Japanese and American
subjects showed similar facial responses while
watching a stressful film, as long as they did
not know they were being observed. When
another person was present, however, American
subjects continued to show a look of revulsion,
whereas Japanese subjects masked
their expressions. It is also clear that there are
culture-specific sex differences in facial display
rules. To varying degrees in Western culture,
males are expected to inhibit fear expressions
and to act aggressive. Females are expected to
inhibit anger and to act coy.
As with most cortically mediated events,
normal adults have relatively good awareness
of what their faces are doing when they
implement display rules. They have no difficulty
repeating these movements on command and
can easily dispense with them when they seem
not to be adaptive.
In contrast, the structure of genuine
emotional movements of the face is not typical
of cortically mediated events. Unlike most
cortically mediated behaviors, most emotional
facial expressions are present very early in life
(Oster, 1978). Nearly all of the adult
configurations of muscle contractions are seen in
early infancy (Izard et al., 1980; Oster &
Ekman, 1978). These configurations become
associated with specific emotions well before
the end of the second year. Ekman and Oster
(1979) note that distress and disgust expressions
are present at birth. Social smiles begin to
emerge by 4 weeks. "Interest" can be seen in the
face of 3-week-old infants (Oster, 1978). Anger
and contempt may be seen by 6-months (Izard,
1978). Meaningful surprise and fear
configurations are seen in the second year of
life. (Ekman & Oster, 1979).
An extrapyramidal origin for genuine emotional
expressions is also indicated by the fact

Neuropsychology of Facial Expression William E. Rinn 18
that anencephalic infants (infants born with
no cortex, basal ganglia, or other structures
higher than the midbrain) show at least some
normal facial expressions such as crying and
rudimentary aspects of disgust (Guyton, 1976;
Steiner, 1973). The observation that congenitally
blind children display a full range of
spontaneous expressions demonstrates that
learning through imitation is not required
(Freedman, 1964; Goodenough, 1932;
Thompson, 1941).
Emotional expressions are also highly
stereotyped and relatively inflexible. Although
some cultural variability is seen, there are at
least six well-defined expressions that are
common to all human societies: anger, disgust,
happiness, sadness, fear, and surprise (Ekman
& Oster, 1979). Izard (1977) reports that interest
and shame expressions are also universal.
Although we usually (not always) have
conscious awareness of our emotional
expressions, we do a poor job of posing them on
command. Among other things, the timing
(onset and offset) and the coordination of the
various regions of the face (brows, eyes, mouth)
are usually conspicuously off in posed
expressions (Ekman & Friesen, 1975). Certainly,
we frequently have difficulty voluntarily
inhibiting genuine expressions.
Behaviors of the Upper Face
The upper face has a number of behaviors
that have no clear analog in the lower face. It
is difficult to classify some of these behaviors
as volitional or emotional. However, with a
careful analysis of the behaviors themselves,
it is often possible to infer the neural origins
(cortical vs. extrapyramidal) of these
movements. Three upper face behaviors will be
discussed here.
The first is the contraction of the corrugator
muscles during mental effort. The resultant
"knit brow" appearance can often be observed
during problem solving mentation (e.g., while
playing chess, working a crossword puzzle, or
doing difficult mental arithmetic). Although
corrugator contractions are often associated
with unpleasant affect, persons displaying the
knit brow of concentration do not necessarily
experience anything unpleasant. As often as
not, the associated mental task appears to be
recreational.
It is worth noting that simple attention to
a stimulus or task does not produce the knit
brow. It seems rather to require a particular
kind of mental effort. Darwin (1872/1965)
noted that, "A man may be absorbed in the
deepest thought and his brow will remain
smooth until he encounters some obstacle in
his train of reasoning or is interrupted by some
disturbance, and then a frown passes like a
shadow over his brow" (p. 221).
Oster (1978) has observed knit brow
expressions in infants 3 weeks of age. This
makes it unlikely that they are of cortical origin.
Moreover, in adults they commonly appear
even when the subject is unaware that he
or she is being observed. Additionally, Darwin
(1872/1965) documented the universality of
this behavior, noting that people of all cultures
"frown when they are puzzled" (p. 222).
These facts make it unlikely that this expression
is the product of a display rule or any
aspect of the social regulation of the face.
In infants, the knit brow pattern commonly
precedes a smile. Typically, the infant stares
with fixed attention at an object with brows
knit as if studying it. After a few seconds, the
brows relaxed and the zygomatic muscle
contracts the face into a smile. Oster (1978)
believes that the knit brow reflects the effort of
trying to make sense of a new stimulus (i.e.,
trying to integrate it into an existing schema).
When this is finally accomplished, the reduction
of effort causes the brows to relax. The
reduction of effort is held to be affectively
pleasant; hence the smile.
The second type of upper face behavior to
be considered is the tendency to contract the
frontalis muscle during attentive listening. This
phenomenon is commonly seen during
conversation and may be recognized by the
elevation of the brows. EMG studies have also
shown systematic increases in frontalis tension
during attentive listening, with no similar
increases in "control" muscles such as those of
the chin and forearm (Wallerstein, 1954;
Bartoshuk, 1956). These brow responses are
similar to volitional movements in that most
persons can produce them on command. They
are similar to involuntary responses in that
they occur spontaneously and, unless they are
pointed out, most persons remain oblivious
to the fact that they are producing them.
One possible explanation for these brow

Neuropsychology of Facial Expression William E. Rinn 19
behaviors is that they are vestiges of ear perking
movements used by lower mammals to orient
to a given point in space. In lower mammals,
including chimpanzees and gorillas, the frontalis
muscle is continuous with the muscles that move
the ears. It is only with the enlargement of the
frontal lobes in Homo sapiens that the front part
of the skull is pushed forward and the frontalis
muscle becomes separated from the auricular
muscles (Huber, 1931).
