J Neurophysiol 96: 2830 –2839, 2006.
doi:10.1152/jn.00628.2006.
Invited Review
Language and the Aging Brain: Patterns of Neural Compensation
Revealed by Functional Brain Imaging
Arthur Wingfield1 and Murray Grossman2
1
Volen National Center for Complex Systems, Brandeis University, Waltham, Massachusetts; and 2Department of Neurology, University of
Pennsylvania School of Medicine, Philadelphia, Pennsylvania
Submitted 16 June 2006; accepted in final form 21 August 2006
INTRODUCTION
In this review we have two goals. One is to present current
views on the neural structures that underlie sentence comprehension when listening to everyday speech. Our second goal is
to suggest why, in spite of age-associated declines in sensory
and cognitive function and microscopic changes in the CNS,
language comprehension typically remains well preserved in
normal aging.
Although varying in detail from one language to another, all
languages of the earth have certain fundamental features in
common. First, all languages have a lexicon. This is a vocabulary keyed to specific concepts such as objects (nouns),
actions (verbs), and modifiers of nouns (adjectives) and verbs
(adverbs). Although many sub-human species can use lexicallike elements to communicate with others of their species,
humans are unique in the power to develop sophisticated
language structures. These structures free us from the here and
now, allowing us to communicate with others of our species in
a highly flexible manner about events, objects, states of mind,
the past and the future. A second universal component of
language accounts for this flexibility. This is a syntax: a system
of rules that specify allowable combinatorial relationships
between lexical elements and the additional cognitive resources we need to implement these rules. This system allows
us to communicate using meaningful sentences to express
complex thoughts and intentions.
Address for reprint requests and other correspondence: A. Wingfield, Volen
National Center for Complex Systems, MS 013, Brandeis University,
Waltham, MA 02454-9110 (E-mail: [email protected]).
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Lesion studies to functional brain imaging
Much of the early research into the brain structures that carry
language was motivated by the desire to understand the loss of
language comprehension or production after stroke or other
sources of brain injury. Such studies attempted to correlate the
site of the lesion with the consequences to language function
and for many years served as the sole means of understanding
brain-language relations. These studies of aphasia (the disruption of language after brain damage) had already by the late
19th century isolated the “language area” in the left cerebral
hemisphere in right-handed (and most left-handed) individuals
(Goodglass and Wingfield 1998).
Within a broad perisylvian region, deficits in language
production were shown to be associated with damage to the
ventral inferior frontal cortex (vIFC; BA 44/45/47), which
includes Broca’s area, and deficits in language comprehension
associated with damage to the posterior lateral temporal cortex
(PLTC; BA 21/22/42), a part of which is commonly referred to
as Wernicke’s area. This early picture was completed by
discovery of a white-matter tract, the arcuate fasciculus, connecting these two regions. The aphasic syndromes of Broca’s
aphasia, Wernicke’s aphasia, and conduction aphasia were thus
neatly accounted for by damage to, or disconnections between,
these centers and pathways (Geschwind 1965, 1969). We show
these three components of the core sentence processing region
colored in blue in Fig. 1, with the arcuate fasciculus represented by the connecting blue double-headed arrow.
Such lesion-based research was significantly enhanced by
technological advances in the development of computerized
axial tomography (CT) and structural magnetic resonance imaging (MRI) that allowed contemporary visualization of lesion
location, freeing investigators from reliance on postmortem
data to study cognitive-cortical correlations. The reliance on
correlations between damaged brain areas and the loss of
particular functions to draw inferences about normal function
in nondamaged individuals, however, remained the same.
The past 10 years have witnessed a dramatic development in
our understanding of brain-language relations. Evidence-based
models of large-scale neural networks can now be constructed
by examining cerebral activation during the performance of
language functions like speaking, reading, and understanding
syntactic relations between the words of a sentence. This was
made possible by the development of positron emission tomography (PET) and functional magnetic resonance imaging
(fMRI), which allow investigators to visualize patterns of brain
activity while a subject is performing a cognitive or linguistic
task.
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Wingfield, Arthur and Murray Grossman. Language and
the aging brain: patterns of neural compensation revealed by
functional brain imaging. J Neurophysiol 96: 2830 –2839, 2006;
doi:10.1152/jn.00628.2006. Human aging brings with it declines in
sensory function, both in vision and in hearing, as well as a general
slowing in a variety of perceptual and cognitive operations. Yet in
spite of these declines, language comprehension typically remains
well preserved in normal aging. We review data from functional
magnetic resonance imaging (fMRI) to describe a two-component
model of sentence comprehension: a core sentence-processing area
located in the perisylvian region of the left cerebral hemisphere and an
associated network of brain regions that support the working memory
and other resources needed for comprehension of long or syntactically
complex sentences. We use this two-component model to describe the
nature of compensatory recruitment of novel brain regions observed
when healthy older adults show the same success at comprehending
sentences as their younger adult counterparts. We suggest that this
plasticity in neural recruitment contributes to the stability of language
comprehension in the aging brain.
