PersPecTives
opinion
Active perception: sensorimotor
circuits as a cortical basis for language
Friedemann Pulvermüller and Luciano Fadiga
Abstract | Action and perception are functionally linked in the brain, but a hotly
debated question is whether perception and comprehension of stimuli depend on
motor circuits. Brain language mechanisms are ideal for addressing this question.
Neuroimaging investigations have found specific motor activations when subjects
understand speech sounds, word meanings and sentence structures. Moreover,
studies involving transcranial magnetic stimulation and patients with lesions
affecting inferior frontal regions of the brain have shown contributions of motor
circuits to the comprehension of phonemes, semantic categories and grammar.
These data show that language comprehension benefits from frontocentral action
systems, indicating that action and perception circuits are interdependent.
The brain collects information about the
environment through sensory systems and
computes motor responses. How sensory
and motor systems interact and how higher
cognitive processes contribute to these com­
putations is not fully understood. An influ­
ential theory views input systems as separate
from motor systems: input systems filter
sensory input in a feedforward manner 1,
resulting in perceptual processes which, after
possible interaction with attention, emo­
tion and memory modules, influence motor
systems controlling actions2,3. According to
this ‘separation’ view, the posterior part of
the cortex of higher mammals is mainly con­
cerned with sensory information, whereas
the frontal motor cortex (which includes
premotor and primary motor areas) serves
a ‘slave’ role under the dictate of perceptual
and cognitive systems.
Recent years have seen major challenges
to this hypothesis through the discovery of
sensorimotor neurons that are active during
both action execution and corresponding
perceptions (see Supplementary
information S1 (box)). The monkey pre­
motor area F5 contains such mirror neurons,
which show striking specificity: they fire
during the execution of actions of a specific
type (for example, peanut breaking) and
equally during the observation of another
individual (monkey or human) performing
the same action4. They may even respond to
the sound of that action5. The multimodal
action specificity of mirror neurons suggests
action–perception integration at the neuro­
nal level, possibly in the form of neuronal
circuits distributed over sensory and motor
areas6,7. According to this ‘integration’ view,
perception, cognition and motor control
share neuronal mechanisms to which senso­
rimotor neurons are of key importance6,8–11.
Action–perception circuits as a basis of
higher cognition offer an alternative to the
view that action and perception mechanisms
are segregated. In the separation view,
perception­related mirror activity in motor
systems could be interpreted as sensory­to­
motor ‘overspill’ that does not contribute
to perception. Motor system activation
during perception would accordingly
emerge owing to input from perceptual
areas, but the opposite link — from motor to
perception circuits — would either be absent
or have no basic function in perception. The
importance of sensory input for action con­
trol is widely accepted12, and an evaluation
of — and eventually a decision between —
the two theories depends on the relevance of
activity in motor systems for perception and
nATuRe RevIewS | NeuroscieNce
comprehension. Recent research into the
brain basis of language has shed light on
the neural circuits underlying different
facets of the perception and comprehension
of signs, their meaning and syntactic struc­
ture. This information is essential for assess­
ing the relevance of motor mechanisms in
perception and comprehension.
Here, we first highlight anatomical and
neurocomputational data on the general
properties of language circuits and then ana­
lytically review neurofunctional studies of
phonological, semantic and syntactic processes
in the healthy and functionally impaired
human brain. This evidence leads us to
conclude that language mechanisms involve
functionally interdependent brain systems
for action and perception.
Functional neuroanatomy of language
Comparative neuroanatomical and neuro­
physiological studies have suggested that a
sector of mirror neuron area F5 in macaques
is cytoarchitectonically comparable to
Brodmann area 44 (BA 44) in the human
inferior frontal cortex, which is part of
Broca’s area13. Studies have shown this area
to be active in human action observation,
action imagery and language understand­
ing 14–16. This suggests a possible evolutionary
relationship between monkey mirror
neurons and the emergence of human
language through a sensorimotor matching
mechanism in the human ‘motor brain’ that
might be important for cognitive processes9.
In macaques, extensive neuroanatomical
links exist between premotor areas and pari­
etal areas involved in somatosensory and
visual processing and, consistent with these
structural connections, all of these areas
contain mirror neurons10,17.
Despite anatomical and physiological
evidence supporting a possible link between
mirror neurons and human language, there
is a fundamental quantitative difference
between human language and the com­
munication systems of apes and monkeys.
Humans easily master vocabularies compris­
ing tens of thousands of words and symbols,
whereas our closest relatives use up to only
40 signs, including their species­specific
calls18. In addition, only humans have well­
known syntactic abilities, which apply to all
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PersPectives
action domains (see the section on grammar,
below). At the neuroanatomical level, the
two principal regions for language —
the superior temporal areas adjacent to the
auditory cortex and the inferior frontal areas
anterior to the articulatory motor cortex —
are connected by several white­matter tracts:
the extreme capsule, the uncinate fascicle
and the arcuate fascicle. The arcuate
fascicle is well developed in the left,
language­dominant hemisphere of the
human brain but weakly developed in apes
and monkeys (FIG. 1). Thus, the substantial
differences in vocabulary size and syntactic
complexity have an anatomical correlate
in frontotemporal action–perception con­
nections, suggesting that these connections
could be the basis of the differences.
Humans are born with remarkable per­
ceptual sensitivities that allow them to detect
basic properties of speech that are common to
all languages. However, during the first year
of life, these sensitivities undergo modifica­
tion, reflecting an exquisite tuning to phono­
logical properties of the native language19,20.
Interestingly, during this babbling phase
a
b
Human
IFS
Syllable repetition
CS IPS
10
45
47
44
39
40
PrCS
9
46
PMd
F3op
22
6
STS
37
21
T1p
Chimpanzee
CS
IFS 46 8 PrCS
T 1a
39
40
22
37
45 44 6
47
FOP
IPS
Sentence comprehension
STS
F3tri
Macaque
AS
45 44
CS
6
T2p
IPS
7a
7b
22
FUS
STS
F3orb
T2a
Figure 1 | cortical anatomy underlying language processing: from monkeys to humans.
