Human Language and Our
Reptilian Brain
the subcortical bases of speech,
syntax, and thought
32
FOR THE PAST 200 YEARS, virtually all attempts to account for the neural
bases and the evolution of human language have focused on the neocortex.And
in the past 40 years, linguists adhering to Noam Chomsky’s theories
have essentially equated language with syntax, hypothetically specified by an
innate, genetically transmitted “universal grammar.” In Human Language and our
Reptilian Brain (2000), I attempt to shift the focus. My premise is that speech
is the central element of human linguistic ability and both speech and syntax
are learned skills, based on a neural “functional language system” (FLS). Although
neither the anatomy nor the physiology of the FLS can be specified
with certainty at the present time, converging behavioral and neurobiological
data point to language being regulated by a distributed network that crucially
involves subcortical structures, the basal ganglia, often associated with reptilian
brains though they derive from amphibians.
Like other distributed neural systems that regulate complex behavior, the
architecture of the FLS consists of circuits linking segregated populations of
neurons in structures distributed throughout the brain, cortical and subcortical,
including the traditional “language” areas (Broca’s and Wernicke’s areas) as
well as other neocortical areas.The FLS rapidly integrates sensory information
Department of Anthropology, Brown University, Providence RI 02912-1978.
Email: Philip_Lieberman@brown.edu.
Perspectives in Biology and Medicine, volume 44, number 1 (winter 2001):32–51
© 2001 by The Johns Hopkins University Press
Philip Lieberman
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winter 2001 • volume 44, number 1 33
with stored knowledge; it is a dynamic system, enlisting additional neural resources
in response to task difficulty. Regions of the frontal lobes of the human
neocortex, implicated in abstract reasoning and planning, and other cortical
areas are recruited as task difficulty increases. Since natural selection selects for
timely responses to environmental challenges, it is not surprising that the FLS
also provides direct access to the information coded in a word, i.e., primary
auditory, visual, pragmatic, and motoric information. The mental operations
carried out in the brain are not compartmentalized in the “modules” proposed
by most linguists and many cognitive scientists.The neural bases of human language
are intertwined with other aspects of cognition, motor control, and
emotion.
The human FLS is unique; no other living species possesses the neural
capacity to command spoken language, which serves as a medium for both
communication and thought.The FLS appears, however, to have evolved from
neural structures and systems that regulate adaptive motor behavior in other
animals. In this light, the subcortical basal ganglia structures usually associated
with motor control that are key elements of the FLS reflect its evolutionary
history: natural selection operated on neural mechanisms that yield adaptive—
that is, “cognitive”—motor responses in other species. There is no reason to
believe that the basic operations of the human brain differ for motor control
and language. Insights gained from the study of the neural bases of motor control
apply with equal force to human language; although the neural architecture
that regulates motor control and syntax is part of our innate endowment,
the details are learned.And the early stages of the evolution of the cortico-striatal
neural circuits that regulate human language and thought may have been
shaped by natural selection to meet the demands of upright bipedal locomotion,
the first defining feature of hominid evolution.
This evolutionary perspective may not be familiar to some cognitive scientists,
linguists, and philosophers. I hope, however, that biological linguists
working in an evolutionary framework will lead the way to new insights on
the nature of language. Paraphrasing Dobzhansky,“Nothing in the biology of
language makes sense except in the light of evolution.”
Functional Neural Systems
The traditional view of the neural bases of human language derives from 19thcentury
phrenology. Phrenologists claimed that discrete parts of the brain,
which could be discerned by examining a person’s cranium, were the “seats”
of various aspects of behavior or character. Neo-phrenological theories do not
claim that a bump on your skull shows that you are virtuous, but phrenology
lives on in the traditional Broca-Wernicke model of the neural bases of language.
In 1861, Broca ascribed the word-finding difficulties and speech production
deficits of his patient to damage to a frontal region of neocortex,
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Broca’s area. Shortly after, “receptive” deficits involving comprehension were
ascribed to damage to a posterior area of cortex, Wernicke’s area (Wernicke
1874). Lichtheim’s 1885 model, subsequently reiterated by Geschwind (1970),
claimed that the neural basis of human language was a cortical system linking
Wernicke’s area with Broca’s area. According to this model, Wernicke’s area
processes incoming speech signals; information is transmitted via a cortical
pathway to Broca’s area, which serves as the “expressive” language output
device. The Lichtheim-Geschwind theory is taken by linguists such as
Chomsky (1985) and Pinker (1994) to be a valid model of the neural architecture
underlying human linguistic ability. According to Pinker, “Genuine
language . . . is seated in the cerebral cortex, primarily the left perisylvian
region” (p. 334), and the “the human language areas [comprise]Wernicke’s and
Broca’s areas and a band of fibers connecting the two” (p. 350).
Although the Lichtheim-Geschwind model has the virtue of being simple,
neurophysiological studies show that it is wrong. Different regions of neocortex
are specialized to process particular stimuli, visual or auditory; other
regions participate in regulating motor control or emotion or holding information
in short-term (working) memory, etc. But complex behaviors, such as
looking at and reaching for an object, are regulated by neural circuits that constitute
distributed networks that link activity in many different neuroanatomical
structures.As Mesulam notes,“complex behavior is mapped at the level of
multifocal neural systems rather than specific anatomical sites, giving rise to
brain-behavior relationships that are both localized and distributed” (1990, p.
