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Journal of Geriatric Psychiatry and Neurology

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Contemporary Review 2009: Cognitive Aging


Lauren L. Drag and Linas A. Bieliauskas
J Geriatr Psychiatry Neurol 2010 23: 75 originally published online 25 January 2010
DOI: 10.1177/0891988709358590

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Journal of Geriatric Psychiatry
and Neurology
Contemporary Review 2009: Cognitive Aging 23(2) 75-93
ª The Author(s) 2010
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DOI: 10.1177/0891988709358590
http://jgpn.sagepub.com
Lauren L. Drag, MA, PhD,1 and Linas A. Bieliauskas, MS, PhD1

Abstract
This article addresses key topics in cognitive aging, intending to provide the reader with a brief overview of the current state of
research in this growing, multidisciplinary field. A summary of the physiological changes in the aging brain is provided as well as a
review of variables that influence cognitive abilities in older age. Normal aging differentially affects various aspects of cognition, and
specific changes within various domains such as attention, executive functioning, and memory are discussed. Various theories have
been proposed to account for the cognitive changes that accompany normal aging, and a brief examination of these theories is
presented in the context of these domain-specific changes.

Keywords
aging, cognition, neuropsychology

Received June 5, 2009. Received revised October 27, 2009. Accepted for publication November 18, 2009.

When our 80-year-old grandmother spends 20 minutes looking Aside from the frontal lobes, the hippocampus is another
for the eyeglasses perched on top of her head, we chuckle and well-studied region that shows structural changes in normal
chalk it up to normal aging. However, at what point should we aging.7 Although the extent of neuronal loss in this region has
start being concerned about age-related cognitive changes? been debated, it is commonly accepted that hippocampal atro-
Intact cognitive abilities are needed to carry out everyday activ- phy accompanies normal aging but is less than that seen with
ities, such as managing the finances, remembering to take med- Alzheimer disease (AD). The hippocampus is involved in
ications, driving in unfamiliar environments, remembering a memory processes, and cross-sectional studies have associated
grandchild’s birthday, and learning to use a new computer. hippocampal atrophy with memory loss in normal aging.8-10 In
As the proportion of adults older than 60 years of age is pro- addition, a longitudinal study by Persson et al11 demonstrated
jected to reach unprecedented numbers in the near future and that hippocampal volume loss over time is associated with
lifetime expectancy has risen to more than 80 years, it has decreased memory performance even in healthy older adults.
become increasingly important to better understand the cogni- Compared to the hippocampus, the surrounding entorhinal cor-
tive changes that accompany normal aging. tex, an area targeted by early AD pathology, remains relatively
unaffected by the normal aging process.7
These brain volume changes are not linear across the life
Biological Changes span, as brain volume changes are minimal in younger and
middle-aged adults.12 The rate of age-related volume decline
Normal aging is accompanied by many physiological changes accelerates with increasing age. For example, ventricular
in the brain, both structurally and functionally. Structurally, the expansion, a latent measure of brain atrophy,7 occurs at an
aging brain declines in volume, although not uniformly across annual rate of 0.43% in young adults but increases to 4.25%
regions. The frontal cortex is most affected, declining at faster after the age of 70.
rates than temporal, parietal, or occipital cortices.1,2 Studies Beyond these structural changes, the cerebrovascular
using diffusion tensor imaging have shown that age-related system also changes over time. Normal aging is accompanied
changes in white matter integrity are greatest in anterior
regions,3,4 and it has been suggested that the myelinated fibers
in this region are more susceptible to breakdown, which may
be a contributing factor to age-related frontal pathology.5 1
Department of Psychiatry, University of Michigan Health System, Ann Arbor,
Volume-based imaging studies have also shown that age- MI, USA
related decline in gray matter is also greatest in frontal
Corresponding Author:
regions.6 This preferential involvement of the frontal lobes has Linas A. Bieliauskas, 2101 Commonwealth Blvd, Ste C,
a significant impact on cognitive processes supported by this Ann Arbor, MI 48105, USA.
region, as discussed in later sections. Email: linas@umich.edu

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76 Journal of Geriatric Psychiatry and Neurology 23(2)

by decreases in resting blood flow, the metabolic rate of


oxygen consumption, and the vascular reactivity of cerebral Probability of neuronal activation in
vessels to various chemical modulators.13 There are also response to a specific stimulus in
changes in functional blood flow as evidenced by neuroima- younger adults
ging studies. One finding is that older adults tend to show 100
increased bilateral prefrontal activation compared to younger

Probability of activation
adults when completing the same task, leading to decreased
lateralization of function. Based on these findings, the hemi-
spheric asymmetry reduction in older adults (HAROLD) model
postulates that under similar circumstances, prefrontal activa-
tion during cognitive processes tends to be less lateralized in
older adults than in younger adults.14 These patterns of bilateral
activation have been illustrated using neuroimaging with both Target
simple motor tasks such as button-pressing15 and also more 0
complex tasks such as verbal working memory and memory Stimulus value
retrieval.16-18 A second neuroimaging finding is of an age-
related reduction in occipitotemporal activity coupled with an
increase in frontal activity. This posterior–anterior shift, Probability of neuronal activation in
labeled PASA, has been demonstrated across multiple different response to a specific stimulus in
cognitive functions, including attention, visuospatial process- older adults
ing, and memory (see Davis et al. for review).19 100
A theory of functional compensation has been proposed to
Probability of activation

account for these age-related changes in functional activation.