Additionally, within the facial nerve nucleus,
the cell body groups that map to the auricular
muscles (the dorsomedial and intermediate)
also map to the frontalis (Courville, 1966a).
Indeed, attempts to wiggle the ears often result
in contractions of the temporal portions of the
frontalis. It is here suggested that signals from
these regions of the facial nucleus, which would
cause ear perking in lower animals, are
responsible for the brow elevations seen in
humans during attentive listening.
The third type of brow behavior to be
considered is described by Ekman and Friesen as
"punctuation" movements. These are very
brief (as short as 50 msec) contractions of the
muscles of the upper face (especially the
frontalis) that occur during speech and appear to
add semantic emphasis or to reflect the pitch
and stress contours of the vocal intonation.
Although these punctuation movements are
commonly bilateral, most persons show some
observable degree of asymmetry. Moreover,
most persons show this asymmetry
systematically, that is, the bias is always or
predominantly in one direction or the other. The
direction of this asymmetry is about evenly
divided between left and right brow dominant
individuals (Rinn et al., 1982). This is in
marked contrast to the well-established left
bias in the lower face during posed expressions
(discussed below; Sackeim & Gur;, 1978;
Campbell, 1978).
Although occurring in the context of speech,
a manifestly cortical and volition behavior,
these punctuation movements have features
more typical of those mediated by
extrapyramidal motor centers. Most subjects are
totally unaware that they move their brows in
this manner. They may deny knowledge of it
even if attention is called to it immediately after
an occurrence. Moreover, most subjects can
volitionally produce only very crude
approximations of the spontaneous movements
on command. This is particularly true for
unilateral punctuation movements. Instructions
to reproduce spontaneous unilateral brow
movements volitionally typically yield bilateral
movements, movements of only the wrong
brow, or no movement at all (Rinn et al.,
1982).
Because the upper face is spared in unilateral
facial paralysis of cortical origin, these
punctuation movements are typically unaffected
by such damage. However, although no
systematic studies have been conducted, I have
observed that punctuation brow movements
are absent in the masked-face syndrome of
Parkinson's disease, in which the functions of
the basal ganglia are compromised. Indeed,
speech itself may lack normal pitch and stress
contours (Chusid, 1979). It therefore seems
likely that the basal ganglia play a major role
in generating these movements. Systematic
observations of masked-face Parkinson patients
has not been conducted to determine
whether they show the knit brow of
concentration, or raised brows during attentive
listening. However, preliminary results of
research I am currently conducting indicate that
congenitally blind subjects commonly produce
a knit brow during puzzlement, elevated brows
during attentive listening, and punctuation
brow movements during speech. This strongly
suggests that these movements are not learned
through imitation, and therefore are not of
cortical origin.
Sensory Functions of the Trigeminal Nerve
I have already given brief mention to the
trigeminal nerve. It was noted above that the
motor portion of the trigeminal innervates the
muscles that move the mandibles during
chewing, but that is only half of the story.
Some branches of the trigeminal nerve are
sensory rather than motoric in function. The
sensory branches carry tactile sensation from
the corneas of the eyes, the inside of the mouth
(including the gums and tongue), the nasal
cavities and paranasal sinuses, the teeth, and
the meninges. They also convey cutaneous
sensation (touch, temperature, and pain) from
the skin of the face and the top of the head,
and proprioception (muscle sense) from the
four chewing muscles that are supplied by the
trigeminal's motor portion (Noback &

Neuropsychology of Facial Expression William E. Rinn 20
Figure 10. The cutaneous distribution of the
sensory branches of the trigeminal nerve.
Demarest, 1975; DeJong, 1979). The portion of
the trigeminal nerve that carries cutaneous
sensation is divided into three branches, each
of which conveys tactile information from a
specific facial region. (See Figure 10.)
The sensory fibers in the trigeminal nerve
terminate in any of three different sensory nuclei
in the brain stem, depending on the kind
of information they carry. Fibers conveying
pain and temperature information from the
three peripheral branches descend to the higher
levels of the spinal cord, where they synapse
in the trigeminal spinal nucleus. Fibers
conveying light touch sensation for the three
regions of the facial skin terminate in the
principal sensory trigeminal nucleus, located in
the pons. The third brain stem nucleus that
receives sensory input from the trigeminal
nerve is the mesencephalic trigeminal nucleus,
located above (rostral to) the pons. This nucleus
is believed to be involved with proprioception
(muscle sense). It receives input from
the muscle stretch receptors in the muscles
supplied by the motor portion of the trigeminal
(i.e., the chewing muscles). It appears that it
also received input from the three branches
of the trigeminal that convey sensation from
the facial skin (Kugelberg, 1952). It sends
output to both the trigeminal and facial motor
nuclei, and appears to play a key role in reflexes
involving the chewing muscles, as well as in
reflexes involving the mimitic muscles.
All three trigeminal sensory nuclei relay the
impulses they receive to the thalamus, which
in turn, relays them to the somatosensory region
of the cortex. The somatosensory cortex
(or sensory strip) is a topographically organized
representation of the body, situated on the
posterior lip of the central sulcus, just across
from the motor strip. The somatosensory cortex
is believed to be the region where conscious
bodily sensations are organized.