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a | Frontotemporal connections in the left hemisphere of the brain inNature
humans,
chimpanzees
and
macaques. These frontotemporal connections are present in monkeys128 but became richer during
evolution, especially the dorsal connection by way of the arcuate fascicle129. in humans, the frontotemporal link through the arcuate fascicle is stronger in the left hemisphere than in the right hemisphere25. The numbers indicate Brodmann areas. b | Frontotemporal connections in the human brain
between areas that are active during syllable repetition and during sentence comprehension through
the arcuate fascicle (upper arc in the top diagram) and the extreme capsule (lower arc in both diagrams). We propose that rich frontotemporal connections are necessary for binding auditory and
articulatory information in action–perception circuits (BOX 1). As, anterior sulcus; cs, central sulcus;
FOP, frontal operculum; F3op, pars opercularis (also known as Brodmann area 44); F3orb, orbital part
of the inferior frontal gyrus; F3tri, triangular part of the inferior frontal gyrus; FUs, fusiform gyrus; iFs,
inferior frontal sulcus; iPs, intraparietal sulcus; PMd, dorsal premotor cortex; Prcs, precentral sulcus;
sTs, superior temporal sulcus; T1a, anterior part of the superior temporal gyrus; T2a, anterior part of
the middle temporal gyrus; T1p, posterior part of the superior temporal gyrus; T2p, posterior part
of the middle temporal gyrus. Part a is modified, with permission, from Nature Neuroscience REF. 129
© (2008) Macmillan Publishers Ltd. All rights reserved. Part b is reproduced, with permission, from
REF. 130 © (2008) National Academy of sciences.
352 | MAy 2010 | voluMe 11
(months 6–12), the sounds that babies articu­
late become increasingly similar to the types
of speech sounds, or phonemes, that they
hear frequently; such acoustic–phonological
tuning to language­specific sounds is also
manifest in neurophysiology 21,22, suggesting
sensorimotor interactions.
Rich links between articulatory and audi­
tory neurons are required to learn the
precise mapping between acoustic patterns
and the motor programmes necessary for
successful word repetition, which emerges
after the babbling phase23. The articulation
of a word (and the early babbling of syl­
lables) is controlled by neuronal activity in
the inferior frontal motor cortex, which is in
turn controlled by inferior frontal premotor
and prefrontal circuits (BOX 1). At the same
time, speech sounds and spoken words elicit
activity in the auditory system, mainly in
superior temporal primary auditory, audi­
tory belt and parabelt areas. Importantly,
connections between these sites enable
the cortex to strengthen these links and
thereby store correlations between inferior
frontal neurons that contribute to articula­
tory actions and superior temporal neurons
that are involved in auditory perception. As
neurons that frequently fire together also
strengthen their mutual connections, early
articulations and word production lead to the
emergence of action–perception circuits for
phonemes and words7,24. In addition, synaptic
strengthening due to co­activation also sug­
gests that somatosensory neurons might be
involved in these action–perception circuits.
Action–perception learning of speech
sounds and spoken words requires strong,
reciprocal superior temporal–inferior frontal
connections. As mentioned above, these
connections are strong only in humans
and are weak in non­human primates.
This might therefore explain why language
has not emerged in non­human primates. In
addition, the brain laterality of language could
be explained by the structural asymmetry
of the arcuate fascicle, which is more pro­
nounced in the left hemisphere in humans25,
giving the left perisylvian cortex a privileged
status in building action–perception circuits
for speech7. This hypothesis does not rule
out the possibility of the opposite causal
link — stronger fibres developing as a
consequence of laterality — but offers an
explanation of language laterality based on
anatomical and physiological observations.
we acknowledge that, apart from action–
perception learning, the human brain also
supports the purely perceptual learning
of small vocabularies of word forms in
the absence of articulation26, but note that
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monkeys also exhibit this type of perceptual
learning 27. notably, children with severe
neurological motor deficits that affected
articulation had reduced auditory vocabular­
ies — that is, they understood fewer words
than children with similar deficits that did
not affect articulation28 — a finding consist­
ent with the importance of motor links for
vocabulary learning.
neurocomputational studies of early stages
of language acquisition and adult language
processing further confirm the importance
of action–perception links in building neu­
ronal correlates of phonemes and words29–31.
neuronal­network studies incorporating
synaptic learning rules and neuroanatomical
connectivity between simulated areas support
the view that, in the healthy, non­deprived
brain, correlated activation of connected
articulatory and acoustic cortical systems
leads to the emergence of distributed action–
perception circuits during language learning
(BOX 1). The role of these circuits in sound and
word processing is discussed below.
The motor side of speech perception
when we articulate a syllable, a word or a
sentence, our self­produced sounds stimu­
late the auditory system in the superior
temporal cortex. However, activation of
the superior temporal cortex, including the
temporal plane, was also seen in subjects
when the sounds created by their whispered
articulations were masked by noise, and this
activation increased with speech rate32, sug­
gesting motor­to­auditory activation flow
in the cortex during speech production.
Conversely, listening to speech sounds that
require strong articulatory activity — espe­
cially the rolling ‘r’ — activates the motor
system, as revealed by measuring muscle
excitation following magnetic stimulation of
the motor cortex 15,33. neurometabolic studies
confirm that the inferior frontal premotor
cortex and the prefrontal cortex are active
during the identification and discrimination
of speech sounds and also during passive
speech perception34–37.
Speech sounds elicit stronger activity
than similar, non­speech stimuli in the ante­
rior and lateral superior temporal cortex 38,39,
and recent studies reported that this region
also exhibits fine­grained activation differ­
ences depending on the phoneme type37,40,41.