Invited Review
LANGUAGE AND THE AGING BRAIN
1.
callosal white matter fibers, especially in anterior brain regions
(Head et al. 2004).
In the review that follows, we first outline the cognitive
changes associated with normal aging and how they constrain
language comprehension and production. We will also recognize the spared abilities that keep language among the best
preserved of cognitive functions in normal aging. Second, we
will draw from neuroimaging studies to describe our current
understanding of the critical regions and large-scale neural
circuits involved in sentence comprehension. Finally, we will
examine current views on how the aging brain recruits neural
resources to support successful comprehension in the face of
sensory-cognitive decline. By examining language comprehension in the aging brain, we address one of the most fundamental questions in current neurobiology: how stable behavior can
be produced in spite of changes in underlying neural structures
and circuit parameters (Prince et al. 2004).
Neuroanatomic model of sentence comprehension.
As we shall see, armed with such techniques it is now also
possible to examine the special challenges of language processing in older adulthood. To be sure, some aspects of
language ability decline as we age, but an equally intriguing
question is how language comprehension remains so relatively
stable even though the older brain undergoes a variety of
neurobiological changes. Notable among these changes are
data from in vivo structural MRI studies that show age-related
reductions in brain volume, especially in frontal and medial
temporal areas (Raz et al. 1997, 2004).
In Fig. 2 we reproduce scatter plots of adjusted brain volume
from four cortical areas (selected from Raz et al. 2004) that
make two important points. The first of these is to demonstrate
that the degree of volumetric decline is not uniform across all
cortical areas. Two areas that show the strongest correlation
between adjusted volume and age are the lateral prefrontal
cortex (top left) and hippocampus (top right). These areas are
important, respectively, for working memory and maintenance
of information for memory consolidation. One can illustrate
the point that volumetric decline is not uniform across the
cortex with two selected areas from Raz et al.’s data that show
quite limited age correlations: inferior parietal cortex (bottom
left) and primary visual cortex (bottom right). These crosssectional data, which are scatter plots of individual subjects,
make the second point, which is the wide variability among
individuals across the age range.
Contrary to earlier notions that this reduced brain volume
reflects significant cell death with normal aging, much of this
volumetric loss may result from reduced synaptic density in
these areas. Of presumed great functional significance are
accompanying regional changes in dendritic morphology, cellular connectivity, and changes in neurotransmitter integrity
(Bannon and Whitty 1997; Wong et al. 1997). Albeit more
subtle in normal aging than in age-related neuropathology such
as Alzheimer’s or Parkinson’s disease, these changes nevertheless have measurable impact on network dynamics that
carry cognitive function (see Burke and Barnes 2006; for a
discussion and review from the human and animal literature).
In addition to these cortical changes, diffusion tensor imaging
(DTI), a new magnetic resonance technique that allows mapping of white matter tracts by imaging the direction of water
diffusion through tissue, shows age-related deterioration of
J Neurophysiol • VOL
Sensory and cognitive constraints on older adults’
language processing
A central feature of normal aging is a general slowing in a
variety of perceptual and cognitive operations (Salthouse
1996). Although there is little loss of word knowledge in all but
the oldest-old (Verhaeghan 2003), word retrieval while speaking becomes slower and more difficult. This can lead to more
frequent occurrences of “tip-of-the-tongue” states, where a
desired word or person’s name is known, but there is difficulty
in its retrieval (Burke et al. 1991).
The issue of age-related slowing takes on special significance in the realm of spoken language comprehension. Speech
rates in everyday conversation range from 140 to 180 words
per minute (wpm). While speech is arriving at this rapid rate,
individual words must be identified and structural relations
between the words must be established (which are the objects,
FIG. 2. Scatter plots of adjusted cortical volumes of 2 areas found by Raz
et al. to show strong correlations with age: lateral prefrontal cortex (top left)
and hippocampus (top right) and 2 sample areas that show reduced correlations: inferior parietal cortex (bottom left) and primary visual cortex (lower
right). The filled circles and solid regression lines show data for women
and the open circles and broken regression lines show the data for men.
[Reproduced from Figs. 4 (page 385), 5 (p. 386), and 6 (p. 387) from Raz
et al. (2004).]
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FIG.
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Invited Review
2832
A. WINGFIELD AND M. GROSSMAN
J Neurophysiol • VOL
(Wingfield and Stine-Morrow 2000). Indeed, in all but latestage Alzheimer’s disease, the formal qualities of speech production (syntactic form, melodic line) and the ability to comprehend at least the surface meaning of speech are maintained
(Kempler 2005).
Until recently the study of compensation in adult aging has
been confined to behavioral studies that have elucidated the
factors that come into play at a descriptive level, such as the
way older adults can effectively use linguistic context to aid
word recognition (Pichora-Fuller et al. 1995; Wingfield et al.