598). A given neuroanatomical structure typically supports many segregated
neuronal populations that project to different parts of the brain, forming circuits
that regulate different aspects of behavior.
In other words, although specific operations are performed in particular
parts of the brain, a particular behavior is regulated by a network, a “functional
neural system,” that integrates activity in structures distributed throughout the
brain. Studies that relate brain activity to behavior in humans and other species
show that a class of functional neural systems generates timely responses to
environmental challenges and opportunities. These functional neural systems
integrate incoming sensory information with an animal’s knowledge base and
modify or generate goal-directed motor activity that enhances biological fitness.The
postulated human “functional language system” (FLS) regulates language,
the derived feature that sets human beings apart from other living
species.
The FLS is a distributed network that includes basal ganglia structures that
regulate sequencing in seeming unrelated activities such as moving one’s fingers,
talking, comprehending distinctions in meaning conveyed by syntax, and
solving cognitive problems (Cunnington et al. 1995; Grossman et al. 1991,
1993; Lange et al. 1992; Lieberman et al. 1990, 1992; Natsopoulos et al. 1993;
Pickett et al. 1998). Basal ganglia sequence the pattern generators governing
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motor activity and cognitive operations, by means of segregated neuronal populations
that project to neuronal populations in other subcortical structures
and cortical areas throughout the brain.
The FLS and Basal Ganglia:
Cortico-Striatal Circuits
Two sources of evidence are discussed in some detail in Human Language and
our Reptilian Brain. Since only human beings possess an FLS that regulates spoken
language and complex cognitive behavior, it is not possible to employ
highly invasive techniques that might reveal the its neural circuitry or the
computations that are effected in its component neuroanatomical structures.
Since human physiology is manifestly similar to that of other species, however,
valid inferences concerning the human brain can be derived from the study of
the brains of other species. Comparative neurophysiological studies of other
species have revealed many aspects of basal ganglia circuitry and function. In
some instances, comparable studies of human brains are feasible.These studies
clearly show that neural circuits link basal ganglia structures and cerebellum to
prefrontal cortical areas implicated in cognition, as well as to cortical areas
associated with motor control.
Experiments in nature involving human subjects constitute the second line
of inquiry. Studies of the behavioral effects of brain damage resulting from
trauma or disease demonstrate that subcortical structures are essential components
of the FLS. While language often recovers after humans suffer cortical
damage, perhaps reflecting cortical plasticity (Elman et al. 1996), damage to
subcortical circuits results in permanent language deficits (Stuss and Benson
1986). Speech, lexical access, the comprehension of meaning conveyed by sentences,
and various aspects of higher cognition are regulated by parallel circuits
that involve basal ganglia and other subcortical structures, as well as other neocortical
structures.
One of the major findings of clinical studies over the past two decades is that
behavioral changes once attributed to frontal-lobe cortical dysfunction can be
observed in patients having lesions in subcortical basal ganglia. Cummings
(1993) identifies five parallel basal ganglia circuits of the human brain:
a motor circuit originating in the supplementary motor area, an oculomotor
circuit with origins in the frontal eye fields, and three circuits originating in
prefrontal cortex (dorsolateral prefrontal cortex, lateral orbital cortex and anterior
cingulate cortex).The prototypical structure of all circuits is an origin in
the frontal lobes, projection to striatal structures (caudate, putamen, and ventral
striatum), connections from striatum to globus pallidus and substantia nigra,
projections from these two structures to specific thalamic nuclei, and a final
link back to the frontal lobe. (Cummings, 1993, p. 873)
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Representative Experimental Data
The Syntax of Rat Grooming
Most linguists believe that the defining characteristic of human linguistic
ability is syntax, which binds a finite number of words into “well-formed” sentences
that can convey an unbounded set of meanings. Studies of rodents show
that they too make use of a “syntax,” regulated in basal ganglia, to bind individual
movements into “well-formed” grooming programs. The grooming
movements of rats do not convey an unbounded set of meanings, or perhaps
any meaning to other rats. However, experiments performed on rats show that
show that damage to the striatum disrupts the integrity of the sequences of gestures
that normally occur, but does not disrupt the individual gestures that
would make up a grooming sequence. In other words, the “syntax” of grooming
is regulated in the basal ganglia. Damage to other neural structures—prefrontal
cortex, primary or secondary motor cortical areas, or cerebellum—does
not affect the grooming sequence. Electrophysiological data confirm the role
of basal ganglia in regulating the sequence in which these individual movements
(e.g., forelimb strokes versus body licks) occur (Aldridge et al. 1993).
Learned Behavior
Rats raised completely isolated from other rats execute the same grooming
pattern, demonstrating its innate nature.And so it is likely that rodent grooming
patterns are coded by a genetically transmitted “universal grooming grammar,”
analogous to the hypothetical universal grammar that, according to
Chomsky, determines the syntax of all human languages. Although most theoretical
linguists accept some form of Chomsky’s theory, many studies suggest
that human beings learn the particular syntax of the languages that they command
by means of cognitive processes and neural mechanisms similar in manner
and kind to those employed in learning to play a violin, tennis, or even
walking (for reviews, see Elman et al. 1996; Lieberman 1991, 2000). Neurobiological
studies reveal the role of basal ganglia in the acquisition of learned
behavior.
