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Brain 2009: 132; 1989–1992
| 1989
BRAIN
A JOURNAL OF NEUROLOGY
BOOK REVIEW
Another way to understand
The two dominating views emanating from the early studies on
the motor system developed from two opposite angles. The sensory motor perspective dating back to Descartes (1664) envisioned
movements as the result of sensory stimuli. This view was later
supported by the neurophysiology of reflexes operating at
different levels of complexity (Jackson, 1931).
The ideomotor theory originating from psychology (Lotze, 1852;
James, 1890) took the opposite motor–sensory perspective regarding volition and intention as the major source of actions. Voluntary
actions were considered in terms of their behavioural goals and
the percepts they generate. But there is a voluntary automatic
dissociation since the way this is accomplished by motor commands remains subconscious: the ongoing execution processes
are automatically adjusted.
The concepts of common coding (Prinz, 1990) and of motor
imagery (Jeannerod, 1994, 1997) broadened the theoretical
framework by recognizing the pivotal role of commensurate sensory motor representations and of motor simulation. Jeannerod
considered covert motor actions as actions in their own right. In
neural terms, the state where an action is simulated and the state
preceding its execution are similar, thus constituting a continuum
between covert and overt stages. Envisaging action observation as
another form of covert action brought the close relation between
action understanding and action performance into focus.
Neuroimaging studies showed that action execution, imitation,
imagination and observation can all recruit similar brain circuitries
and show subliminal activation of the motor system. The elaboration of the functional anatomy of motor cognition not only
allowed a better understanding of the links between perception
and action, but also opened fresh approaches for the study of
the first-person versus third-person perspective by identifying the
neural circuitries engaged in the distinction between self and
others.
These concepts provided fertile ground for a breakthrough in
the field of experimental neurophysiology, the discovery of the
mirror neurones in the early 1990s by Rizzolatti and his colleagues
in Parma (Gallese et al., 1996; Rizzolatti et al., 1996). This novel
operational principle disclosed the dual representational mode of
action and action observation at the level of single neurones.
Using the investigative repertoire in the human, its application to
higher functions could be pursued; and the evolving implications
MIRRORS IN THE
BRAIN: HOW OUR
MINDS SHARE
ACTIONS AND
EMOTIONS
By Giacomo Rozzolati
and Corrado Sinigaglia
2007.
Oxford and New York:
Oxford University Press
ISBN: 978-0-19921798-4
Price: £24.95/$44.95
(Hardback)
began to penetrate the cognitive and social sciences and
the humanities. Therefore, it is timely to have an authentic
account of the development of the mirror neurone story and its
presumed theoretical implications as presented by Giacomo
Rizzolatti and philosopher of science Corrado Sinigaglia in their
book ‘Mirrors in the Brain’.
The story originated from observations in the monkey lab about
the surprising property of neurones in ventral premotor cortex
which discharged not only when the monkey performed a
motor act such as grasping an apple, but also when a monkey
observed the very same gesture produced by someone else.
The first chapters place this new feature of neuronal functioning
in its historical context and provide the reader with some relevant
background information about the functional organization of
the sensory motor system.
Special attention is given to the role of the three visual information streams in understanding the pre-processing of the relevant sensory information. The ventrodorsal stream is addressed as
a major route with two specialized types of neurones of interest.
The neurones in the anterior part of the superior temporal sulcus
(STS) respond selectively to a wide range of body movements
performed by others (Perrett et al., 1989). These neurones differ
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1990
| Brain 2009: 132; 1989–1992
from the mirror neurones in that they are not active during any of
the monkey’s own movements. However, their ability to identify
movements performed by others conveys suitable information to
the next processing stage, the anterior inferior parietal lobule.
Other than the STS neurones, many of the parietal neurones are
multimodal. They respond not only when particular movements
are seen, but also when these movements are carried out. Thus
they reveal the same characteristic features of mirror neurones as
first observed in the next processing stage in the premotor cortex.
Visuomotor neurones in the premotor cortex had been
described before. The so-called canonical premotor neurones discharge when an object is seen as well as when the monkey
performs the subsequent gesture of grasping the object. In contrast to these canonical neurones, the mirror neurones do not
discharge when the objects are seen, but only and selectively
when trained monkeys perform specific movements or when
they observe the same gesture being performed by the experimenter or by another monkey. Such a specific relationship
between movement and movement observation can be specified
for a number of different prototypical gestures such as holding,
manipulating, placing, bimanual interactions and in particular
grasping. The activation of the mirror neurones is limited to
those motor acts involving a body part—to object interaction, so
called transitive motor acts.