1991) and to use the intonation pattern of speech to help
identify the major clauses, or “thought units,” in a syntactically
complex sentence (Kjelgaard et al. 1999). The development of
neuroimaging techniques has, for the first time, allowed us to
gain insight into how the aging brain compensates for the
abovementioned sensory and cognitive declines in terms of
patterns of upregulation (an increase in brain activity evidenced by increased blood flow) that correspond to the compensatory allocation of neural resources.
Neural recruitment as a mechanism for maintained
language performance
One central question must be how anatomic and physiological changes in the aging brain yield declines in certain aspects
of language function. At the same time, we must also address
the question of how performance is nevertheless typically
maintained at a relatively high level in spite of these demonstrable changes. Functional imaging research has begun to
answer these questions.
The primary technique used in most of the studies we will
describe makes use of blood-oxygen-level-dependent (BOLD)
functional magnetic resonance imaging (fMRI). This technique
is based on the finding that changes in neural activity are
accompanied by alterations in the deoxyhemoglobin concentration of the blood in the region of this activity. The resultant
alteration in the magnetic property of the blood is detected in
the MRI signal and serves as an indicator of increased mental
activity. The brain images shown in such studies represent
subtractions of activity levels during performance of an experimental task against a resting baseline or the activity level
consequent to some other control condition.
A number of imaging studies contrasting performance by
healthy young and older adults have shown a major difference
in observed patterns of neural activation when young and older
adults are asked to perform the same cognitive task. In general,
there is a shift from more focal activation in young adults to
more widespread patterns of activation in older adults (e.g.,
Cabeza 2002; Logan et al. 2002). Such pattern changes in older
adults can include a decrease in neural activation in some brain
regions and increases in others relative to young adults. This
pattern has been observed in a number of cognitive domains,
from encoding pictures (Gutchess et al. 2005) to studies of
episodic memory (Cabeza 2001). At least two hypotheses can
be entertained concerning these age-related differences.
One hypothesis attributes
such pattern differences to reduced cerebral specialization in
the course of the aging process. This can be referred to as the
dedifferentiation hypothesis. This account holds that more
widespread activation seen in older adults is a consequence of
DEDIFFERENTIATION HYPOTHESIS.
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which are the actions, and who is doing what to whom), and
this material must be integrated with what has already been
heard. Processing operations that cannot be accomplished as
the speech is being heard must be conducted on a transient
trace of that speech in memory. It would thus not be surprising
if older adults had more difficulty comprehending and storing
in memory rapid speech than their young adult counterparts.
This turns out to be the case (Gordon-Salant and Fitzgibbons
1997; Wingfield 1996; Wingfield et al. 1999).
The aging process is also typically accompanied by a reduction in the capacity of working memory. This is the ability to
temporarily hold and simultaneously manipulate information
in immediate memory (Baddeley 1996). Understanding who
gave whom the present in the sentence, “Mary who liked
Catherine gave her the present” requires the listener to detect
the overall sentence frame, “Mary gave her the present,” and
the embedded clause, “who liked Catherine,” and to integrate
the two correctly in working memory. As such, working
memory is known to constrain the comprehension of sentences
with complex syntactic structures (see the review in Wingfield
and Stine-Morrow 2000) and also to result in older adults’
avoidance in producing syntactically complex utterances the
organization of which puts a special burden on working memory (Kemper 1992).
Although there is a question of whether all aspects of
language processing are constrained by a single workingmemory resource or by a complex of specialized resources
(e.g., Caplan and Waters 1999), there is no doubt that workingmemory limitations constrain cognition in aging adulthood. As
might be predicted from these two observations, complex
syntax and rapid speech rates operate in a multiplicative
fashion in affecting sentence comprehension with their combined effects being more challenging for older than for younger
adults (Wingfield et al. 2003).
A third feature that affects comprehension of spoken language is the increased incidence of hearing decline among the
aging population. Although many adults retain good hearing
well into old age, some degree of age-related hearing loss
(presbycusis) is not uncommon among older adults. This loss
tends to be differentially greater for the higher sound frequencies that are critical for speech perception (Morrell et al. 1996).
In addition to simple acuity losses due to cochlear hair cell
loss, there can also be higher-level auditory-processing deficits
that leave speech sounding unclear or garbled (phonemic regression), even when it is amplified (Jerger et al. 1989; Schneider and Pichora-Fuller 2000).
Hearing loss may not merely cause the older adult to miss
critical words in a conversation. An additional concern is that
successful perception in the context of poor auditory acuity
may come at the cost of perceptual effort drawing on resources
that might otherwise be available for encoding what has been
heard in memory or for higher-level comprehension operations. That is, even a modest decline in hearing acuity can have
a negative effect on memory and comprehension even when it
can be demonstrated that the words themselves have been
correctly identified (see Wingfield et al. 2005 for data and a
discussion).