Facial Muscle Spindles
The receptor organs for muscle proprioception,
called muscle spindles, operate essentially
as stretch receptors. They are found in
nearly all the striate muscles of the body in
humans and other mammals as well as in fish,
reptiles, and birds (Olkowski & Manocha,
1973). However, there is little evidence for the
existence of muscle spindles in the muscles of
facial expression. Most authorities believe
spindles are either very scarce or absent in
these muscles (Bowden & Mahran, 1956;
Brodal, 1981; Dubner et al., 1978; Gandiglio &
Fra, 1967; Moldaver, 1973; Olkowski &
Manocha, 1973; Sanes & Ison, 1980; Shahani &
Young, 1973). Kadanoff( 1956) found evidence
for a few spindles and other similar structures
in some facial muscles, but noted that they
were aberrant in form and not sensory in nature.
Kugelberg (1952) inferred the presence of
spindles in the orbicularis oculi because
percussion of the skin over this muscle regularly
elicits a blink reflex. He assumed that the
afferent leg of this reflex originated in spindles
in the orbicularis oculi. However, it now appears
that this reflex originates in receptors in the
facial skin rather than muscle and is transmitted
to the brain stem via the trigeminal nerve
(Gandiglio & Fra, 1967; Shahani & Young,
1973).
The apparent lack of spindles in the muscles
of expression is even more striking compared
to their abundance in the muscles of mastication
(supplied by the trigeminal nerve). The
masseter and temporalis, for example, are
among the muscles most richly supplied with
spindles (Kubota, Komatsu, Nakamura, &
Masegi, 1980; Lennartsson, 1980a, 1980b;
Olkowski & Manocha, 1973; Rozhold, 1980a,
1980b). High spindle counts have also been
found in the muscles of the tongue (Rozhold,
1980c), and moderate numbers have been
documented in certain of the extraocular

Neuropsychology of Facial Expression William E. Rinn 21
muscles—the muscles that move the eyes
(Olkowski & Manocha, 1973).
There is no obvious explanation for the
apparent dearth of spindles in the muscles of
expression. Olkowski and Manocha (1973)
have noted that muscles from various regions
of the body may be classed as "spindle poor"
or "spindle rich." The shoulders and thighs
are spindle poor, whereas more distal reaches
of the extremities are more richly supplied.
However, the highest numbers are in the upper
vertebral column and the chewing muscles.
Brown and Rushworth (1973) have suggested
that load bearing muscles (i.e., muscles that
normally work against resistance) could be
expected to contain more spindles than muscles
that work under isotonic conditions. Since the
muscles of expression move no skeletal
structures, they might be expected to contain
fewer spindles.
It should be pointed out that some authorities
believe that all muscles—not just the facial
muscles—are insentient, and that impulses
generated by muscle spindles and other muscle
sense receptors are utilized only in unconscious
reflex circuits. However, it is established that
afferent impulses from muscle spindles find
their way to the cortical somatosensory area—
the region where conscious bodily sensation
is believed to be mediated (Merton, 1972;
Guyton, 1976; Gardner, 1975). It is obvious,
moreover, that people generally report feeling
the state of contraction of their muscles (e.g.,
as when lifting a weight). At this writing, the
issue is unresolved.
A question that immediately comes to mind
is how is it that we are aware of the patterns of
our facial muscle contractions if the muscles are
insentient? There is no clear answer for this
question at this time. Dubner, Sessle, and Storey
(1978) have suggested that mechanoreceptors
deep in the facial skin are sensitive to skin
movement brought about by contraction of the
facial muscles. The sensory impulses would then
be carried to the brain stem via the trigeminal
nerve. When these impulses are integrated in the
sensory cortex, they could provide the basis for
recognizing the expression. This is a plausible
explanation, but at present, it is little more than
speculation. Accounts of the clinical sequelae of
trigeminal nerve damage, including complete
trigeminal tractotomy, generally do not describe
any loss of the patient's sense of his or her facial
expression (cf., Brett, Ferguson, Ebers, & Paty,
1982; DeJong, 1979; Patten, 1978); but this
has not been carefully explored.
Facial Asymmetry and Hemispheric
Differences in Emotion
Over the past 10 years, a sizeable literature
has accumulated describing experimental and
clinical observations indicating that the left
and right hemisphere differ in their emotional
tone. The evidence for this conclusion comes
from a wide variety of studies using diverse
populations and procedures. (See Tucker,
1981, for a review.) Asymmetry in facial
expression is but one line of evidence for this
conclusion, but it is the area most relevant to
the topic at hand. Thus I will restrict my
comments to this point.
Since 1978, a number of studies have reported
findings that the left side of the face
dominates the emotional expression. That is,
the expression emanating from the left side of
the face involves greater facial movement and
is judged more intense than that emanating
from the right side (Borod & Caron, 1980;
Moscovitch & Olds, 1982; Sackeim, Gur, &
Saucy, 1978). In nearly every report, the authors
have explained the findings as an indication
of right hemisphere lateralization for
emotion.
Although this explanation has gained wide
currency, it is not the only one possible. The
chief problem is that it is inconsistent with
the widely accepted dictum that only higher
cortical functions such as language, praxis, or
visual-spatial reasoning are lateralized to a
single hemisphere of the brain. Indeed, Luria's
(1973) principle of progressive lateralization
states that lateralized functions are anatomically
restricted to the secondary and tertiary
association areas of the cerebral cortex. The
emotional tone of one's experience or behavior
is generally believed to be determined by
subcortical systems (e.g., the limbic system, the
hypothalamus, the extrapyramidal motor system,
etc.), and is therefore unlikely to be lateralized.
The main role of higher cortical processes
in emotion is in its instrumental regulation—
the volitional control of emotions — or in the
social regulation of the face (the implementation
of display rules, etc.).