In his discussion of the implications of the mirror neuron system,
Jeannerod (2001) proposed that one major function is linked
to imitative behaviour. Rizzolatti and Sinigaglia regard this interpretation as less likely since true imitation, as developed in
humans, does not yet exist in the brains of macaques. They
view these neurones as primarily involved in the understanding
of the meaning of actions performed by other conspecifics. This
matching hypothesis implicates the immediate recognition of
specific types of action and the preparation of a response in the
most appropriate manner. This recognition process takes its meaning on the basis of the accumulated motor knowledge and
the vocabulary of motor acts in the brain of the observer. This
resonance in turn enables the observer to interpret the intention of
motor events. This is facilitated by one other feature of mirror
neurones: they can deal with different modalities such as sound
or vision, or vision and sound. The latter is particularly relevant for
the oro-facial cortical representation, which shows mirror neurone
properties for ingestive actions (biting an apple) as well as for
communicative (expressive grimacing) gestures.
The next important step in the development of the mirror neurone concept was to prove its existence in the human. Functional
neuroimaging, magnetoencephalography and transcranial magnetic stimulation (TMS) studies provided converging evidence
that during observation of hand–arm, foot and mouth actions
ventral premotor cortex become consistently activated. Concerns
that these activations in the vicinity of Broca’s area are due to
internal verbalization of the observed actions were eliminated by
revealing that different effectors activate specific parts of premotor
cortex according to its somatotopic organization, loosely following
the homuncular pattern of the primary motor cortex (Buccino
et al., 2001). An important additional feature was that the posterior parietal lobe is activated in addition to the premotor cortex
during the observation of object-related actions. These activations
Book Review
also follow a somatotopic pattern. These data indicate that the
mirror system is more extended in the human than in monkeys.
In addition, the human mirror neurone system can also code
intransitive motor acts and miming. Such direct access to the
motor areas is seen as the basis for immediate understanding
devoid of any conceptual, mental or linguistic mediation. Of
course there are other means of understanding intentions
conveyed by the movements of others. But mirror neurones are
regarded as key players, since no other neural system has been
identified to explain these immediate mind-reading capacities.
In pursuing the question of whether or not the mirror system
may operate at higher levels of complexity, the next chapter of
the book deals with imitation and language. The authors emphasize that the term imitation has two meanings. One is the capacity
to replicate a motor act which already belongs to the agent’s
motor repertoire. The second is to envisage imitation for the
purpose of learning a new pattern on the basis of action observation. Regarding replication the principle of ideomotor compatibility
requires a common representational domain for perception and
action. Various experiments underpin the involvement of the
mirror system in action imitation by replication revealing
activations of the frontal pole of the mirror system in the left
inferior frontal gyrus. In contrast, imitational learning activated
prefrontal Brodmann area 46 in addition to the premotor and
parietal areas (Buccino et al., 2004a).
The human data thus provide evidence that the mirror neurone
system plays a pivotal role in communication such as manual
pantomime, intransitive gestures and oro-facial communicative
expressions. The authors raise the issue of whether progressive
evolution of the mirror neurone system is at the root of the formation of a neural substrate for communicative behaviour. Simian
experiments had already identified a new variant of mouth mirror
neurones that respond to the sight of intransitive communicative
gestures such as lip smacking or teeth grinding. This variant added
a novel quality to the conventional type of ingestive mouth mirror
neurones. Experiments on human subjects using TMS provided
evidence for such a view. These experiments showed that the
motor potentials from the lips are enhanced only when subjects
listen to speech or look at corresponding lip movements but only
in response to stimulation of the left hemisphere.
Ingestive and communicative oro-facial gestures use a common
set of movement prototypes. One is the mouth open–close alternation that could represent an evolutionary milestone from chewing and mastication to the participation of these activities in calls
and speaking. The progressive integration of these facial, vocal
and manual gestures is seen as the building block for language
evolution thus providing a gestural origin for language at the
beginning with ‘speaking’ by action later integrated with phonetics. Consequently, the evolution towards language may have
undergone several stages: first, lip reading predominantly using
the mimetic gestural system followed by the emergence of a
bimodal proto-language formed of gestures and sounds and finally
the appearance of a prevalently vocal system of communication.
Sketching a possible evolutionary scenario over the last
20 million years, the authors infer that the last step of the transition to an autonomous vocal system must have meant that the
motor neurones responsible for controlling the oro-laryngeal
Book Review
gestures acquired the capacity to become active in response to
sounds produced by corresponding utterances of other conspecifics. Envisaging the evolution of an ‘echo-mirror neurone system’
as the neural basis of oral language introduces a major new argument into the controversial discussions about language evolution.