Basal ganglia circuits regulating learned motor tasks appear to be shaped by
associative processes. Kimura, et al. (1993), studied the responses of striatal
interneurons as monkeys learned a classic Pavlovian conditioned motor task—
a sound preceded a task that earned a reward.The data showed that basal ganglia
“coded” the learned response.The independent studies of Graybiel and her
colleagues (1994) confirm these results. Dopamine sensitive striatal interneurons
respond contingent on reward.The striatal architecture noted by Graybiel,
et al. (1994), could carry out both associative Hebbian learning and supervised
learning in a manner similar to current computer-implemented models
of distributed neural networks (Elman et al. 1996). Other independent studies,
in which monkeys learned tasks when they were rewarded with fruit juice,
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confirm the role of reward-based, “appetitive,” activation of midbrain dopamine
sensitive neurons.
Human Finger Sequencing
Techniques that indirectly monitor human basal ganglia activity yield data
consistent with these invasive electrophysiological studies of motor control.
Human basal ganglia circuits regulate sequential, self-paced, manual motor
control tasks. Depleted production of the neurotransmitter dopamine degrades
basal ganglia activity in Parkinson’s disease, largely sparing the cortex (Jellinger
1990).Abnormalities in motor sequencing are one of the signs of Parkinson’s
(Harrington and Haaland 1991). Cunnington and his colleagues (1995) monitored
the activity of the supplementary motor area of the cortex in normal
subjects and in patients with Parkinson’s disease by means of movementrelated
potentials, electrical signals that are emitted before a movement.
Subjects pushed buttons with their index fingers in various experimental conditions;
EEG signals were recorded from the supplementary motor area before
and during each button-push. The button-pushing data reveal basal ganglia
activity similar to that noted by Aldridge and his colleagues (1993) for rats, as
well as studies of spatial sequencing in monkeys that make use of invasive techniques.The
basal ganglia
activate the preparatory phase for the next submovement, thereby switching
between components of a motor sequence. Since the basal ganglia and supplementary
motor area are more involved in temporal rather than spatial aspects
of serial movement, this internal cueing mechanism would coordinate the
switch between motor components at the appropriate time, thus controlling
the timing of submovement initiation. (Cunnington et al. 1995, p. 948)
Stereotaxic Surgery
Studies of the effects of surgery on humans offer another source of data
concerning basal ganglia function.“Stereotaxic” surgical techniques have been
perfected that selectively destroy basal ganglia structures or the targets of circuits
from these structures in thalamus. Thousands of operations were performed
before Levodopa treatment was available to offset the dopamine depletion
that is the immediate cause of Parkinson’s disease. In many instances, these
operations reduced the debilitating rigidity and tremor of patients with
Parkinson’s. Marsden and Obeso (1994) review the outcomes of these surgical
interventions and similar experimental lesions in monkeys. They address the
seeming paradox that surgery that destroys subcortical structures, known to
regulate various aspects of motor control, reduces tremor and rigidity but has
little effect on motor control.As Marsden and Obeso note, the reason appears
to be the distributed parallel nature of the basal ganglia system regulating
motor control:
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Perspectives in Biology and Medicine
Neurons in supplementary motor area, motor cortex, putamen and pallidum,
all exhibit very similar firing characteristics in relation to movement. . . .
Within each of these various motor areas, neuronal populations seem to be
active more or less simultaneously, rather than sequentially.They appear to
cooperate in an overall distributed system controlling the shape of movement
(Marsden and Obeso 1994, p. 886)
Marsden and Obeso suggest that the basal ganglia have two different motor
control functions in human beings:
First, their normal routine activity may promote automatic execution of routine
movement by facilitating the desired cortically driven movements and
suppressing unwanted muscular activity. Secondly, they may be called into play
to interrupt or alter such ongoing action in novel circumstances. . . . Most of
the time they allow and help cortically determined movements to run
smoothly. But on occasions, in special contexts, they respond to unusual
circumstances to reorder the cortical control of movement. (p. 889)
Many studies show that the basal ganglia circuitry implicated in motor control
does not radically differ from that implicated in cognition. Marsden and Obeso
conclude:
the role of the basal ganglia in controlling movement must give insight into
their other functions, particularly if thought is mental movement without
motion. Perhaps the basal ganglia are an elaborate machine, within the overall
frontal lobe distributed system, that allow routine thought and action, but
which responds to new circumstances to allow a change in direction of ideas
and movement. Loss of basal ganglia contribution, such as in Parkinson’s disease,
thus would lead to inflexibility of mental and motor response. . . . (p. 893)
Aphasia
Marsden and Obeso’s conclusions are supported by the studies of aphasia
that have structured theories of mind and brain for more than a century.
Although the most apparent linguistic deficit of the syndrome named for
Broca, “Broca’s aphasia,” is labored, slow, slurred speech, other disruptions to
normal behavior can occur, such as deficits in fine manual motor control and
oral apraxia (Stuss and Benson 1986). Broca’s aphasics often have difficulty
executing either oral or manual sequential motor sequences (Kimura 1993).