In speech production, phonetic­distinctive
features — for example, tongue tip­produced
‘alveolar’ phonemes (such as ‘t’) versus
lip­produced ‘bilabial’ phonemes (such as
‘p’) — show somatotopy in the way they are
mapped onto the motor system (precentral
gyrus). Interestingly, the lateral part of the
Box 1 | Functional anatomy of language: from brain areas to neuronal circuits
a
b
M1
PF PM
c
Lesion
in
M1
PM
PF
PB
AB
A1
A1AB
PB
M1
Speech production
PM
PF
PB
AB
A1
Speech perception
OK
Delay
Error
Fail
OK
Delay
Error
Fail
5
3
7
12
51
100
0
23
14
12
34
0
0
7
73
71
15
0
95
67
6
5
0
0
100
49
1
0
0
0
0
29
23
3
10
12
0
22
70
9
3
5
0
0
6
88
87
83
Computational models that replicate cortical structure and function have provided evidence for the
Nature
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| Neuroscience
existence of action–perception circuits distributed over inferior frontal and
superior
temporal
areas of
the human cortex. Six main areas of the left-perisylvian language cortex are shown by different colours
in part a of the figure. Part b shows the corresponding ‘areas’ that were used in a model network
architecture mimicking the language cortex30: primary auditory (A1), auditory belt (AB), auditory
parabelt (PB) in the superior temporal region (Brodmann area 41 (BA 41), BA 42 and BA 22), prefrontal
(PF; BA 45), premotor (PM; includes both BA 44 and BA 6) and primary motor (M1; BA 4) cortex in the
inferior frontal cortex. Connections between the modelled areas incorporated links that have been
shown in neuroanatomical studies (FIG. 1). The production of speech sounds and whole words was
modelled by simultaneous activation of neurons in motor (M1) and auditory (A1) areas, leading to a
spread of activation throughout the six areas of the model. As realistic Hebbian learning was used to
modify the weights of connections, neurons that activated together became more strongly connected.
This process yielded specific but partly overlapping distributed neuronal circuits for individual speech
sounds and words. After learning, any stimulation of a word’s auditory neurons in A1 led to full
activation of the entire circuit, even spreading towards its motor neurons in M1 (REFs 30,118).
This observation shows that the word-specific neuronal assemblies developed by the model link
together action and perception circuits. These and related studies29,119 show that human neuroanatomy
and general neurophysiological principles produce action–perception circuits for language as a
consequence of learning. The networks can be used to predict linguistic brain activation30.
The action–perception model of word processing explains important features of language deficits
caused by disease of the brain. Most of these deficits affect speech production as well as speech
perception and comprehension. However, there can be a predominance of deficits in either the
action or the perception domain. Inferior frontal lesions tend to cause pronounced deficits in
speech production, whereas superior temporal lesions have the greatest effect on perception.
The model explains these features as follows: multimodal deficits arise because lesions to the
centre of the action–perception circuit (areas PM, PF, PB and AB) compromise circuit function in
general. The double dissociation between motor (Broca’s) aphasia and sensory (Wernicke’s) aphasia
caused by inferior frontal (PF and PM) and superior temporal (AB and PB) lesions, respectively, arises
because focal lesions of key loci within a distributed circuit have different effects on general
network function: a lesion in a circuit towards its ‘motor’ end reduces activity propagation to the
motor output; a lesion close to its ‘auditory’ end reduces the effect of incoming activity, in addition
to the lesion effect on general circuit function. The closer a lesion is to the input or output fibres of
the circuit, the greater the imbalance between deficits in action and perception. In the extreme,
after a lesion in one of the peripheral areas of the network (M1 or A1), circuits are cut off from their
output or input but circuit function is not substantially impaired; this results in isolated motor or
auditory deficits. These conclusions were confirmed in a neurocomputational ‘lesion’ study, in
which 75% of the artificial neurons in each simulated area of the model of the language cortex were
selectively damaged31. The table (see the figure, part c) lists the percentage of network responses
that are correct and impaired after lesions in particular ‘areas’ in simulations of word production
and recognition. As distributed circuits explain the double dissociation between action and
perception deficits, they provide an alternative to modular models according to which action
and perception are supported by separate processing components (see also REF.3). Figures are
reproduced, with permission, from REF. 30 © (2008) Wiley-Blackwell.
nATuRe RevIewS | NeuroscieNce
voluMe 11 | MAy 2010 | 353
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PersPectives
precentral cortex that is active in ‘p’ sound
production is also activated during listening
to ‘p’ sounds, and the inferior precentral area
involved in producing a ‘t’ sound is activated
when hearing the sound37. Somatotopic
activation in the motor system therefore not
only reflects phonetic distinctions between
speech sounds, but also indicates phonetic–
linguistic correspondence between articu­
lated and heard phonemes and even includes
specific information about how speech
sounds are produced (FIG. 2). whether other
phonetic features (such as voicing and nasal­
ity) are also reflected in somatotopic motor
system activation should be addressed in
future studies.
The motor somatotopy associated with
hearing speech, as revealed in transcranial
magnetic stimulation (TMS) and functional
MRI studies15,37, shows that the motor system
extracts fine­grained phonological informa­
tion and suggests that this information is
relevant in the speech perception process.
a Articulator movement
Silent articulation
Lip M1
Tongue M1
Listening to syllables
130
% Response time
b
Indeed, a group of theories has postulated
that action mechanisms are important
in speech perception24,42–44. However, the
functional­separation view of motor and
sensory brain mechanisms questions such
general relevance, an opinion that was also
put forward in recent publications39,45 with
the suggestion that “motor processes that
are involved in speech production do not
directly contribute to speech perception
and comprehension”39. we now address this
controversy by briefly reviewing the relevant
data from neuropsychology.