In spite of impediments such as these, healthy older adults
communicate with good effectiveness. This is so because
linguistic knowledge, and the procedural rules for implementing this knowledge, remain well preserved in normal aging
Invited Review
LANGUAGE AND THE AGING BRAIN
A diminution of task differentiation in the older brain might have several consequences. The
more widespread activation associated with age-related dedifferentiation could lead to activation of, for example, areas of
frontal cortex the engagement of which compensated for the
decreased specificity in neural activation (Park et al. 2003,
2004). Alternatively, there may be cases where one might
interpret an increase in areas of cortical activation as reflecting
the older brain strategically recruiting additional neural resources to maintain performance at a high level. We will refer
to this alternative as the compensation hypothesis. The compensation hypothesis argues that the additional brain regions
activated during task performance in older adults reflect focused recruitment in a specific anatomic distribution in response to the diminishing cortical resources that are available
as we age. Unilateral activation during cognitive-task performance by young adults, for example, may be supplemented by
recruitment of homologous regions in the contralateral hemisphere in older adults (Cabeza et al. 2002). When performing
tasks that are primarily sensory in nature, older adults show
recruitment of frontal cortex not activated by younger adults
(Cabeza et al. 2004). Because frontal brain regions are associated with executive functions like working memory but not
sensory functions, this would be consistent with older adults
employing higher-level activation to compensate for sensory
decline.
In weighing the evidence for the compensation hypothesis,
the key question is whether increased activation in brain
regions during task performance by older adults that does not
appear when young adults perform the same task necessarily
implies that these additional areas of activation are contributing
meaningfully to successful task performance. This interpretive
question can be met in two ways. One is to use an event-related
imaging design in which one focuses on patterns of cerebral
blood flow only for test trials in which performance has been
successful. This strategy allows imaging in younger and older
adults to be equated for performance accuracy. Another strategy is to contrast patterns of neural activation for older adults
who tend to do well in task performance versus those who do
not. This strategy takes advantage of the wide variation in task
performance in older subjects while equating for age. Both
approaches are represented in the studies to be described.
COMPENSATION HYPOTHESIS.
J Neurophysiol • VOL
A second concern is that age-related physiological functioning may confound the interpretation of observed activations.
These might include changes in the cerebrovascular tree that
can slow transit time or in vascular-neuronal coupling
(D’Esposito et al. 1999). Concerns such as these are addressed
by performing comparable contrasts within groups of healthy
older adults that provide results compatible with the contrasts
of older adults with younger adults.
Anatomic model of sentence processing
Sentence processing offers an important test condition for
examining these hypotheses. This is so because people engage
in sentence processing naturally and with remarkable efficiency, even in healthy aging. This minimizes interpretive
confounds that would be related to performance of unfamiliar
or artificial tasks that may represent an additional source of
difficulty for older relative to younger adults. Sentence processing also allows one to isolate factors of interest in the
stimulus materials, such as demands on working memory, that
can be manipulated experimentally. Finally, because language
processes are understood in such detail, it is possible to
examine the specific sources of compensation that contribute to
age-related cognitive performance.
We will examine these questions from the perspective of a
neural model of sentence processing that hypothesizes two
major dissociable components: the previously noted core sentence processing component that subserves many of the central
or “universal” facets of language that are implicated in sentence processing and an associated large-scale network of brain
regions that supports executive resources such as working
memory deployed as needed to help support sentence comprehension.
Figure 1 illustrates the previously described core sentence
processing network (in blue) built around the ventral inferior
frontal cortex (vIFC, which includes Broca’s area) and the
posterolateral temporal cortex (PLTC, which includes Wernicke’s area) in left peri-Sylvian cortex. As first implied by the
effects of focal brain damage, this core network for sentence
processing has been confirmed and more exactly specified by
neuroimaging studies in healthy adults (e.g., Caplan et al.
2000; Friederici 2002; Luke et al. 2002).
The resource network involves at least several frontal cortical regions and extends to include right hemisphere structures
as well as subcortical structures. The left hemisphere structures
associated with the recruitment of working-memory and executive resources include dorsolateral prefrontal cortex (dlPFC)
and dorsal portion of left inferior frontal cortex (dIFC). Regions in the right hemisphere include PLTC and dIFC. These
regions are shown in red in Fig. 1.
From the perspective of this model, these resources are
recruited to supplement the core sentence-processing network
when working-memory demands are increased in the face of
long and/or syntactically complex sentences. These areas associated with working-memory support are distinct from activation in other areas such as anterior cingulate that respond to
an attentional challenge as imposed by, for example, significantly accelerated speech rate (Peelle et al. 2004). Subcortical
regions may also contribute to comprehension by upregulating
structures such as the striatum during error monitoring when
performing a difficult task.
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cortical regions losing their dedicated contribution to a specialized function. Such a decline in specialization of regional
brain function with age would result in additional brain areas
being activated in the older adult in regions that are often
engaged by a similar kind of task. As a consequence one might
see two cognitive tasks activating distinct but anatomically
related brain regions in young adults, whereas older adults
would show activation of both sets of regions for both tasks.