Higher-level linguistic and cognitive deficits also occur. The utterances produced
by Broca’s aphasics were traditionally described as “telegraphic.”When
telegrams were a means of communication, the sender paid by the word, and
“unnecessary” words were eliminated; hence the utterances of English-speaking
aphasics who produce messages such as “man eat fish” have a telegraphic
quality.Aphasic telegraphic utterances are often thought to be a compensatory
behavior: aphasic speakers presumably produce short utterances to minimize
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their speech production difficulties. It is evident, however, that Broca’s aphasics
also have difficulty comprehending distinctions in meaning conveyed by
moderately complex syntax. Although agrammatic aphasics are able to judge
whether sentences are grammatical, albeit with high error rates, the comprehension
deficits of Broca’s aphasics have been replicated in many independent
studies (cf Blumstein 1995). Nonlinguistic deficits also occur; Kurt Goldstein
(1948) noted the loss of the “abstract capacity,” deficits in planning and deriving
abstract criteria, and “executive capacity generally associated with frontal
lobe activity.”
Acoustic analyses show that the characteristic speech production deficit of
Broca’s syndrome is impaired sequencing. It is first useful to note the aspects
of speech production that are not impaired in Broca’s aphasia.The production
of the formant frequency patterns that specify vowels and consonants is unimpaired,
though there is increased variability (Ryalls 1986). Since formant frequency
patterns are determined by the configuration of the supralaryngeal
vocal tract (primarily tongue and lip activity) we can conclude that the control
of these structures is unimpaired.The “encoding” or “melding” of formant
frequency patterns (Liberman et al. 1967) which characterizes the production
of human speech is likewise preserved in Broca’s aphasia.
Speech Encoding
A short digression on the nature and selective advantage of speech encoding
is perhaps germane. Speech encoding is one of the keys to human linguistic
ability. It allows us to communicate rapidly, transcending the limits of the
human auditory system and the bounds of short-term auditory memory. As
the supralaryngeal vocal tract configuration gradually changes, so do the formant
frequencies. The result is an acoustic melding of the formant patterns
that specify individual sounds into syllable-sized units (Liberman et al. 1967).
For example, it is impossible to produce the isolated sound [b] without also
producing a vowel or “continuant” such as [ba] or [bs].The formant frequency
transitions specify the initial consonant as well as the vowel—consonant and
vowel are fused into a syllable.This process yields the high-information transfer
rate of human speech: the encoded syllables are transmitted at a rate that
does not exceed the fusion frequency of the auditory system, and listeners then
resolve the encoded syllables into the phonetic code. The process yields a
transmission rate of 20 to 30 phonetic units per second, exceeding the fusion
frequency of the human auditory system. If we were forced to communicate
at the slow syllabic rate, we would forget the beginning of a complex sentence
before we heard its end.
The encoding process involves two factors. Inertial “coarticulation” effects
inherently encode the formant frequency pattern. For example, when producing
the sound [t] of the syllable [ta], the tongue blade initially must be in contact
with the palate.The tongue can not move instantly away from the palate
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Perspectives in Biology and Medicine
to the lower position necessary for [a]. Consequently, the formant frequency
pattern gradually changes as the tongue moves from its syllable-initial position
to the [a] position. A similar effect holds for the syllable [tu] except that the
consonant “transition” flows into the formant frequency pattern of the vowel
[u]. However, inertia cannot account for “anticipatory” coarticulation. Human
speakers plan ahead as they talk, anticipating sounds that will occur. Speakers,
for example, round their lips (move their lips forward and towards each other)
at the very start of the syllable [tu], anticipating the vowel [u].They do not do
this when they produce [ti], because the vowel [i] is produced without liprounding.
(It is easy to see this effect if you look into a mirror and say tea and
to.) The time course for anticipatory planning varies from one language to
another; children learn to produce these encoded articulatory gestures in the
first few years of life. Acoustic analyses of anticipatory—i.e., planned—coarticulation
in aphasics shows that Wernicke’s aphasics cannot be differentiated
from normal controls (Katz 1988). Broca’s aphasics, though they vary in the
degree to which anticipatory coarticulation occurs, do not differ markedly
from normal controls.
Voice-Onset-Time
The major speech production deficit of Broca’s syndrome involves sequencing.
Aphasic subjects lose control of the sequencing between larynx and
supralaryngeal vocal tract activity.The acoustic cue that differentiates stop consonants
such as [b] from [p] in the words bat and pat is “voice-onset-time”
(VOT), the interval between the burst of sound that occurs when a speaker’s
lips open and the onset of periodic phonation produced by the larynx. The
sequence between laryngeal phonation and the burst must be regulated to
within 20 msec. Broca’s aphasics are unable to maintain motor sequencing
control; their intended [b]s may be heard as [p]s, [t]s as [d]s, and so on. Despite
this deficit, however, the intrinsic duration of vowels is unimpaired in Broca’s
aphasia.