Two alternative explanations of left face
dominance for expression may be advanced,

Neuropsychology of Facial Expression William E. Rinn 22
both of which I believe are more consistent
with established theory and with findings
outlined earlier in his report. The first of these
suggests that findings that appear to show right
hemisphere lateralization for emotion may
actually be due to a left hemisphere superiority
for the inhibition of emotion. It may be noted
that many authorities have suggested that the
frontal cortex inhibits subcortical arousal
mechanisms (Lindsley, 1951; Luria &
Homskaya, 1970; Tucker, 1970). The role of
language (clearly a cortical process) in the
regulation of behavior in general has been
documented by many researchers, most notably
Luria (1973) and Vygotsky (1934/1962). Its
role in emotion control seems most clearly
indicated in the case of cognitive defense
mechanisms (e.g., rationalization,
intellectualization, etc.). I suggest that the left
hemisphere, by virtue of its linguistic and
prepositional thought capabilities, is better
equipped to inhibit unwanted emotional
episodes. This would result in better inhibition
of the right face, and, by default, greater
expressiveness in the left face.
This model also addresses a related issue.
A number of recent studies have suggested
that the right hemisphere is specialized only
for negative (unpleasant) emotions, and that
positive emotions are left hemisphere events.
(See Sackeim et al,, 1982, for a review.) Indeed,
some studies of facial asymmetry have found
left face dominance to be less pronounced or
absent for expressions of positive emotions
(Bruyer, 1981; Sackeim & Gur, 1978;
Schwartz, Ahern, & Brown, 1979). It is here
suggested that this effect is due to unequal
inhibition by the left hemisphere of positive
and negative emotions. It seems unlikely that
anyone would use complex cognitive strategies
to rationalize away their feelings of mirth or
joy. Thus, positive emotions would not be
subject to left hemisphere inhibition and would
not be more inhibited on the right side of the
face. This explanation suggests that the left
hemisphere is not specialized for positive
emotion except in the sense that it does not
inhibit positive emotion as it does negative. It
should be noted that although some studies
have found no asymmetry or very slight left
face dominance for positive emotional
expressions, numerous studies have demonstrated
a substantial left face dominance for smiles
(Borod & Caron, 1980; Campbell, 1978, 1979;
Heller & Levy, 1981;Rinnetal., 1982; Rubin
& Rubin, 1980).
The second alternative explanation for left
face expressive dominance concerns a principle
covered earlier in this report: The cortical
origin of volitionally induced movements of
the face versus the extrapyramidal origin of
genuine emotional movements. If only cortical
functions are lateralized, and only volitionally
induced expressions are cortical, one might
expect only volitionally induced expressions
to be lateralized and, consequently,
asymmetrically displayed on the face. In point of
fact, most studies demonstrating left face
dominance for emotional expressions have
used either posed expressions or expressions
generated in the course of a face-to-face
conversation (a situation in which cortically
mediated display rules become manifest).
Ekman, Hager, and Friesen (1981) have shown
that when subjects do not know they are being
observed, their spontaneous expressions are
essentially symmetrical. Two early studies by
Lynn and Lynn (1938, 1943) in which subjects
were unaware that they were being observed
found smile asymmetries to be nearly evenly
divided between left and right dominant
events. Thus, it would seem that only
volitionally induced or otherwise cortically
mediated expressions are more pronounced on
the left.
Even if the finding of left face (right
hemisphere) dominance is confined to posed
(volitional, social, cortical) expressions, the
finding is still very interesting. Most learned
volitional motor skills are mediated by the left
hemisphere (e.g., speech, praxis). It is, in fact,
a left hemisphere lesion that is usually
responsible for the clinical syndrome of
buccofacial dyspraxia. Patients with buccofacial
dyspraxia are unable to perform complex or
meaningful facial movements, especially in
pantomime, even though they have no facial
weakness. Such patients may be unable to
demonstrate how to use a straw, blow a kiss,
blow out a match, or whistle on verbal command
or by imitation. Preliminary findings of a study
by Borod, Koff, Perlman, and Nicholas,
however, showed that patients with buccofacial
dyspraxia due to left hemisphere lesions
generally retain the ability to pose emotional
expressions (J. C. Borod, personal
communication, February 1982). This confirms
a similar clinical observation by Hécaen (1981).

Neuropsychology of Facial Expression William E. Rinn 23
This finding, together with the finding of left
face dominance for posed expressions, suggests
that the posing of an emotional expression is
an exception to the general principle of left
hemisphere superiority for tasks requiring
complex motor organization.
One possible explanation for this apparent
right hemisphere specialization for volitional
facial expressions is that the posing of an
expression involves a visual-spatial pattern
matching task in which the to-be-matched
pattern is coded primarily in the right
hemisphere. As noted earlier in this report, a
considerable amount of data supports the claim
that recognition and memory for faces and
emotional expressions is essentially lateralized
to the right hemisphere, probably because of
the visual-spatial nature of the stimuli or
processing demands. When we attempt to
motorically construct a facial expression, we are
attempting to arrange the facial features in a
configuration matching one of these sensory
schemas. Since the criterion (to-be-matched)
sensory schema is stored in the right hemisphere,
right hemisphere motor mechanisms may
be best equipped to provide the motor
schema.
Although it cannot categorically be ruled
out that emotion itself is somehow lateralized
to a single hemisphere, or that positive and
negative emotions are lateralized to different
hemispheres, I believe that most or all of the
findings reported in the literature can be just
as well or better explained in terms of more
generally accepted principles of neuropsychology.
Certainly, this is the case for asymmetries
in facial expressions.
Directions for Future Research
Throughout this review, an attempt has been
made not only to present data from a number
of studies, but also to integrate these data and
to suggest general conclusions. Many of these
conclusions can be directly translated into
guidelines for future investigation in the field.