The appearance of widespread activation when older adults
are confronted with a cognitive task could thus reflect a general
decline in neural efficiency, resulting in the loss of differentiated function that is ordinarily observed when young adults
engage the same activity (Park et al. 2003). A key question
here is whether an observed increase in areas of activity in
older adults helps or hinders task performance. There are
certainly cases where more widespread activation is thought to
interfere with cognitive success (Cabeza 2001; Logan et al.
2002).
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Invited Review
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A. WINGFIELD AND M. GROSSMAN
Modified compensation hypothesis: the interaction of
biological and cognitive factors during sentence
comprehension in adult aging
The compensation model of directed cognitive and neuroanatomic activity during healthy aging was examined in a
series of BOLD fMRI experiments that manipulated a grammatical component and a working-memory component of sentences (Cooke et al. 2002; Grossman et al. 2002a,b). The
premise underlying this work was that although sentence comprehension is fundamentally preserved in the face of an aging
CNS, comprehension can nevertheless suffer, especially when
the sentences contain complex syntax and wording that may
tax working-memory resources.
Consider, for example, a relatively simple active-conjoined
sentence such as “The man insulted the woman and hired a
lawyer.” In this sentence, there are several important thematic
roles: the agent (the man) who performs both actions (insulting
and hiring) and the recipient of the actions (the woman and the
lawyer). A more complex sentence type is one in which the
meaning is expressed with a subject-relative embedded clause,
such as “The man, who insulted the woman, hired a lawyer.” In
this case, the agent and the recipient retain their thematic roles,
but the main clause (The man hired a lawyer) is interrupted by
a relative clause (who insulted the woman). It is possible to
determine who hired the lawyer, but it requires a bit more
cognitive effort.
An even more complex syntactic form is one in which the
meaning is expressed using an object-relative embedded
clause, such as “The woman, who the man insulted, hired a
lawyer.” In object-relative clause sentences, the embedded
clause not only interrupts the main clause, but the head noun
phrase (The woman) functions as both the agent of the main
clause (who hired a lawyer) and the recipient of the relative
clause (who the man insulted). Because the thematic roles in
object-relative clause sentences are not canonical and require more extensive thematic integration, they are more
J Neurophysiol • VOL
difficult to comprehend than subject-relative clause or active-conjoined sentences.
In addition to this purely syntactic manipulation, one can
also independently and orthogonally manipulate demands on
working memory by separating the major elements of the
sentence by either a short three-word adjectival phrase (e.g.,
The woman with blond hair, who insulted the man, hired a
lawyer) or a longer six-word adjectival phrase (e.g., The
woman with blond hair and dark glasses, who insulted the
man, hired a lawyer). Numerous behavioral studies have shown
these factors to have a significant and graded effect on comprehension errors and processing times in young (e.g., Just et
al. 1996) and older (Fallon et al. 2006; Wingfield et al. 2003)
adults.
Grossman et al. (2002a) presented sentences that embodied these principles to young and older adults while the
subjects were in the bore of an MRI scanner. The subjects’
task was simply to answer a probe question about who
performed the action described in the sentence with each of
the sentences randomly including a male or female as the
agent (see Cooke et al. 2002 for the specific stimulus
sentences used and a more detailed account of their features). The behavioral data showed that although on average
sentence-comprehension accuracy was poorer for older
adults relative to young adults, there was much broader
variability in the comprehension performance of the older
adults compared with their younger counterparts. This suggested two groups of comprehenders among these otherwise
healthy elderly adults.
One group of elderly subjects was as accurate as their
younger peers in their sentence comprehension. We refer to
these as the good comprehenders. A second group showed
significantly impaired sentence comprehension relative to the
young adults. These we refer to as the poor comprehenders.
The poor comprehenders were quite similar to the young adults
in comprehending simpler sentences. It was when sentences
were more syntactically complex and especially challenging to
working-memory resources that the poor comprehenders separated themselves from the young adult subjects and the good
comprehender elderly group. As we will describe, Cooke,
Grossman, and their co-workers observed distinct brain activation profiles for the young subjects and for the good and poor
comprehender elderly groups while comprehending easier and
more difficult sentences.