Prefrontal Activity and Aphasia
Although aphasia is by definition a language disorder, cognitive deficits
were noted in early studies. Kurt Goldstein, a leading figure in aphasia
research, stressed loss of the “abstract” attitude (1948). Goldstein described the
difficulties that aphasic patients had planning activities and strategies, shifting
strategies, formulating abstract categories, and thinking symbolically. Subsequent
research has found that these cognitive deficits are associated with
impaired frontal lobe—particularly prefrontal—cortical activity (Stuss and
Benson 1986). But frontal lobe cognitive deficits do not necessarily result from
damage to frontal lobe structures. Studies employing positron emission tomography
(PET) and CT scans show that damage to either prefrontal cortex, or to
subcortical structures supporting circuits to prefrontal cortex, can yield frontal
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lobe cognitive deficits. Metter, et al. (1989), found that all of their Broca’s
patients had subcortical damage to the internal capsule and parts of the basal
ganglia. PET scans showed that these patients had vastly reduced metabolic
activity in the left prefrontal cortex and Broca’s region.
The Subcortical Locus of Aphasia
Marie (1926) claimed that subcortical lesions were implicated in the deficits
of aphasia.This was reasonable,since the middle cerebral artery is the blood vessel
most susceptible to thrombotic or embolic occlusion.The central branches
of this artery supply the putamen, caudate nucleus, and globus pallidus.
Moreover, one of the central branches of this artery is the thin-walled lenticulostriate
artery,which is exceedingly vulnerable to rupture.Brain imaging techniques
confirm Marie’s position: absent subcortical damage, permanent aphasia
does not occur.As Stuss and Benson note in their review of studies of aphasia,
damage to “the Broca area alone or to its immediate surroundings . . . is insufficient
to produce the full syndrome of Broca’s aphasia. . . .The full, permanent
syndrome (big Broca) invariably indicates larger dominant hemisphere destruction
. . . deep into the insula and adjacent white matter and possibly including
basal ganglia” (1986, p. 161). Moreover, subcortical damage that leaves Broca’s
area intact can result in Broca-like speech production deficits (e.g., Alexander
et al. 1987; Mega and Alexander 1994). Damage to the internal capsule (the
nerve fibers that connect neocortex to subcortical structures), the putamen, and
the caudate nucleus can yield impaired speech production and agrammatism
similar to that of the classic aphasias, as well in addition to other cognitive
deficits.Alexander and his colleagues (1987) reviewed l9 cases of aphasia resulting
from lesions in these subcortical structures.Language impairments occurred
that ranged from fairly mild disorders in the patient’s ability to recall words, to
“global aphasia,” in which the patient produced very limited nonpropositional
speech. In general, the severest language deficits occurred in patients who had
suffered the most extensive subcortical brain damage.The locus for the brain
damage traditionally associated with Wernicke’s syndrome includes the posterior
region of the left temporal gyrus (Wernicke’s area), but often extends to
the supramarginal and angular gyrus, again with damage to subcortical white
matter below (Damasio 1991). Indeed, recent data indicate that premorbid linguistic
capability can be recovered after complete destruction ofWernicke’s area
(Lieberman 2000).As D’Esposito and Alexander (1995) conclude in their study
of aphasia deriving from subcortical damage, it is apparent “That a purely cortical
lesion—even a macroscopic one—can produce Broca’s or Wernicke’s aphasia
has never been demonstrated” (p. 41).
Neuro-Degenerative Diseases
Studies of the behavioral consequences of diseases such as Parkinson’s disease
and progressive supranuclear palsy provide independent evidence for the
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role of basal ganglia in the FLS. These neuro-degenerative diseases result in
major damage to basal ganglia, mostly sparing the cortex until the late stages,
when cortical receptors may become damaged (Jellinger 1990).The primary
deficits of these diseases are motoric: tremors, rigidity, and repeated movement
patterns occur. However, subcortical diseases also cause linguistic and cognitive
deficits. In extreme form, these subcortical diseases result in a dementia
(Albert et al. 1974).
Sentence comprehension deficits linked to syntax have been noted in several
Parkinson’s studies (Grossman et al. 1991, 1993; Lieberman et al. 1990,
1992; Natsopoulos et al. 1993). Illes, et al. (1988), found that the sentences produced
by Parkinson’s subjects are often short and have simplified syntax. Illes
and her colleagues attributed these effects to the speakers’ compensating for
speech production difficulties. However, a subsequent study revealed sentence
comprehension deficits in Parkinson’s disease that could not be attributed to
compensatory strategies (Lieberman et al. 1990). In this study, based on a sentence
comprehension test designed for hearing-impaired children, the subjects
simply had to utter the number (one, two, or three) that identified a line drawing
that best represented the meaning of the sentence that they heard. Nine of
a sample of 40 non-demented Parkinson’s subjects showed comprehension
deficits. Because the vocabulary of the test is simple and can be comprehended
by six-year-old hearing children, the results argue against the subjects having
had any difficulties with vocabulary. Cognitive loss was associated with
impaired sentence comprehension; the subjects who had sentence comprehension
deficits showed no symptoms of Alzheimer’s disease, but cognitive
decline was apparent to the neurologist who had observed them over a period
of time.
Verbal Working Memory
The sentence comprehension deficits of Broca’s aphasia and Parkinson’s disease
appear to reflect impairment of processing in verbal “working memory.”