One point that deserves emphasis is the need
for objective description of facial movements.
Studies that have raters infer the nature or
strength of the emotion underlying a given
expression are using very indirect and highly
subjective measures of facial behavior. An
anatomically based system of coding facial
movements is essential to any researcher hoping
to discern the neural basis of these
movements.
Although one can generate anatomically
based descriptions of still photos of facial
expressions, motion pictures are preferable.
Still photos give a very restricted sample of
the subject's facial behavior, showing the
individual's expression as it existed for only a
split second in time. Motion pictures allow
broader sampling, through multiple observations
of the individual over the course of several
minutes. Equally important, still photos give
no clue to the timing of the movement (its
speed of onset, duration, etc.), the expressions
that proceeded or followed it, the vocal and
gestural accompaniments to the expression, or
the situational context in which it occurred.
All of these factors may be important in any
attempt to decipher the neurological basis of
the expression. Videotape is an inexpensive,
accurate, and versatile medium for these
purposes.
Another point to be emphasized is the
desirability of analyzing the upper face
separately from the lower face. These regions
are capable of acting independently of each
other. Descriptions in which they are combined
(as are often seen in studies of facial asymmetry)
may generate conclusions that are valid for only
one of these regions. More importantly, there
are vast differences between the brows and
lower face both in behavior and in the patterns
of neural innervation. Failure to take account
of these differences will confound any study
that hopes to make neurologic or behavioral
statements about the face.
A final point that deserves mention is the
importance of distinguishing between posed
and spontaneous-emotional facial expressions.
Posed expressions utilize cortical (pyramidal)
circuits; spontaneous expressions are of
essentially extrapyramidal origin. In practice,
however, the distinction between volitional and
emotional is not a simple one. Purely volition
expressions may be observed by having subjects
pose expressions to verbal commands.
(Even this method may not completely suffice
if the subject attempts to generate the expression
by imagining an emotion-evoking stimulus.)
To ensure that an expression is purely
spontaneous-emotional it is necessary that the
subject be unaware that he or she is being
observed. This is because most people tend to
hide their feelings from others by volitionally

Neuropsychology of Facial Expression William E. Rinn 24
moderating their facial expressions or by
volitionally superimposing a different expression.
Thus, most expressions generated during face
to face communication have both volitional
(cortical) and emotional (extrapyramidal)
components.
We are only beginning to understand the
neurological basis of the bodily expression of
emotion. Although the work accomplished in
recent years has been marked by creative and
sometimes ingenious methodologies, the
conclusions generated have often departed
radically from accepted principles of
neuropsychology. It would seem that it is now
time to reconcile these departures, either by
modifying recent conclusions or by reassessing
our accepted notions of brain function.
References
Andrew, R. J. (1965). The origins of facial expressions.
Scientific American, 213, 88-94. (Offprint No. 627)
Barcia, D., & Martinez, P. F. (1978). Parkinson's disease with
depression treated with electroshock. Archivos de
Neurobiologia, 41, 393-398.
Barr, M. L. (1974). The human nervous system. Hagerstown,
MD: Harper & Row.
Bartoshuk, A. K. (1956). Electromyographic gradients and
electroencephalographic amplitude during motivated
listening. Canadian Journal of Psychology, 10, 156-164.
Benton, A,, L. (1980). The neuropsychology of facial
recognition. American Psychologist, 35, 176-186.
Blurton-Jones, N. G. (1971). Criteria for describing facial ,
expressions of children, and Human Biology, 43, 365-413.
Borod, J. C, & Caron, H. S. (1980). Facedness and emotion
related to lateral dominance, sex and expression type.
Neuropsychologia, 18, 237-241.
Bowden, R. E. M., & Mahran, Z. Y. (1956). The functional
significance of the pattern of innervation of the muscle
quadratus labii superioris of the rabbit, cat, and rat. Journal
of Anatomy, 90, 217-227.
Brett, D. C, Ferguson, G. G., Ebers, G. C., & Paty, D. W.
(1982). Percutaneous trigeminal rhizotomy: Treatment of
trigeminal neuralgia secondary to multiple sclerosis.
Archives of Neurology, 39, 219-221.
Brodal, A. (1981). Neurological anatomy: In relation to
clinical medicine. New York: Oxford University Press.
Brown, W. F., & Rushworth, G. (1973). Reflex latency
fluctuations in human single motor units. In J. E. Desmedt
(Ed.), New developments in electromyography and clinical
neurophysiology (Vol. 3). Basel: Karger.
Bruyer, R. (1981). Asymmetry of facial expression in brain
damaged subjects. Neuropsychologia, 19, 615-624.
Campbell, R. (1978). Asymmetries in interpreting and
expressing a posed facial expression. Cortex, 14,327-342.
Campbell, R. (1979). Left handers' smiles; Asymmetries in
the projection of a posed expression. Cortex, 15, 571-579.
Celesia, G. G., & Wanamaker, W. M. (1972). Psychiatric
disturbances in Parkinson's disease. Diseases of the
Nervous System, 33, 577-583.
Chusid, J. G. (1979). Nervous system. In M. A. Krupp &
M. J. Chatton (Eds.), Current medical diagnosis and
treatment, 1979 (chap. 16). Los Altos, CA: Lange
Medical Publications, 1979.
Chusid, J. G., & McDonald, J. J. (1962). Correlative
neuroanatomy and functional neurology. Los Altos, CA:
Lange Medical Publications.
Courville, J. (1966a). Rubrobulbar fibres to the facial
nucleus and the lateral reticular nucleus. Brain Research,
1, 317-337.
Courville, J. (1966b). The nucleus of the facial nerve: The
relation between cellular groups and peripheral branches
of the nerve. Brain Research, I, 338-354.