PATTERN FOR GOOD ELDERLY COMPREHENDERS. Consider first
the contrasts of brain activation in young adults versus the
older adults whose comprehension accuracy was relatively
close to that of the young adults. The top two brain renderings
in Fig. 3A were created by subtracting the activation levels
measured in the various brain regions for the good comprehender older adults from the young adults’ activations. Subtracting in this direction shows that the young adults were
producing a significantly greater degree of activation than the
older adults in the posterolateral temporal-parietal cortex in the
left hemisphere. This region is thought to support a short-term
auditory-phonological buffer that retains information transiently during the course of processing (Chein and Fiez 2001;
Jonides et al. 1998). This region also includes the core left
posterior sentence processing component. (These renderings
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This two-component model predicts that in healthy aging the
core sentence-processing network is activated in a relatively
consistent manner to support the generally good quality of
older adults’ sentence comprehension. Evidence for the stability of this core language area comes from sources such as
activation studies of single-word comprehension that show
little age-related change (Madden et al. 1996, 2002; Lustig and
Buckner 2004). The model also predicts that cortical regions
supporting executive resources are upregulated by the older
brain to compensate for declining working-memory resources
during language processing. Such activation would be especially noted in tasks that involve comprehension of complex
sentences. Evidence compatible with this hypothesis comes
from functional imaging studies showing increased activation
in these areas in healthy aging during nonlinguistic workingmemory challenges (Rypma et al. 2001). Compensation may
involve not only a change in the anatomic distribution of
regional brain activity but also a change in the temporal course
during which the activation occurs. Finally, upregulation of
working-memory resources and prolonged activation may be
among the mechanisms that help explain the basis for stable
language functioning in healthy aging despite the microscopic
changes that occur in the aging brain.
Invited Review
LANGUAGE AND THE AGING BRAIN
2835
also illustrate the involvement of a network of cortical areas
upregulated in support of sentence processing beyond the left
perisylvian core sentence-processing area. In particular, the
network upregulates by augmenting working-memory resources needed to support sentence processing.
follow the usual convention of representing larger activation
differences with brighter colors.)
In contrast to this area in which the elderly good comprehenders showed less activation than the young adults
during sentence comprehension, the compensation hypothesis would lead one to expect to see the successful older
adults recruit other brain regions to maintain their successful performance. This contrast can be revealed by subtracting the activation levels in the young adults from the older
adults’ activations. The consequences of this subtraction are
shown in the two brain renderings in Fig. 3B, where one sees
these successful older adults showing significant upregulation in two areas. One of these is increased activity in the
dorsal portion of left inferior frontal cortex. This area is
thought to be important for maintaining and rehearsing
stored verbal information in working memory (Chein and
Fiez 2001; Smith et al. 1998) and is anatomically and
functionally distinct from the ventral portion of left inferior
frontal cortex (Amunts et al. 1999) that appears to be more
strongly associated with grammatical aspects of sentence
processing (Cooke et al. 2002, 2006).
In addition to this increased activation in the left hemisphere, one also sees in Fig. 3B that the successful older adults
showed additional activation in the right posterolateral temporal-parietal region. The young adults also showed increased
activation in this area but only for sentences that especially
stressed working-memory demands (Cooke et al. 2002). For
the older adults, these areas of activation were evident for all
types of sentences.
These findings for the elderly good comprehenders are thus
largely consistent with the compensatory hypothesis in so far
as left dorsal inferior frontal and right temporal-parietal regions
are upregulated to compensate for the reduced left temporalparietal activation they show relative to the young adults. They
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FIG. 3. Regional brain activation contrasts during sentence comprehension
for young adults, elderly good comprehenders, and elderly poor comprehenders. A: areas activated by young adults to a greater degree than the elderly good
comprehenders. B: areas activated by elderly good comprehenders to a greater
degree than young adults. C: areas activated to a greater degree by elderly good
comprehenders than by elderly poor comprehenders. D: areas activated to a
greater degree by elderly poor comprehenders than by elderly good comprehenders. [A and B are reproduced from Fig. 3 (p. 311) in Grossman et al.
(2002a), and C and D are reproduced from Fig. 2 (p. 306) in Grossman et al.
(2002b).]
PATTERN FOR POOR ELDERLY COMPREHENDERS. It is important
to affirm that the activation pattern described in the preceding
text was operating in a compensatory fashion in support the
above older adults’ good comprehension. That this is likely the
case can be seen in Fig. 3, C and D, in which the patterns of
activation of the elderly good and poor comprehenders are
contrasted (Grossman et al. 2002b).
C represents the result of subtracting the activation pattern
observed while the elderly poor comprehenders were engaging
in the sentence-comprehension task from the activation pattern
of the elderly good comprehenders. This subtraction shows that
the poor comprehenders engaged significantly less activation
of the core sentence-processing areas in inferior frontal cortex
and posterior-superior temporal cortex of the left hemisphere
relative to the good comprehenders. It should be noted that the
reduced activation in this area in the poor comprehenders did
not interfere with their comprehension of grammatically simpler sentence forms; as previously noted, their performance
deficit relative to the young adults and the elderly good
comprehenders appeared only when the sentences were more
syntactically complex.
In contrast with this area of reduced activation, subtracting the activation pattern of the poor comprehenders from
that of the good comprehenders, shown in Fig. 3D, revealed
the poor comprehenders to be upregulating dorsolateral
prefrontal cortex to a degree not shown by the good comprehenders. Dorsolateral prefrontal cortex is often activated
during general problem-solving activities, regardless of the
verbal or nonverbal nature of the material (Paulus et al.