The concept of working memory derives from about 100 years of research on
short-term memory. Short-term memory is usually thought of as a buffer in
which information is briefly stored; working memory includes computation as
well as storage. Baddeley and his colleagues (e.g., Gathercole and Baddeley
1993) showed that verbal working memory was implicated in both the storage
of verbal material and the comprehension of sentences. Baddeley proposed
that verbal working memory involves two components, an “articulatory loop”
whereby subjects maintained speech sounds in working memory by subvocally
rehearsing them using the brain mechanisms that regulate overt speech, and a
“central executive” process.
The central role that speech plays in the human FLS is manifest in the
“rehearsal” mechanism, whereby words are subvocally maintained in working
memory using the neuroanatomical structures that regulate speech produc-
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tion. Many experiments show that subjects have more difficulty recalling a
series of longer words than shorter words, as might be predicted if the articulatory
buffer had a finite capacity. When the presumed articulatory rehearsal
mechanism is disrupted by having subjects vocalize extraneous interfering
words (e.g., the numbers one, two, three) during the recall period, recall deteriorates
dramatically.Verbal working memory appears to be an integral component—perhaps
the key component—of the human functional language system,
coupling speech perception, production, semantics, and syntax.
The sentence comprehension test used by Lieberman, et al. (1990, 1992),
included sentences with syntactic constructions that are known to place different
processing demands on verbal working memory in neurologically intact
adult subjects: e.g., “center embedded” sentences, such as “The boy who was
fat sat down”; “right-branching” relative clause sentences, such as “I saw the
boy who is fat”; conjunctions, like “The boy swam and the girl rowed”; and
“simple” declarative sentences, like “I saw the boy.” Some of the sentences,
such as “The apple was eaten by the boy,” were semantically constrained
(apples generally do not eat anything); others, such as “The boy was kissed by
the girl,” were semantically unconstrained.Whereas neurologically intact control
subjects make virtually no errors when they take this test battery, the overall
error rate was 30 percent for some Parkinson’s subjects.The subjects’ comprehension
errors typically involved repeated errors on particular syntactic
constructions. Therefore, their syntax comprehension errors could not be
attributed to general cognitive decline or attention deficits.The highest number
of errors (40 percent) were made on “left branching” sentences—such as
“Because it was raining, the girl played in the house”—that departed from the
canonical English form of subject-verb-object.Thirty percent errors occurred
for right branching sentences with final relative clauses, such as “Mother
picked up the baby who is crying.”Twenty percent error rates also occurred
on long conjoined simple sentences, such as “Mother cooked the food and the
girl set the table.”This again points to verbal working memory load being a
factor in sentence comprehension; longer sentences place increased demands
on verbal working memory.
Similar sentence comprehension error rates for non-demented Parkinson’s
disease subjects have been found in the independent studies of Grossman, et
al. (1991, 1993), Natsopoulos, et al. (1993), and by Pickett, et al. (1998), for a
subject having brain damage limited to basal ganglia. Grossman, et al. (1991),
also tested Parkinson’s subjects’ ability to copy unfamiliar sequential manual
motor movements, a procedure analogous to that used by Kimura (1993), who
found these deficits in Broca’s aphasia. The Parkinson’s subjects’ manual
sequencing and sentence comprehension deficits were correlated, and the correlation
is consistent with Broca’s area playing a role in manual motor control
and in verbal working memory through circuits supported by basal ganglia
(Lieberman 1984; Marsden and Obeso 1994; Rizzolatti and Arbib 1998).
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Perspectives in Biology and Medicine
Sequencing Deficits in Speech, Syntax, and Cognition
Lieberman, et al. (1992), reported striking similarities between the pattern
of deficits in Parkinson’s disease and Broca’s aphasia.Acoustic analysis showed
a breakdown in nine subjects’ VOT control, similar in nature to Broca’s aphasia.The
speech of the Parkinson’s disease subjects was similar to that of Broca’s
aphasics in other ways: they produced appropriate formant frequency patterns
and preserved the vowel length distinctions that signal voicing for stop consonants
when they occur after vowels. The Parkinson’s subjects who had VOT
overlaps had significantly higher syntax error rates and longer response times
on tests of sentence comprehension than did the VOT non-overlap subjects;
moreover, the number ofVOT timing errors and number of syntax errors were
highly correlated.
VOT Deficits: Sequencing or Laryngeal Control?
Impaired laryngeal control, perceptually characterized as hoarse “dysarthric”
speech, and low amplitude speech, or “hypophonia,” is a sign of Parkinson’s
disease.Therefore, it would be reasonable to suppose that impaired laryngeal
control, in itself, might be the root cause of the VOT deficits of
Parkinson’s disease.A study of Chinese-speaking Parkinson’s subjects resolved
this question (Lieberman and Tseng 1994). Chinese makes use of phonemic
tones, controlled variations in the fundamental frequency of phonation (F0),
to differentiate words.The syllable [ma] produced with a level F0 contour in
Mandarin Chinese, for example, signifies mother, whereas it signifies hemp
when produced with a rising F0 contour.Twenty Parkinson’s disease subjects
read both isolated words and complete sentences in test sessions before or
shortly after they took medication that increased dopamine levels.VOT overlap
for Parkinson’s subjects was significantly greater than that of age-matched
speaking normal controls for both the pre-medication and post-medication
test sessions. ButVOT overlap decreased significantly post-medication for half
of the Parkinson’s subjects, demonstrating that dopamine-sensitive subcortical
circuits were implicated in sequencing the laryngeal and supralaryngeal vocal
tract motor commands that yield VOT distinctions. Acoustic analysis showed
that the Parkinson’s subjects were always able to generate the controlled F0
patterns that specify Chinese phonemic tones. Since the F0 patterns that specify
these phonemic tones are generated by precise laryngeal maneuvers, it is
apparent that that sequencing deficits are responsible for the observed VOT
overlaps.