Crelin, E. S. (1981). Development of the musculoskeletal
system. CIBA Clinical Symposia, 33(\).
Darwin, C. R. (1965). The expression of the emotions in
man and animals. Chicago: University of Chicago Press,
1965. (Original work published 1872)
DeJong, R. N. (1979). The neurologic examination (4th
ed.). Hagerstown, MD: Harper & Row.
DeMyer, W. (1980). Technique of the neurologic
examination. New York: McGraw-Hill.
Dorland's illustrated medical dictionary (25th ed.). (1974).
Philadelphia: Saunders.
Dubner, R., Sessle, B. J., & Storey, A. (1978). The neural
basis of oral and facial function. New York: Plenum.
Ekman, P. (1972). Universal and cultural differences in
facial expressions of emotion. Nebraska Symposium on
Motivation, 1971, 207-283.
Ekman, P. (1980, September). Presentation. In G. E.
Schwartz & P. Ekman (Leaders), Advanced Workshop:
Emotion and facial expression: Research and Practice.
Workshop conducted at the meeting of the American
Psychological Association, Montreal.
Ekman, P., & Friesen, W. V. (1975). Unmasking the face.
Englewood Cliffs, NJ: Prentice-Hall.
Ekman, P., & Friesen, W. V. (1978). Facial Action Coding
System. Palo Alto, CA: Consulting Psychologists Press.
Ekman, R, Hager, J. C., & Friesen, W. V. (1981). The
symmetry of emotional and deliberate facial actions.
Psychophysiology, 18, 101-106.
Ekman, P,, & Oster, H. (1979), Facial expressions of
emotion. Annual Review of Psychology, 30, 527-554.
Engle, G. L. (1963). Toward a classification of affects. In
P. H. Knapp (Ed,), Expressions of the emotions in man.
NewYork: International Universities Press.
Freedman, D. G. (1964). Smiling in blind infants and the
issue of innate vs. acquired. Journal of Child Psychology
and Psychiatry, 5, 171-184.
Friesen, W. V. (1972). Cultural differences in facial
expressions in a social situation: An experimental test of
the concept of display rules. Doctoral dissertation,
University of California, San Francisco. Dissertation
Abstracts International, 33, 3976B. (University
Microfilms No. 73- 03651)
Gandiglio, G., & Fra, L. (1967). Further observation on
facial reflexes. Journal of the Neurological Sciences, 5,
273-285.
Gardner, E. (1975). Fundamentals of neurology.
Philadelphia: Saunders,
Gilbert, C, & Bakan, P. (1973). Visual asymmetry in
perception of faces. Neuropsychologia, 11, 355-362.
Goodenough, F. L. (1932). Expression of the emotions in a
blind-deaf child. Journal of Abnormal and Social
Psychology, 27, 328-333.

Neuropsychology of Facial Expression William E. Rinn 25
Gray, H. (1977). Anatomy: Descriptive and surgical
(American revision of 15th English edition of 1901). New
York: Bounty Books.
Gray, H. (1973). Anatomy of the human body (29th American
ed., Charles Mayo Goss, Ed.). Philadelphia: Lea and
Febiger.
Guyton, A. C. (1976). Organ physiology: Structure and
function of the nervous system. Philadelphia: Saunders.
Hamburg, D. A. (1963). Emotions in the perspective of
human evolution. In P. H. Knapp (Ed.), Expression of the
emotions in man. New York: International Universities
Press.
Harker, L. A., & McCabe, B. F. (1977). Surgical anatomy of
the facial nerve. In L. R. Rubin (Ed.), Reanimation of the
paralyzed face: New approaches. Saint Louis, MO: Mosby.
Haymaker, W. (1969). Bing's local diagnosis in neurological
diseases. St. Louis, MO: Mosby.
Hécaen, H. (1981). Apraxias. In S. B. Filskov & T. J. Boll
(Eds.), Handbook of clinical neuropsychology (chap. 8).
New York: Wiley.
Heller, W., & Levy, J. (1981). Perception and expression of
emotion in right handers and left handers.
Neuropsychologia, 19, 263-272.
Holstege, G., Kuypers, G. H. J. M., & Dekker, J. J. (1977).
The organization of bulbar fibre connections to the
trigeminal, facial and hypoglossal motor nuclei. Brain, 100,
265-286.
Horenstein, S. (1977). Emotional aspects of neurologic
disease. In A. B. Baker & L. H. Baker (Eds.), Clinical
Neurology (Vol. 3). Hagerstown, MD: Harper & Row.
Huber, E. (1931). Evolution of the facial musculature and
facial expression. Baltimore, MD: Johns Hopkins
University Press.
Izard, C. E. (1977). Human emotions. New York: Plenum.
Izard, C. E. (1978). On the ontogenesis of emotions and
emotion-cognitive relationships in infancy. In M. Lewis &
L. A. Rosenblum (Eds.), The development of affect. New
York: Plenum.
Izard, C. E. (1979). The Maximally Discriminative Facial
Movement Coding System (Max). Newark: Instructional
Resources Center, University of Delaware.
Izard, C. E., & Dougherty, L. M. (1982). Two complementary
systems for measuring facial expressions in infants and
children. In C. E. Izard (Ed.), Measuring emotions in
infants and children. Cambridge, England: Cambridge
University Press.
Izard, C. E., Huebner, R. R., Risser, D., McGinnes, G. C., &
Dougherty, L. M. (1980). The young infant's ability to
produce discrete emotional expressions. Developmental
Psychology, 16, 132-140.
Kadanoff, D. (1956). Die sensiblen Nervenendigungen in der
mimischen Muskulatur des Menschen. Zeitschrift fur
Mikroskopisch-Anatomisch Forschung, 62, 1-15.