2001; Prabhakaran et al. 2001; Ramnani and Owen 2004).
This prefrontal region is not activated in young adults
during sentence-comprehension tasks. This would suggest
that the older adults who are less successful in their comprehension of grammatically complex sentences were attempting to understand these sentences by adopting a general-purpose problem-solving approach to the task.
Adopting this general problem-solving approach may not
hinder comprehension of grammatically simpler sentences because their interpretation is quite straightforward. However,
treating a grammatically complex sentence like any kind of
cognitive challenge that requires planning and mental manipulation, rather than engaging specialized linguistic processes to
understand the specific grammatically determined features of a
complex sentence, appears to undermine comprehension that
depends on complex grammatical processing. These findings
resonate in an interesting way with suggestions that dealing
with complex syntax engages prefrontal cortex, including
vIFC, in controlling selection among competing parsing representations as would be the case when noncanonical sentences
are encountered (Novick et al. 2005).
The findings for the poor comprehending elderly are also
generally consistent with the compensatory hypothesis because, like those for the elderly good comprehenders, they too
illustrate a change in the characteristic brain activation pattern
in response to a cognitive challenge. However, we see here the
Invited Review
2836
A. WINGFIELD AND M. GROSSMAN
FIG. 4. Activation patterns in a late time window for
young adults responding to resource-demanding grammaticality judgments (A and B), and in a late time
window for older adults for simple (C) and more resource-demanding grammaticality judgments (D and E).
A and B are taken from Fig. 3 (p. 22) of Cooke et al.
(2006). C–E are previously unpublished.
Extending the modified compensatory hypothesis: the
temporal course of activation during comprehension of
grammatical features that vary in resource demands
The interaction of biological and cognitive compensation
can be further evidenced by examining sentence processing
with a task that manipulates resource demands in a more subtle
manner. In this study, we assessed executive resources inherent
to more difficult grammatical features of a sentence. This is
based on the seminal electrocortical event-related potential
(ERP) work of Angela Friederici and her colleagues (Friederici
1995; Friederici et al. 2003). Friederici and her co-workers
showed a change in the anatomic distribution of the ERP
depending on the resource demands of the grammatical elements being judged in a sentence. These investigators also
demonstrated changes in the temporal course of processing,
with the ERPs for resource-demanding materials extending
into a later time window than with less demanding sentences.
In a study of young adults, Cooke et al. (2006) pursued
the neuroanatomic substrate and time course associated with
processing three different kinds of grammatical features in a
sentence and the presumed working-memory demands
needed to sustain success. The task was a grammatical
acceptability test in which the subject was required to judge
the coherence of sentences that did or did not contain a
grammatical violation. One feature examined was the inflectional form of the past participle, where in some sentences the morpheme –ed was omitted (e.g., “The test is
being explained/explain to excited new college students.”
(The incorrect form in this and subsequent examples are
given in bold type.) With such sentences one may also add
to the working-memory demands by inserting additional
wording, such as “The test is being vaguely yet slowly
explained/explain to excited new college students.” (The
words used to increase the working-memory resources
needed for the sentences are shown in italics.)
More demanding in terms of working-memory demands
would be acceptability judgments for sentences containing a
noun-verb substitution (e.g., “The dance is being not too
seriously rehearsed/rehearsal prior to the debut perforJ Neurophysiol • VOL
mance.”). The final type of sentence contained a transitivity
violation; a sentence containing a verb that cannot be
expressed in a passive form because the verb is intransitive
(e.g., “The woman is being brazenly and rudely harassed/
winked by the building workers outside.”). Identifying
transitivity violations are thought to involve relatively
prominent working-memory demands relative to the required linguistic operations.
Examination of activation patterns for young adults during correct grammaticality judgments in an early time window showed left inferior frontal recruitment. Whereas lessdemanding judgments activated vIFC, more-demanding
judgments recruited both ventral and dorsal portions of IFC.
More-demanding grammaticality judgments were also associated with right inferior frontal activation during this early
time window (Cooke et al. 2006). Our question was whether
fMRI could be used to look at activation patterns appearing
during a later time window, paralleling the ERP studies of
Friederici and her co-workers. This would allow us to
establish whether the age-related compensatory mechanisms
discussed in the preceding text play out both in terms of
their anatomic distribution and in terms of their temporal
course.
Although temporal resolution of fMRI is poor, we were
nevertheless able to monitor BOLD activity levels 2 s later than
the point at which the BOLD hemodynamic response is typically monitored. The imaging findings seen during this later
time window are illustrated in Fig. 4. For the young adults, the
relatively simple grammaticality judgment with few resource
demands (recognizing -ed violations) resulted in no late activation. By contrast, these young adults showed suprathreshold
activation in the late time window when judging the two more
resource-demanding grammatical features. This is illustrated in
Fig. 4. The activation in the late time window for young
subjects can be seen in A for recognition of noun-verb substitutions and in B for recognizing transitivity violations. In both
cases, the young adults sustained into the later time window
left inferior frontal cortex recruitment. As can be seen, there
was no increased right hemisphere activation relative to the
simpler grammatical judgment. This result for the young adults
is consistent with the ERP findings of Friederici and her
colleagues.