The separation of sensory and motor
processes for language can be traced back
to the comments of nineteenth­century
neurologists on language deficits caused by
brain lesions. “Sensorial aphasia” following
posterior brain lesion was characterized as
“loss of understanding of spoken and writ­
ten language” but “preservation of [the]
faculty of volitional speech”46, whereas
“motor aphasia” following inferior frontal
Labial
Dental
120
110
100
90
80
Tongue M1
Lip M1
Figure 2 | speech sounds in motor systems. Neuroscience research has revealed the brain correlates
Nature Reviews
| Neuroscience
of speech sounds and their phonetic features. These were found in the superior
temporal
cortex and
also in the cortical motor system. a | Brain activation revealed by functional Mri during articulator
movements (left panel; tongue movement shown in green and lip movement shown in red), silent
articulation of syllables including ‘t’ or ‘p’ (middle panel; ‘t’ articulation shown in green and ‘p’ articulation shown in red) and listening to syllables including ‘p’ and ‘t’ sounds (right panel).The similarity
between these activation patterns shows that, in the motor system, hearing speech sounds that are
produced with the tongue and lips activates brain areas that are involved in the production of those
tongue- and lip-related sounds and in simple repetitive tongue and lip movements14,37. b | stimulation
points in a transcranial magnetic stimulation study (left panel) and the resulting change in response
times in a speech perception task (right panel). consistent with the action–perception model (BOX 1),
weak magnetic stimulation of the lip and tongue areas in the left, dominant hemisphere biases the
perceptual system to ‘hear’ the concordant speech sound (‘p’ in case of lip motor area stimulation)
and to incorrectly perceive incongruent phonemes55. Part a is reproduced, with permission, from
REF. 37 © (2006) National Academy of sciences. Part b is reproduced, with permission, from REF. 55
© (2009) cell Press.
354 | MAy 2010 | voluMe 11
lesions was characterized as loss of volitional
speech with spared understanding of spoken
words47. Clearly, such binary descriptions
in terms of ‘spared’ and ‘impaired’ func­
tions are inappropriate for describing the
usually gradual (not all­or­nothing) effect
of brain lesions, and it was wernicke who
highlighted specific problems in “voluntary
speech” in cases of “sensorial” aphasia48.
However, speech and language problems
were not observed in patients with “motor”
aphasia resulting from inferior frontal
lesions46–48.
However, the deficit in speech compre­
hension in all types of aphasia — includ­
ing motor (also known as Broca’s) aphasia
— is so well known and established that a
sentence comprehension test, the Token
Test 49, is widely used in the clinic to identify
patients with aphasia among individuals
with brain lesions. Although patients with
inferior frontal lesions and Broca’s aphasia
usually have mildly impaired speech
comprehension50, some of them may present
without comprehension impairments in
clinical tests of single­word comprehen­
sion. However, a good performance on tests
developed to detect profound deficits should
not be taken as evidence of spared func­
tions. If speech is speeded up and overlaid by
noise, as is often the case in real life, single­
word comprehension is impaired in patients
with a left inferior frontal lesion and Broca’s
aphasia51 and, even under optimal percep­
tual conditions, single­word comprehension
is delayed51 and the normal activation in
response to phonologically similar words is
reduced52,53. These studies show that lesions
in inferior frontal and premotor areas com­
promise the patients’ ability to comprehend
meaningful words.
understanding single words requires at
least two types of information: phonologi­
cal information about relevant acoustic fea­
tures of speech sounds, which is required
for speech perception; and information
about the meaning of words, which is
required for semantic comprehension.
In action–perception circuits, the activated
action part sends back excitatory projec­
tions to the auditory–perception part,
leading to facilitation; lesions in inferior
frontal areas impair the speech perception
process because they degrade this feedback
activation and hinder the circuit in becom­
ing fully active (BOX 1). At the phonological
level, this mechanism can be probed in
experiments assessing the discrimination
and identification of phonemes or
syllables in isolation. Interestingly, the
discrimination and identification of speech
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sounds and syllables is impaired in apha­
sic patients with lesions in the frontal
cortex 54 (BOX 1; for further discussion, see
Supplementary information S2 (box)).
At a more specific level, TMS of lip and
tongue areas in the precentral cortex had a
considerable effect on phoneme identifica­
tion in people listening to consonant–vowel
syllables that were overlaid by noise55.
Interestingly, stimulation of the tongue area
increased the accuracy and speed with which
tongue­related sounds were identified, but
led to errors and delays in perceiving
lip­related sounds. The opposite pattern
arose when the lip area of the precentral
cortex was stimulated: ‘d’ and ‘t’ sounds
tended to be misheard as ‘b’ and ‘p’ sounds,
and processing speed was increased for lip
sounds but slowed for tongue sounds (FIG. 2).
Together with the lesion evidence and other
TMS studies15,56,57, this recent work dem­
onstrates an essential and specific role of
the premotor cortex and/or primary motor
cortex in speech perception and confirms
predictions of a neurobiological model of
language in which action and perception
mechanisms are bound together in distrib­
uted cell assemblies7,30 that include mirror
neurons58. However, as we and others have
argued before, these results provide only
partial support for the motor theory of
speech perception, which originally postu­
lated that there is a motor system for speech
processing that is functionally separate from
the system for non­linguistic action process­
ing; such modularity is difficult to reconcile
with current neuroscience data indicating
that the same precentral area is involved in
moving the tongue and in pronouncing a ‘t’
sound37,44,45,55 (FIG. 2).
Category-specific semantic circuits
Contrasting with the relatively focused peri­
sylvian areas involved in speech perception,
a wide range of additional cortical areas has
been found to be active during semantic
comprehension36,59. As, in one view, the
meaning of a word is the object it relates to60,
the area that links words to their meanings
was sought in the middle and inferior tem­
poral cortex, where auditory language areas
and the visual stream for object processing
converge. Specific inferior temporal areas are
indeed activated by words conveying differ­
ent kinds of visual information (for example,
“round” versus “brown”)61–64. However, the
visual system and adjacent areas are not the
only brain regions that processes object­
related information about word meaning.