In short, the VOT overlaps that can occur in Parkinson’s disease appear to
reflect degraded sequencing of the individual motor commands that constitute
the motor “program” that generates speech.This is not surprising, in light of
studies of sequential non-speech motor activity in Parkinson’s disease (Cunnington
et al. 1995; Marsden and Obeso 1994) and the sequencing of sub-
Human Language and Our Reptilian Brain
winter 2001 • volume 44, number 1 45
movements of rodent grooming noted by Aldridge, et al. (1993). If the human
neural circuitry regulating voluntary laryngeal activity during speech production
is similar to that of monkeys, then the locus of VOT sequencing deficits
may be the coordination of a laryngeal circuit involving anterior cingulate
gyrus and independent circuits involving neocortical areas that regulate
supralaryngeal vocal tract maneuvers. Significantly, no neocortical areas appear
to be implicated in the regulation of non-human primate vocalizations (Sutton
and Jurgens 1988).
Discussions of other experimental data consistent with basal ganglia regulating
and shifting sequential motor and cognitive acts await the reader of Human
Language and our Reptilian Brain. Hypoxia on Mount Everest impairs both
VOT and sentence comprehension (Lieberman et al. 1994, 1995). Pickett, et
al. (1998), in a study of a subject having brain damage limited to basal ganglia,
found speech motor-sequencing deficits as well as deficits involving sequencing
in the comprehension of distinctions in meaning conveyed by syntax and
in cognitive tasks.Vargha Khadem, et al. (1998), documented speech and language
deficits in subjects having a genetically transmitted anomaly that results
in bilateral reduction of caudate nucleus volume. Cognitive deficits similar to
those occurring with frontal lobe damage can be traced to impaired basal ganglia
activity in Parkinson’s disease (Lange et al. 1992). Cerebellar damage also
yields similar deficits (Pickett 1998). In short, subcortical structures are essential
elements of the FLS that regulate human language and some aspects of
cognition.
On the Evolution of Adaptive Behavior
Despite strident claims to the contrary (e.g., Pinker 1994), chimpanzees can
produce about 150 words using manual sign language or computer keyboards,
roughly equivalent to the abilities of two-year-old children. Chimpanzees also
can understand spoken English words (Gardner and Gardner 1984; Gardner et
al. 1989; Savage-Rumbaugh and Rumbaugh 1993). Indeed, other species
comprehend spoken words.Your dog almost always comprehends a few words.
The celebrated circus dog Fellow understood at least 50 words (Warden and
Warner 1928).Therefore, lexical ability dissociated from speech production is
a primitive feature of language that undoubtedly existed in the ancestral
species that was the common ancestor of human beings and apes, and all
archaic hominid lineages. Syntactic ability, which was and still is taken by many
linguists to be a unique human attribute (Calvin and Bickerton, 2000; Lieberman
1984, 1991), also is present to a limited degree in chimpanzees. Analyses
of the American Sign Language communications of the Project Washoe chimpanzees
show that they used two-sign combinations and some three-sign combinations.
Savage-Rumbaugh, et al. (1986), show that the six-year-old pygmy
chimpanzee Kanzi comprehends simple sentences having the canonical
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Philip Lieberman
Perspectives in Biology and Medicine
English form in which the subject precedes the object.When he heard sentences
like “Put the pine needles on the ball” or “Put the ball on the pine needles,”
Kanzi responded correctly to the English-language command about 75
percent of the time, demonstrating a sensitivity to basic word order in English.
But chimpanzees cannot talk—speech remains the unique, derived, feature
of human language. Despite many attempts over the past 300 years, no one has
been able to train a chimpanzee to talk.The supralaryngeal vocal tract anatomy
of chimpanzees prevents them from producing the vowels such as [i] and [u]
(the vowels of the words see and do). However, speech communication could
take place without the capability of producing the vowel [i], albeit with
increased error rates (cf Lieberman 1984, 1991, 2000); analyses of chimpanzee
vocalizations and the capabilities of their vocal tracts show that they could
speak producing bilabial and alveolar-dental consonants like [b], [p], [m], [t],
[d], [s], and so on, and all vowels save [i], [u], and [a] (Lieberman 1968, 1984).
But chimpanzees can not even freely permute the sounds that occur in their
natural repertoire of calls. The limiting factor is the chimpanzee brain.