The final chapter deals with emotions. ‘The Expression of the
Emotions in Man and Animal’ by Charles Darwin (1872) is taken
as an impressive example—many of the illustrations sketched by
Duchenne—to demonstrate that a repertoire of emotional primitives has been preserved throughout evolution. The authors raise
the question whether an emotional mirror system would not be
more effective in understanding the meaning of observed
emotional expressions than the full sensory analysis and cognitive
processing chain. Since many of the primary emotions are related
to ingestion, taste and smell, the insular lobe is seen as playing a
pivotal role. As a cortical area for exteroceptive and enteroceptive
processing, it represents a nodal structure for the mediation of
a range of elementary emotions. The authors’ proposal that the
understanding of the emotive states of others depends on a mirror
mechanism that codes the sensory information directly in
emotional terms is supported by a number of studies. According
to this view the lack of such a mechanism would allow the
perception of emotional behaviour but leave it ‘purely cognitive
in form - pale, colourless, destitute of emotional warmth’ (James,
1890). Thus, the immediate understanding of the emotional
behaviour of others on the basis of the emotional mirror neurone
system is considered as a candidate for the mediation of empathy.
The book closes by concluding that, although the mirror
neurone system acquired a successively more complex organization and architecture during evolution, the underlying mechanisms
preserve a common functional matrix. Therefore the elucidation of
the nature of the mirror neurone system provides a starting point
for the investigation of the cerebral processes responsible for a
vast range of behaviours including the most complex levels of
inter-individual and social relationships. The authors consider the
transformation of the arbitrary divisions between perceptive,
motor and cognitive processes into a more coherent picture as a
major advance. The different subsystems become bound by the
acting brain into a pragmatic, pre-conceptual and pre-linguistic
form of understanding—some form of essential cognition. Such
a rapid system seems suitable for catching important value setting
and salient features to gate the motivational and emotional processes involved in the formation of mental processes. The book
develops a fascinating and coherent story about the gradual development from the early observations on a small strand of neurones
in a limited portion of the premotor cortex to the perspective of a
widespread system that developed during evolution and has come
to assume particular relevance in the human species.
The vast impact of the discovery of the mirror neurones on the
field of motor neuroscience is reflected by the intense discussion
about the implications. The core concept that mirror neurones
allow the observer to understand a perceived action by means
of motor simulation of the agent’s observed movements seems
generally accepted. But the generalizations envisaging the mirror
system as operational principle underlying many higher level brain
functions meet reservations. For language, the motor theory of
speech perception (Liberman et al., 1967) has paved the way as
Brain 2009: 132; 1989–1992
| 1991
it has become a pertinent theme in cognitive science during the
past half century, although so far lacking any known neural
substrate.
It is the attribution of the mirror neurone system to a motor
theory of social cognition in particular that has been debated by
many researchers in the field. There is a controversy over the claim
that the mirror system only resonates to those movements which
are already part of the ‘vocabulary of motor acts’. This assumption
is based on experiments which revealed activations only when
subjects observed movements that were part of their own motor
repertoire. Observations of movements outside the subjects’ own
motor repertoire, such as dogs barking, produce no activations
(Buccino et al., 2004b). There is, however, a growing body of
evidence showing that animals can exhibit perceptual competencies that do not show up in their motor repertoire, thus challenging the role of motor knowledge as a premise for resonating the
meaning of movements performed by others (Wood et al., 2007).
Jacob and Jeannerod (2005) agree that the mirror system allows
an observer to understand a perceived action by simulation
without executing it. But they envisage the motor properties of
the mirror system as ‘well designed for representing an agent’s
motor intention involved in an object-oriented action, not for
representing an agent’s social intention’.
Implicit processes are at the core of the authors’ conclusion that
‘our perceptions of the motor acts and emotive reactions of others
appear to be united by a mirror mechanism that permits our
brain to immediately understand what we are seeing, feeling, or
imagining others to be doing, as it triggers the same neural
structures . . . that are responsible for our own actions and emotions’. In their book, A Universe of Consciousness, Edelman and
Tononi (2001) envisage ‘external reality’ as a construction of the
brain from a chaotic, constantly changing world without labels.
But their point of departure is the synthesis of sophisticated
sensory information and semantic enrichment as creating the
qualia and the knowledge we have about our surroundings.
The concept that ‘the acting brain is also and above all a brain
that understands’ introduces a complementary perspective.
Knoblich and Prinz (2005) point to an important difference
between the two approaches: sensory analysis and semantic
enrichment provide information about the past and the present;
but motor systems are anticipation engines, providing information
about the future, the consequences of a given action, the anticipation what the other is going to do next on the basis the
simulation processes that operate in real time.
Since the cognitive aspects of motor behaviour that determine
our conscious interaction with the environment are processed in
parallel with the automatic processing streams, the resonancebased and the analytical operational modes may interact at multiple re-entrant levels. The study of such interactions in the
complex networks in which mirror neurones participate will be a
major challenge for future research.
Hans-Joachim Freund
University of Dusseldorf
Advance Access publication May 11, 2009
1992
| Brain 2009: 132; 1989–1992
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