For example, words related to odours (for
example, “cinnamon”) activate olfactory
brain areas more strongly than do control
words65, without drawing specifically on the
middle or inferior temporal cortex. A similar
point has been made about words that are
semantically related to sounds (for example,
“telephone”), which strongly activate supe­
rior temporal auditory areas even if pre­
sented in written form131. These and similar
results confirm that there is semantic activa­
tion in perceptual areas and adjacent cortices
where information from different modalities
converges59,61,66,67. notably, local activation
differences in perceptual brain systems,
such as the visual and olfactory areas, reflect
semantic differences in word meaning (for
example, relating to object or odour infor­
mation, respectively)7,61,68,69.
However, the meaning of many types of
words is not related to objects or sensations
but to actions60. For example, the processing
of action­related words such as “grasp” has a
functional correlate in the activation of hand
representation areas in the premotor
and motor cortex, as has been shown
using various imaging methods62,70,71. even
fine­grained semantic differences between
action­related words are manifest in motor
activation. words referring to actions pref­
erentially performed with a particular part
of the body (for example, “lick”, “pick” and
“kick”) activate motor and premotor areas
in a somatotopic manner 72,73. Similar activa­
tions were reported for action phrases and
sentences74,75, even abstract ones (for
example, “she grasped the idea”)76. This
somatotopy of action semantics — that
aspects of the meaning of action­related
verbs and sentences can be read from brain
activation maps — suggests that the motor
system contains topographically specific
semantic circuits for fine­grained action
word categories (BOX 2). note that semantic
links to the motor system have been shown
only for words related to actions that the
individuals typically can perform them­
selves; such semantic motor links are absent
for non­human actions (for example, bark­
ing and tail­waggling) and may not occur
in subjects who cannot perform an action
owing to a neurological disease.
neurophysiological (electroencephal­
ography and magnetoencephalography)
studies of the time course of the processing
of action­related words showed rapid activa­
tion of motor regions in response to action­
related words and early somatotopic mapping
of word meaning. This activation occurred
100–250 ms after the information needed to
identify a stimulus word was present — that
is, after the onset of presentation of written
words and after the word recognition point77
nATuRe RevIewS | NeuroscieNce
of spoken words78–80. As the earliest brain
responses indexing the comprehension of
word and sentence meaning occur at the same
time81,82, this early meaning­related motor
system activation is probably a manifestation
of semantic processing rather than a process
that follows meaning comprehension11.
whether action–perception circuits
are necessary for semantic processing can
be investigated using neuropsychological
methods that explore the effect of activity
changes in the cortex on the behaviour of
individuals who have acquired language
normally. A wealth of studies on category­
specific deficits indicate that the frontal
(motor) cortex and the temporo­occipital
(sensory) cortex contribute to different
degrees to the processing of noun catego­
ries — for example, tool words (which relate
to the actions that the tools are used for)
and animal names (which lack an action
relationship)83,84. Data from patients with
stroke­induced lesions in inferior frontal or
temporal areas indicate a double dissocia­
tion between processing action­related verbs
and object­related nouns84–89. Processing of
action­related verbs is also impaired spe­
cifically in patients with degenerative brain
diseases that affect the motor system or
its direct vicinity, including motor neuron
disease90, Parkinson’s disease91,92 and the
‘frontal’ variant of frontotemporal demen­
tia93. These selective noun–verb deficits can
be interpreted in the context of an action–
perception model: most, although certainly
not all, verbs are semantically related to
actions, whereas many nouns tend to relate
to object information that is available
through the visual modality (for data and
discussion, see REF. 94). It has been argued
that the activation of inferior frontal areas
in response to hearing action­related verbs
might be unrelated to the comprehension of
action­related aspects of the words’ mean­
ings95; however, patients with motor neuron
disease or lesions in the left inferior frontal
cortex show parallel impairments in process­
ing action­related verbs and in grouping
action­related pictures according to semantic
similarity 90,96,97. These results show that the
inferior frontal cortex is necessary for the
processing of action­related concepts and
action­related verbs.
The crucial role of the motor system for
semantic processing is most clearly shown
in studies using well­matched subcatego­
ries of action­related words that only differ
minimally in the action types to which
they refer. In a TMS study in which hand
and leg representations of the motor cor­
tex were stimulated, the subjects showed
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Box 2 | Action–perception circuits for semantic processing: models, brain activation and vulnerability to lesions
b
a
–40
–15
Spoken-word form
Colour-related word
Shape-related word
Arm-related word
Leg-related word
Face-related word
c
0
Awg d-prime value
4.0
3.5
3.0
Colour-related word
Shape-related word
Face-related word
Arm-related word
2.5
2.0
1.5
1.0
0.5
0.0
Colour Shape
Face
Arm
Computational modelling, brain activation experiments and
neuropsychological patient studies provide converging support for
category-specific semantic circuits. Part a of the figure shows a model
of action–perception circuits for spoken words and their meaning.
Word-related circuits (shown in grey in the figure, part a) are located
in the perisylvian language cortex, especially inferior frontal and
superior temporal areas, and are strongly lateralized to the dominant
left hemisphere (see also BOX 1). The learned, arbitrary links between
the form of words and their meanings are provided by the coupling
between these word-related circuits and semantic action–perception
circuits (illustrated by different colours in the other brain diagrams in
part a). The higher-order assemblies (including both word formand meaning-related circuits) are specific to the semantic category and
store information about the actions and objects that the words are
typically used to describe. Semantic circuits of words related to
actions that are preferentially performed by moving the face (shown
in green), arms (shown in red), and legs (shown in purple) involve
neurons in somatotopically ordered sections of the motor and
premotor cortex. Words conveying information about the colour
(shown in blue) and shape (shown in orange) of objects are based on
semantic circuits involving different parts of the inferior temporal
stream of object processing.