Kahn, E. A. (1966). On facial expression. Clinical
Neurosurgery: Proceedings of the Congress of
Neurological Surgeons, Miami, Florida, 1964. Baltimore,
MD: Williams and Wilkins.
Karnosh, L. J. (1945). Amimia or emotional paralysis of the
face. Diseases of the Nervous System, 6, 106-108.
Kubota, K., Komatsu, S., Nakamura, M., & Masegi, T.
(1980). Muscle spindle supply to the bovine jaw muscles.
Anatomical Record, 197, 413-422. (Biology Abstracts, Vol.
69, Abstract No. 53471.)
Kugelberg, E. (1952). Facial reflexes. Brain, 75, 385-396
Landis, T., Assal, G., & Perret, G. (1979). Opposite cerebral
hemispheric superiorities for visual associative
processing of emotional facial expressions and objects.
Nature, 278, 739-740.
Lennartsson, B. (1980a). Jaw muscle activity during chin
tapping Acta Odontologica Scandinavica, 38, 1-8.
(Biology Abstracts, Vol. 70, Abstract No. 31503.)
Lennartsson, B. (1980b). Number and distribution of
muscle spindles in the masticatory muscles of the rat.
Journal of Anatomy, 130, 279-288. (Biology Abstracts,
Vol. 70, Abstract No. 49391.)
Leukel, F. (1978). Essentials of physiological psychology.
Saint Louis, MO: Mosby.
Ley, R. G., & Bryden, M. P. (1979). Hemispheric
differences in processing emotions and faces. Brain and
Language, 7, 127-138.
Lindsley, D. B. (1951). Emotion. In S. S. Stevens (Ed.),
Handbook of experimental psychology. New York:
Wiley (Interscience).
Lindzey, G., Prince, B., & Wright, H. K. (1952). A study of
facial asymmetry. Journal of Personality, 21, 68-84.
Luria, A. R. (1973). The working brain. New York: Basic.
Luria, A. R., & Homskaya, E. D. (1970). Frontal lobes and
the regulation of arousal processes. In D. I. Mostofsky
(Ed.), Attention: Contemporary theory and analysis.
New York: Appleton-Century-Crofts.
Lynn, J. G., & Lynn, D. R. (1938). Face-hand laterally in
relation to personality. Journal of Abnormal and Social
Psychology, 33, 291-322.
Lynn, J. G., & Lynn, D. R. (1943). Smile and hand
dominance in relation to basic modes of adaptation.
Journal of Abnormal and Social Psychology, 38, 250-276..
McCurdy, H. (1949). Experimental notes on the asymmetry
of the human face. Journal of Abnormal and Social
Psychology, 44, 553-555.
Merton, P. A. (1972). How we control the contraction of
our muscles. Scientific American, 226, 30-37. (Offprint
No. 1249.)
Moldaver, J. (1973). Some comments on blink reflexes. In
J. E. Desmedt (Ed.), New developments in
electromyography and clinical neurophysiology, (Vol.
3). Basel: Karger.
Moldaver, J. (1964). Facial nerve physiology and electrical
analysis. Transactions of American Academy of
Ophthalmology and Otolaryngology, 68, 1045-1059.
Monrad-Krohn, G. H. (1924). On the dissociation of
voluntary and emotional innervation in facial paralysis of
central origin. Brain, 47, 22-35.
Monrad-Krohn, G. H. (1927). A few remarks on the
question of dissociation between voluntary and
emotional innervation in peripheral facial paralysis. Acta
Psychiatrica et Neurologica, 3, 35-39.
Moscovitch, M., & Olds, J. (1982). Asymmetries in
spontaneous facial expressions and their possible relation
to hemispheric specialization. Neuropsychologia, 20, 71-
81.
Netter, F. (1977). The CIBA collection of medical illustra-
tions: Volume I. The nervous system. Summit, NJ: CIBA.
Noback, C. R. & Demarest, R. J. (1975). The human
nervous system: Basic principles of neurobiology (2nd
ed.). New York: McGraw-Hill.
Olkowski, Z., & Manocha, S. L. (1973). Muscle spindles.
In G. H. Bourne (Ed.), The structure and function of
muscle (2nd ed). New York: Academic Press.
Oster, H. (1978). Facial expression and affect development.
In M. Lewis & L. A. Rosenblum (Eds.), The
development of affect. New York: Plenum.

Neuropsychology of Facial Expression William E. Rinn 26
Oster, H., & Ekman, P. (1978). Facial behavior in child
development. In W. A. Collins (Ed.), Minnesota symposium
on child psychology (Vol. 11). Hillsdale, NJ: Erlbaum.
Patten, J. (1978). Neurological differential diagnosis. New
York: Springer.
Patterson, K., & Bradshaw, J. (1975). Differential
hemispheric mediation of nonverbal visual stimuli. Journal
of Experimental Psychology: Human Perception and
Performance, 1, 246-252.
Penfield, W., & Jasper, H. (1954). Epilepsy and the functional
anatomy of the human brain. Boston: Little- Brown.
Plutchik, R. (1962). The emotions; Facts, theories, and a new
model. New York: Random House,
Poeck, K. (1969). Pathophysiology of emotional disorders
associated with brain damage. In P. J. Vinken & G. W.
Bruyn (Eds.), Handbook of clinical neurology (Vol. 3).
New York: American Elsevier.
Rinn, W. E., Friedman, C., & Meller, P. (1982, August). Left
face dominance for spontaneous emotional expressions:
Neuropsychological implications. Paper presented at the
meeting of the American Psychological Association,
Washington, DC.