Although the young adults showed activation in the late time
window only for resource-demanding grammatical judgments,
older adults tested with the same sets of materials show a
different pattern. One aspect of this difference appears in Fig.
4C which shows older adults upregulating the ventral portion
of left inferior frontal cortex even for the simpler grammatical
feature in the late time window, activation that appeared for
young adults only with more challenging grammatical judgments. To the extent that this age-specific left hemisphere
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interaction of biological and cognitive factors in a modified
compensatory approach to their sentence processing. This
elderly group appeared to have developed a specific cognitive
strategy during sentence processing in their attempt to compensate for their age-related difficulty. As we saw, this strategy
activated dorsolateral prefrontal cortex, a cortical distribution
normally activated for general-purpose problem-solving but
not typically activated during sentence processing. As we also
saw, however, this cognitive strategy and the associated brain
activation pattern were unfortunately not sufficient to yield
fully successful sentence comprehension.
Invited Review
LANGUAGE AND THE AGING BRAIN
Conclusions
Language comprehension is not unique in showing changing
patterns of neural activation in older adults that compensate for
what we have argued would otherwise be far more dramatic
performance declines. Other cognitive domains, such as working memory, recall from episodic memory, and memorydependent response inhibition, also appear to show compensatory changes in older adults. These other functions, however,
still show markedly poorer levels of behavioral performance in
older adults compared with young adults (e.g., Cabeza et al.
2004; Gutchess et al. 2005; Neilson et al. 2002). Two points
need to be made in this regard. The first is that age differences
in language comprehension do appear when older adults are
faced with rapid speech rates or when challenged by grammatical forms that put considerable pressure on working memory.
Nevertheless, language retains a special place among preserved
functions in normal aging. The question thus remains as to why
compensatory activations are enough to preserve many aspects
of language performance but not enough to preserve equal
levels of performance in these other domains. We have attempted to address this question by suggesting that sufficiently
flexible neural and cognitive resources can conspire to circumvent much age-related change to maintain access to the goal of
communicative efficacy.
This compensation is driven by the fact that language holds
a special place in human interaction. Language emerges early
in childhood, requires no formal training despite its complexity, and is present in every society on earth. Where spoken
language is not possible, sign languages mediated by manual
movements have developed to express objects, actions, and
their syntactic relations. In sum, the human brain is “built” to
do language, it is an activity continuously practiced across the
life span, and no less important, it is carried by a rich network
of brain regions that allow sufficient compensation to operate
at a remarkably good level.
Functional neuroimaging has over recent years brought converging evidence to human brain lesion studies by expanding
the picture beyond just the role of the left perisylvian region for
language processing. This is crucial because it appears that
nontraditional language-related brain areas are upregulated
J Neurophysiol • VOL
during healthy aging to maintain performance in the face of the
neuronal decline that accompanies normal aging.
Beyond confirming the importance of the traditional left
hemisphere language regions centering on Broca’s and Wernicke’s areas and their interconnection, functional imaging
studies conducted in our laboratories and elsewhere have
identified a large-scale neural network that is activated during
the course of sentence processing. We characterize this network in terms of a core perisylvian sentence-processing component together with both left and right hemisphere extrasylvian cortical regions that support the executive and workingmemory resources necessary to process complex sentences.
These studies offer a window on the strategic recruitment of
critical brain regions by older adults in response to otherwise
limited working-memory resources not seen during sentence
comprehension in young adults. We have shown that older
adults augment regional brain activation within the languageprocessing system both spatially and temporally to help compensate for age-related neuronal changes. Moreover, healthy
older adults appear to develop cognitive strategies to help
compensate for the age-related decline in the neuronal substrate for sentence processing. This compensation for agerelated changes in neuronal mass and efficacy of neuronal
transmission addresses in human cognitive function the fundamental question (Prince et al. 2004) of how stable behavior can
be produced in spite of changes in underlying neural structures.
We have attempted to show how the aging brain can maintain a relatively high level of performance despite the biological changes associated with aging. The stability in performance is maintained by engaging novel brain regions in space
and over time and implementing novel cognitive strategies in
response to a constant cognitive goal, in this case, effective
sentence comprehension. This highlights the adaptive and
plastic nature of the neurobiology of brain function that supports optimizing goal attainment with available resources even
when in older adulthood these resources may become diminished.
GRANTS
The authors’ work is supported by National Institutes of Health Grants
AG-04517, AG-19714, and DC-05432 to A. Wingfield and AG-17586, AG15116, NS-35867, and NS-44266 to M. Grossman.
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