Results of event-related functional MRI studies (see the figure, part b),
confirm this model of semantic circuits: perceiving colour specifically
activates the anterior parahippocampal gyrus and fusiform gyrus
(shown in blue in the top panel), whereas presentation of matched shape
words sparks activity in the fusiform, middle temporal and dorsolateral
prefrontal cortex63 (shown in orange). The numbers in the images
represent the y-axis coordinates of each slice in Montreal Neurological
Institute (MNI)-standardized brain space. Understanding action-related
words that refer to the face (such as “talk” or “lick”; shown in green), arm
Nature
Reviews
| Neuroscience
(such as “grasp” or “pick”; shown in red) and
leg (such
as “walk”
or
“kick”; shown in purple) activate somatotopic areas in the motor and
premotor cortex (see the image on the right in the lower panel of part
b), which are also active when subjects move these body parts (see the
partly hidden image)79.
Further support for the semantic circuit model comes from studies in
patients. Category-specific action–perception circuits explain the
impairment differences in the recognition of words from specific
semantic categories in patients with semantic dementia. Because this
disease affects the temporal pole and, with further progression of the
disease, the adjacent frontotemporal cortex (as indicated
schematically in the brain diagrams shown in part c of the figure), the
action–perception model predicts that face- and colour-related
semantic circuits, which reach into these areas, will be impaired more
than other semantic networks. The diagram on the left presents the
performance of patients with semantic dementia (red bars) and healthy
control participants (blue bars) in a lexical decision task. In agreement
with the prediction, the patients, who suffer from a severe and general
semantic impairment66, were found to have more pronounced deficits in
processing face- and colour-related words than in processing arm- and
shape-related words120. The consistency between model predictions,
neuroimaging results and neuropsychological deficits suggests an
important role for category-specific action–perception circuits in
semantic processing. Part b (top panel) is reproduced, with permission,
from REF. 63 © (2006) Oxford Journals. Part b (lower panel) is reproduced,
with permission, from REF. 72 © (2004) Cell Press. Histogram in part c is
reproduced, with permission, from REF. 120 © (2009) MIT Press.
356 | MAy 2010 | voluMe 11
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© 2010 Macmillan Publishers Limited. All rights reserved
PersPectives
facilitation of concordant action­related
word types: they responded more quickly
to arm action­related words (for example,
“grasp”) in a lexical decision task when the
hand area was stimulated, whereas stimula­
tion of the leg motor cortex accelerated the
processing of words referring to leg actions
(for example, “walk”)98. Thus, neuron pop­
ulations in motor systems have an effect on
action­related word recognition, and this
effect depends on word meaning. A recent
neuropsychological study found similar
dissociations between fine­grained seman­
tic categories in patients with the pro­
nounced and specific semantic–conceptual
deficit known as semantic dementia (BOX 2).
Together, these results provide further evi­
dence that action–perception circuits are
necessary for, and make an important
contribution to, semantic processing.
Grasping the grammar of actions
The questions that pertain to phonological
and semantic processes can also be applied
to the specifically human linguistic ability to
use and understand a potentially unlimited
set of sentences: is grammar processing, like
the processing of phonology and semantics,
supported by action–perception circuits that
span inferior­frontal and superior­temporal
areas of the cortex? If so, are the action­
related circuits in the inferior­frontal cortex
important for grammatical understanding —
that is, for extracting information from the
syntactic structure of sentences?
neuroimaging research confirms that
Broca’s region (BA 44 or pars opercularis
and BA 45 or pars triangularis) in the infe­
rior frontal cortex and Wernicke’s region in
the superior temporal cortex are key areas of
grammar processing: they are more strongly
active in response to complex sentences than
to simple control sentences, and they are also
strongly active in response to ungrammatical
word strings99–103.
lesion studies have also revealed the
necessary role of Broca’s area and adjacent
perisylvian sites for grammar processing.
Important evidence came from patients with
agrammatism — a grammar processing defi­
cit that is characteristic of Broca’s aphasia104.
Although agrammatism frequently occurs
after lesions in the inferior frontal cortex
including Broca’s area, a systematic study
showed that lesions anywhere in the left
perisylvian cortex can cause this deficit 105.
In addition to deficits in the production
of words and affixes with predominantly
grammatical function and grammatically
correct sentences, the patients typically
show an agrammatical comprehension
Box 3 | Brain mechanisms of syntax — a challenge for neuroscience
How the mechanisms for processing discrete grammatical rules or, alternatively, probabilistic
syntactic regularities, are organized in the brain and how they develop in ontogeny has been studied
with network simulations, but remains a matter of debate121–123. One class of neural network model
extracts information about the combination of string elements from sentences. As the networks did
not seem to develop or use mechanisms that were functionally similar to linguistic rules, researchers
concluded that “no rules operate in the processing of language”124. However, when features of
cortical structure and function (including sequence-sensitive cells, excitatory connections between
neurons in the same area, sparse coding and unsupervised Hebbian learning) were incorporated into
the network, grammar circuits emerged as a consequence of learning. These circuits served
functions similar to rules113, supporting the idea that language processing in neuronal circuits
involves the application of linguistic rules123. The built-in structural features of these networks imply
that some a priori combinatorial knowledge is available at the onset of learning, a claim supported
by differences in brain activation that occur in response to structurally different syllable sequences
in newborn babies125.