Rizzolatti, G., Umilta, C., & Berlucchi, G. (1971). Opposite
superiorities of the right and left cerebral hemispheres in
discriminative reaction time to physiognomic and
alphabetical material. Brain, 94, 431-443.
Rozhold, O. (1980a). Are there muscle spindles in the lateral
pterygoid muscle of man? Ada Universitalis Palackinae
Olomucenis Facultatis Medicae (Praha), 1980,94,473-480.
(Biology Abstracts, vol. 72, Abstract No. 25198)
Rozhold, O. (1980b). Exceptions to the rules of
proprioception among muscle spindles in the muscles of the
human head. Acta Universitalis Palackidnae Olomucenis
Facultatis Medicae (Praha), 1980,94,491-498. (Biology
Abstracts, Vol. 72, Abstract No. 10690)
Rozhold, 0. (1980c). Muscle spindles in the external muscles
of the tongue in man. Acta Universitalis Palackianae
Olomuncenis Facultatis Medicae (Phara), 1980,94,431-
443. (Biology Abstracts, Vol. 72, Abstract No. 25197)
Rubin, D. A., & Rubin, R. T. (1980). Differences in
asymmetry of facial expression between left and right
handed children. Neuropsychologia, 18, 373-377.
Rubin, L. R. (1977). Anatomy of facial expression. In L. R.
Rubin (Ed.), Reanimation of the paralyzed face: New
approaches. Saint Louis, MO: Mosby.
Sackeim, H, A., & Gur, R. C. (1978). Lateral asymmetry in
intensity of emotional expression. Neuropsychologia, 16,
473-481.
Sackeim, H. A., Gur, R. C. J., & Saucy, M. C. (1978).
Emotions are expressed more intensely on the left side of
the face. Science, 202, 434-436.
Sackeim, H. A., Greenberg, M. S., Weiman, A. L., Gur, R. C.,
Hungerbuhler, J. P., & Geschwind, N. (1982). Hemispheric
asymmetry in the expression of positive and negative
emotions: Neurologic evidence. Archives of Neurology, 39,
210-218.
Sanes, J. N., & Ison, J. R. (1980). A silent period in
orbicularis oculi muscles of humans. Journal of Neurology,
Neurosurgery, and Psychiatry, 43, 504-509.
Schemm, G. W. (1961). The cortical localization pattern
following cranial nerve cross anastomosis. Journal of
Neurosurgery, 18, 593-596.
Schemm, G. W., & Kahn, E. A. (1960). The effect of
peripheral nerve cross anastomosis on the cortical
localization pattern. Transactions of the American
Neurological Association, 85, 225-226.
Schwartz, G. E. (1982). Psychophysiological patterning and
emotion revisited: A systems perspective. In C. Izard
(Ed.), Measuring emotion in infants and children,
Cambridge, England: Cambridge University Press.
Schwartz, G. E., Ahern, G. L., & Brown, S. L. (1979).
Lateralized facial muscle response to positive and
negative emotional stimuli. Psychophysiology, 16, 561-
571.
Schwartz, G. E., Fair, P. L., Salt, P., Mandel, M. R., &
Klerman, G. L. (1976a). Facial expression and imagery
in depression: An electromyographic study.
Psychosomatic Medicine, 38, 337-347.
Schwartz, G. E., Fair, P. L., Salt, P., Mandel, M. R., &
Klerman, G. L. (1976b). Facial muscle patterning to
affective imagery in depressed and nondepressed
subjects. Science, 192, 489-491.
Shahani, B. T., & Young, R. R. (1973). Blink reflexes in
orbicularis oculi. In J. E. Desmedt (Ed.), New
developments in electromyography and clinical
neurophysiology (Vol. 3). Basel: Karger.
Steiner, J. E. (1973). The gustofacial response: Observation
on normal and anencephalic newborn infants. In J. F.
Bosnia (Ed.), Fourth Symposium on Oral Sensation and
Perception. Bethesda, MD: U.S. Department of Health,
Education, and Welfare.
Suberi, M., & McKeever, W. F. (1977). Differential right
hemispheric memory storage of emotional and
nonemotional faces. Neuropsychologia, 15, 757-768.
Szentagothai, J. (1948). The representation of the facial and
scalp muscles in the facial nucleus. Journal of
Comparative Neurology, 88, 207-220.'
Thompson, J. (1941). Development of facial expression of
emotion in blind and seeing children. Archives of
Psychology, 1-47.
Tinley, F., & Morrison, J. F. (1912). Pseudobulbar palsy,
clinically and pathologically considered, with the clinical
report of five cases. Journal of Nervous and Mental
Disease, 39, 505-535.
Truex, R. C, & Carpenter, M. B. (1969). Human
neuroanatomy. Baltimore, MD: Williams and Wilkins.
Tucker, D. M. (1981). Lateral brain function, emotion, and
conceptualization. Psychological Bulletin, 89, 19- 46.
Tucker, I. F. (1970). Adjustment: Models and mechanisms.
New York: Academic Press.
Vraa-Jensen, G. (1942). The motor nucleus of the facial
nerve: With a survey of the efferent innervation of the
facial muscles. Copenhagen: Enjar Munksgaard.
Vygotsky, L. S. (1962). Thought and language (E.
Hanfman & G. Vakar, trans.). Cambridge, MA: M.I.T.
Press, 1962 (Original work published in Russian, 1934).
Wallerstein, H. (1954). An electromyographic study of
attentive listening. Canadian Journal of Psychology, 8,
228-238.
Wolff, W. (1933). The experimental study of forms of
expression. Journal of Personality, 2, 168-176.
Received April 14, 1982
Revision received May 16, 1983 •