Chimpanzees can not produce vocalizations that are not “bound” to specific
emotional states. As Goodall (1986) notes, “Chimpanzee vocalizations are
closely bound to emotion. The production of a sound in the absence of the
appropriate emotional state seems to be an almost impossible task for a chimpanzee”
(p. 125). Human beings are able to freely permute the motor commands,
the sub-movements that constitute the sounds of human speech to
form words. The utter lack of productive speech and limited cognitive and
syntactic abilities of apes and other species may reflect basal ganglia circuitry.
Human Language and our Reptilian Brain suggests that our ability to “unbind”
the articulatory submovements that generate words and to produce a virtually
unlimited number of new words that convey referential information derives
from the cortico-striatal circuits that are the focus of this inquiry.
The Antiquity of Hominid Speech
The probable absence of a modern human vocal tract in Neanderthals, and its
almost certain absence in Australopithecines and Erectus grad hominids (Lieberman
1984), does not signify the absence of speech.As the initial Lieberman
and Crelin (1971) paper on Neanderthal speech capabilities stressed, Neanderthals
undoubtedly possessed speech, albeit less efficient speech than modern
humans.This conclusion follows from the logic of natural selection.The perceptual
process that relates formant frequency patterns to particular speech
sounds must take account of the length of a speaker’s vocal tract (longer vocal
tracts produce lower formant frequencies for the same speech sound than
shorter vocal tracts).The vowel [i] (the vowel of see) is optimal for this process
(Nearey 1979), and it makes the process of speech perception less susceptible
to error. However, the human vocal tract increases the risk of choking to death
Human Language and Our Reptilian Brain
winter 2001 • volume 44, number 1 47
when we swallow solid food (noted by Charles Darwin) and has other negative
consequences (increased risk of death due to impacted teeth and less efficient
chewing). But the restructuring of the hominid vocal tract to enhance
the speech perception would not have contributed to biological fitness unless
speech and language were already present in the hominid species ancestral to
modern Homo sapiens. Otherwise there would have been no reason for the
retention of the lower laryngeal position of the human vocal tract.Therefore,
speech and some form of language (including syntactic ability, present in rudimentary
form in living apes) must already have been present in Neanderthals
and in the common ancestors of Neanderthals and modern humans, Homo
erectus and perhaps Australopithecines.
Indeed, some aspects of human speech are very primitive in an evolutionary
sense.The neural processing that allows us to determine the length of the
vocal tract of the person to whom we are listening is not a unique human trait;
studies of monkeys suggest that they also can judge the length of another
monkey’s vocal tract, which is a good index of a monkey’s size, using a similar
process (Fitch 1997). Early hominids must have possessed this ability. Primate
calls also can be differentiated through formant frequency patterns generated
when monkeys or apes close or open their lips as they phonate (Lieberman
1968).The fundamental frequency of phonation (F0), which is determined by
laryngeal muscles and alveolar (lung) air pressure, is one of the principal cues
that signals the end of a sentence and major syntactic units. Most human languages
make use of controlled variations of F0 to produce tones that differentiate
words. Since apes possess laryngeal anatomy that can generate F0 contours,
early hominids must have had this ability. In other words, the roots of
speech communication may extend back to the earliest phases of hominid
evolution.
Walking and Basal Ganglia
About 5 million years ago, a species lived that was the common ancestor of
present-day apes and humans. Early hominid fossils, such as the 4.4-millionyear-old
Ardipithecus ramidus, resemble apes who could have walked upright
(White et al. 1994). Upright bipedal locomotion may have been the preadaptive
factor that selected for neural mechanisms that enhanced motor ability
(Hochstadt 1999). It is apparent that human beings learn to walk.The walking
reflex that exists in newborn human infants appears to be controlled by a
quadripedal neural pattern generator that reflects our hominoid ancestry. We
crawl and toddle before we are able to walk or run. Heel strike, which marks
efficient bipedal locomotion, takes years to develop (Thelen 1984).The subcortical
basal ganglia structures of the FLS also regulate upright, bipedal locomotion.
Indeed, one of the primary signs of Parkinson’s disease, in which basal
ganglia circuits are degraded, is impaired locomotion. Thus, upright, bipedal
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Philip Lieberman
Perspectives in Biology and Medicine
locomotion may have been the initial selective force for the enhancement of
the subcortical-cortical circuits that regulate sequencing of both motor and
cognitive acts.
Many topics that are discussed in Human Language and our Reptilian Brain can
not be treated in this summary. The dopamine depletion that characterizes
Parkinson’s disease may also directly reduce verbal working memory span.
Research in progress suggests that this effect can occur, independent of
sequencing deficits. Studies of the neural bases of motor control also show that
complex behaviors are generally learned rather than innate. Given the participation
of neuroanatomical structures in both motor control and syntactic processing,
it is likely that syntax is learned rather than specified by a Chomskian
universal grammar. It is also clear that algorithmic descriptions of motor
behavior are at best a metaphor: the neural activity that governs motor control
is parallel and distributed. In short, the cumbersome and inadequate algorithmic
descriptions and innate universal grammar specifying the “rules” of syntax
proposed by Chomsky and his disciples are not plausible. Hopefully, the issues
discussed in Human Language and our Reptilian Brain will bring to linguistics and
cognitive science a better appreciation of some of the facts and principles of
biology, leading to a better understanding of what makes us human.
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