The mechanisms underlying grammar and syntax may be domain general, applying to every kind of
action. Indeed, similar to phrases in sentences, basic body acts are joined in action chains to form a
meaningful goal-directed action sequence (drinking from a cup requires grasping, lifting, turning
and so on). Importantly, even very complex types of syntactic structures have an equivalent in other
action domains. The hierarchical structure of embedded or ‘nested’ sentences is paralleled, for
example, in music and bodily interaction111,126, as the following examples illustrate: a centreembedded sentence (“The man {whom the dog chased} ran away”) has the same nested structure as
a standard jazz piece (theme {solos} modified theme) and complex everyday action sequences (open
door {switch on light} close door). In each case, a superordinate sequence surrounds a nested action
or sequence (in the inner parentheses). Because language, music and body action have similar
hierarchical syntactic structures, the principal underlying brain mechanisms might be the same58.
The domain-general role of Broca’s area, especially Brodmann area 44, in the hierarchical structuring
of actions (see the main text) could be derived from its evolutionarily earlier premotor functions in
action control and action recognition. It will be a fruitful target of future research to clarify how
syntactic processes and representations emerge from action–perception circuits and which
properties of the human brain are important for building syntactic circuits127.
deficit: their impairment in understanding
single words is only mild (see the discus­
sion above), but they have great difficulty in
aligning scrambled words into a sentence or
in understanding complex sentences — for
example, passive (but not active) sentences
and object­relative (but not subject­relative)
sentences89,106. The important role of Broca’s
area in understanding the grammar of sen­
tences is paralleled in non­linguistic modali­
ties107. Together with their syntactic deficits,
patients with lesions in the inferior frontal
cortex have difficulty in ordering pictures
into well­known sequences of actions89.
Similar results have been shown in healthy
individuals during temporary inactivation of
Broca’s area by TMS108. The inferior frontal
area also provides a common substrate for
processing grammatical sentences and famil­
iar musical sequences109–111.
In summary, brain activation and lesion
data confirm that Broca’s area in the infe­
rior frontal cortex is active during, and is
necessary for, the production and under­
standing of complex syntactic structures
that are immanent in sequences of body
actions, musical tunes and grammatical
word strings58.
why are inferior frontal cortex and
superior temporal areas important for
nATuRe RevIewS | NeuroscieNce
understanding grammar? we propose that
the brain’s grammar network evolved in
areas in which action–perception circuits
for hand, mouth and articulator actions
were already established — that is, in the
left perisylvian cortex. This includes pre­
motor area BA 44 (REF. 58), which is probably
the human homologue of monkey area F5
(REF. 13). neurons that respond specifically
to sequences of words may also be present
in this area; note that sequence­specific
neurons have been found in a range of ani­
mals (for example, see REF. 112), making it
likely that the same mechanisms operate on
language in humans. neurocomputational
work shows that word sequence processors
are joined together (by learning) into circuits
that provide a basis for higher­level syntactic
structures. These circuits link syntactic cat­
egories (such as articles, nouns and verbs)
to each other 113. even complex types of syn­
tactic structures, such as hierarchical nesting
(BOX 3), might engage word and sequence
processors in the left perisylvian cortex.
Consistent with this conjecture, hearing hier­
archically nested sequences activates the pos­
terior superior temporal cortex together with
the pars opercularis of Broca’s area, which
are linked by the arcuate fascicle114,115. These
results further confirm the important role
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© 2010 Macmillan Publishers Limited. All rights reserved
PersPectives
of the inferior frontal and superior temporal
areas in grammar processing at different
levels. Further deciphering the neuronal wir­
ing that enables the human brain to support
grammar is a major target of future research.
Conclusions
language processing is based on neuronal
circuits that reciprocally connect action
systems of the brain with perceptual cir­
cuits. There is agreement that, in the healthy
brain, the production of phonemes, words
and sentences requires continuous audi­
tory and somatosensory feedback12. Recent
research has answered the complementary
and important question about the functional
contributions of the action system to per­
ception and comprehension. At the level of
speech sound processing, functional changes
in the motor and premotor cortex lead to
phonological deficits in patients, and experi­
mentally activating specific parts of these
brain areas affects the recognition of specific
speech sounds. In the domain of processing
word meaning, the recognition of specific
semantic word categories can be influenced
by magnetic stimulation of the motor system.
In addition, focal brain lesions of fronto­
temporal systems lead to specific deficits
in processing semantic word types that are
consistent with predictions from a model of
category­specific semantic action–perception
circuits. Syntactic processing of sentences,
and also processing the syntax of sequential
actions more generally, requires function­
ality of the perisylvian cortex, especially
inferior frontal areas. These results show the
important contribution of motor systems to
language perception and comprehension at
different levels. They strongly support a new,
more general idea of active perception in
which, for example, ‘listening instead of hear­
ing’ and ‘looking instead of seeing’ are the
cross­modal products of an intention­driven
sensorimotor system laid down in the brain
at the neuronal circuit level.
why should the motor system be
involved in perception if the brain is pro­
vided with exquisite sensory areas? of key
importance to this question are sensori­
motor neurons in the frontocentral cortex:
sensorimotor circuits, established (in this
linguistic context) as a consequence of learn­
ing, provide automatic coupling between
stimulus features and the actions that pro­
duce these sensory features. By way of recur­
rent connections, especially through the
arcuate fascicle, the action circuits feed back
to the auditory cortex, thereby enhancing
the perceptual salience of specific sensory
stimuli. An analogous mechanism probably
forms the basis of visuospatial attention
and the generation of peripersonal space8.
The evidence summarized here shows that
action–perception links are also effective in
language understanding.
These findings have wider implications
for brain theory. In particular, they question
general models of bottom­up sensory
processing that do not acknowledge the
influence of action­related information on
the cognitive perception process. Although
bottom­up models hold true for early stages
of perception1, they do not account for
higher­order perceptual processing and
understanding as it becomes relevant in
cognition, especially language. Crucially,
bottom­up approaches do not explain why
the frontocentral action system has a pro­
found effect on speech sound perception
(FIG. 2), semantic understanding (BOX 2) and
syntactic parsing. Double dissociations
between perceptual and action­related abili­
ties caused by brain lesions are accounted
for by the functional structure of action–
perception circuits (BOX 1). Proposals that
action–perception interactions are optional
or only effective in cases of perceptual chal­
lenge or high attention45, are countered by
observations that the motor system is active
even during attentional distraction from
easy­to­perceive linguistic stimuli116,117. Thus,
action–perception circuits with their sensori­
motor cells, including mirror neurons, offer
a mechanism for language processing and
understanding and for interactive sign
and information processing more generally.
The theoretical framework presented in
this Perspective centres on the neurobio­
logical mechanisms on which language is
based. The empirical evidence for active
perception of language is provided by
Glossary
Motor cortex
Semantics
The portion of the frontal cortex that controls movements
and is therefore classically considered an output area of
the cortex. It includes primary motor, premotor and
supplementary motor areas.
scientific discipline studying the meaning of words and, in
a wider use of the term, meaning in general. The term is
also used as a synonym of ‘meaning’.
Broca’s area
Sensorimotor neuron
A neuron that is activated both by sensory stimulation —
sometimes through various modalities — and during action
execution. Mirror neurons and canonical neurons are
special types of sensorimotor neurons.
The posterior part of the inferior frontal gyrus. It
includes the cytoarchitectonically defined Brodmann
area 44 (BA 44) and BA 45 and is involved in speech
production.
A neuron that activates during action execution and during
the observation of another individual performing a similar
action. some mirror neurons also fire during listening
to action-related sounds.
Syntactic
Relating to the rules of syntax — the grammatical
arrangement of words and phrases in a sentence, which affects
relationships of meaning. For example, changing the
placement of a word or phrase can change the meaning.
A speech sound and smallest unit of speech that can be
used to distinguish between meaningful words in a given
language.
Perisylvian cortex
Neuropsychology
The brain region surrounding the sylvian fissure which,
in the left hemisphere of almost all right-handed people
and in most left-handed people, is most relevant for
language processing. It includes the posterior inferior
frontal cortex, the superior temporal cortex,
inferior parietal areas, the insula and cortico-cortical
fibre bundles.
A scientific discipline studying the effects on behaviour of
changes in neuronal function — caused, for example, by a
brain lesion, magnetic stimulation, drugs or sensory
stimulation.
Phonological
Relating to the scientific discipline of phonology, which
studies the sound structure of languages. The term is also
used to refer to the sound structure of a language itself.
Transcranial magnetic stimulation
A non-invasive method for focal cortical stimulation
by means of a coil positioned on the scalp. It delivers
brief, strong electric pulses. These create a local
magnetic field, which induces a current in the surface
of the cortex that temporarily changes local neural
activity.
Phoneme
Mirror neuron
in representations in adjacent brain regions. Phonological
somatotopy refers to the somatotopic representation of
speech sounds in the motor areas of the articulator that
produced the speech sounds. semantic somatotopy is the
mapping of action-related words to the motor areas
representing the body parts typically involved in executing
the action.
Somatotopy
A property of motor and somatosensory cortices whereby
the spatial organization of adjacent body parts is preserved
358 | MAy 2010 | voluMe 11
Wernicke’s region
The posterior perisylvian cortex, originally identified by the
Polish–German neurologist Carl Wernicke as the area
necessary for speech comprehension. Although definitions
vary, Brodmann area 22 in the superior temporal cortex is
usually included.
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© 2010 Macmillan Publishers Limited. All rights reserved
PersPectives
neurophysiological and neuropsychological
studies and suggests a general model of how
the brain works. The implications of this
framework for linguistic theory are obvi­
ous, as brain correlates of linguistic con­
structs — including phonetic­distinctive
features, semantic categories and syntactic
structures — are related to mechanistic
neuronal circuits, their cortical distribu­
tions, mutual interactions, interdependence
and activation dynamics. we view this new
approach as an integration point at which
linguistic and neuroscience experiment and
theory converge.
Friedemann Pulvermüller is at the Medical Research
Council, Cognition and Brain Sciences Unit, 15 Chaucer
Road, Cambridge, CB2 2EF, UK.
Luciano Fadiga is at the University of Ferrara,
Department of Human Physiology, via Fossato di
Mortara 17/19, 44100 Ferrara, Italy, and the Italian
Institute of Technology, via Morego 30, 16163,
Genova, Italy.
e-mails: friedemann.pulvermuller@mrc-cbu.
cam.ac.uk; [email protected]
doi:10.1038/nrn2811
Published online 9 April 2010
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Acknowledgements
We thank M. Garagnani, I. Laka, R. Wise, R. Moseley and
three anonymous reviewers for their comments on earlier versions of this manuscript. This work is supported by the
Medical Research Council (UK) (U1055.04.003.00001.01)
to F.P., by the Fondazione Cassa di Risparmio di Ferrara to
L.F. and by the European Community (Nestcom (NEST-2005PATH-HUM contract 043,374) to F.P. and Robot-cub, Contact,
Poeticon to L.F.).
Competing interests statement
The authors declare no competing financial interests.
DATABASES
OMiM: http://www.ncbi.nlm.nih.gov/omim
frontotemporal dementia | Parkinson’s disease
FURTHER inFoRMATion
Friedemann Pulvermuller’s homepages:
http://www.mrc-cbu.cam.ac.uk/people/friedemann.pulvermuller; http://www.neuroscience.cam.ac.uk/directory/
profile.php?pulvermuller
Luciano Fadiga’s homepage: http://www.iit.it/en/people.ht
ml?view=profile&layout=profile&id=228
SUppLEMEnTARY inFoRMATion
see online article: s1 (box) | s2 (box)
All liNks Are Active iN the oNliNe pdf
www.nature.com/reviews/neuro
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