This view suggests that these patterns of activation reflect the
recruitment of alternate brain regions to counteract neurocogni-
tive decline.14,20 It has been proposed that aging reduces the
already limited supply of cognitive processes, producing defi-
cits on demanding cognitive tasks.21 Thus, the aging brain
needs to engage additional brain areas to generate the same Target
amount of resources as younger adults. For example, it has 0
been suggested that the PASA pattern reflects the recruitment Stimulus value
of anterior regions to compensate for sensory processing defi-
cits in more posterior regions.22 Elaborating on the compensa-
tion theory, the scaffolding theory, proposed by Park and Figure 1. Age differences in hypothetical activation thresholds for a
neuronal network in response to a stimulus of varying likeness to a
Reuter-Lorenz23 posits that increases in functional brain acti-
target stimulus.
vity, particularly in the frontal cortex, represent ‘‘compensatory
scaffolding.’’ They define scaffolding as ‘‘the recruitment of
additional circuitry that shores up declining structures whose mechanisms.29,30 According to this view, age-related declines
functioning has become noisy, inefficient, or both.’’ They pro- in neuromodulation lead to less accurate information transmis-
pose that scaffolding is not a response to aging itself but is sion, higher levels of random variability, and less distinct (and
instead a response to challenge, as even younger adults can thus more confusable) mental representations of information.
show evidence of compensatory activation. Although increases One theory proposed by Li et al30 is that dedifferentiation may
in activation can reflect successful compensation as evidenced stem from disruptions in the dopamine system, which affect the
by improved performance,18 increases in activation can also modulatory role of the prefrontal cortex. The prefrontal cortex
reflect unsuccessful compensation attempts in the case when provides top-down modulation of goal-based information
age-related decrements are still evident.14,24-26 processing in various posterior brain regions and is responsible
In addition to age-related increases in activation, functional for enhancing the processing of relevant information while sup-
activation patterns also tend to be less specific in older age, and pressing irrelevant information. An age-related decline in pre-
it has also been suggested that declines in neural integrity lead frontal modulation can thus lead to increased neural noise and
to reduced specialization, or differentiation, of task-specific reduced neural specificity in these posterior regions. Therefore,
behaviors. For example, studies have demonstrated less neural older networks are less discriminant and more likely to respond
specialization (ie, less category-specific activation) in older to similar but nontarget stimuli due to a lack of top-down
adults compared to young adults in posterior regions when pro- modulation from the prefrontal cortex. Figure 1 provides a the-
cessing visuospatial information.27,28 The theory of dedifferen- oretical illustration of how the threshold for neuronal network
tiation proposes that aging is associated with declines in neural activation may become less stringent and more variable with
specificity due to difficulty engaging specialized neural age. It has been hypothesized that these declines in neural

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Drag and Bieliauskas 77

specificity result in increased correlations among cognitive


processes, as abilities that are independent in young adults tend
to become interrelated in old age.31-33 However, the extent of 90
these intercorrelations has been subject to debate.34,35 High CR

Correct % performance
80

Moderating Variables in Cognitive Aging 70


Low CR

Albert Einstein was still writing and publishing books at the


age of 71, yet surely we do not hold all septuagenarians to this 60 Threshold
dementia
standard. There are many variables that affect cognitive aging,
including education, intelligence, and sensory abilities. Given Age 30 40 50 60 70 80 90
the many extraneous influences that can moderate the cognitive Lower CR Higher CR
= age 65 = age 85
aging process, it is not surprising that interindividual variability
increases with age. Ardila36 reported increases in cognitive het-
erogeneity across older individuals through greater score dis-
Figure 2. Dementia thresholds and cognitive decline as a function of
persions on intelligence testing. These dispersions were not cognitive reserve (CR). Reprinted with permission from Bieliauskas
uniform across all domains, as tasks assessing executive func- and Antonucci.52
tioning and attention had greater variability than those asses-
sing visuoconstruction and fund of general knowledge.
Greater heterogeneity was also shown in those individuals with years of formal education. In addition, Stern et al48 demon-
lower scores. strated that in a group of individuals with AD with equivalent
It has been proposed that education levels can account for a cognitive symptoms, those with higher education had more
significant portion of the cognitive variance associated with pathology, indicating that they were further along in the disease
normal aging. Studies have found positive relationships process despite evidencing similar cognitive abilities.
between levels of education and performance on cognitive While cognitive reserve may be a protective factor against
tasks including block design, verbal fluency, and digit age-related decline, it may also be that individuals with higher
span.37,38 Within the memory domain, education can affect reserve start out with more resources and therefore take longer
recall ability but generally has minimal effects on recognition to reach the critical threshold where deficits start to appear,
performance, suggesting that education primarily affects mem- even with a comparable rate of decline. For example,
ory performance in tasks with high strategic demands. Years of Tucker-Drob et al49 demonstrated that vocabulary knowledge
education have also been associated with lower rates of cogni- and years of education, 2 markers of cognitive reserve, were
tive decline across time39 (although this has been debated40-42), positively associated with levels of cognitive performance but
better performance on cognitive tasks,43 lower incidence of not rates of decline over time in older adults. They suggested
dementia,44 and reduced brain atrophy,37 though possibly that education positively influenced cognitive abilities in ear-
because a high level of education may be a proxy indicator lier adulthood and that these benefits persisted throughout the
of cognitive reserve. Cognitive reserve is thought of as either life span. Thus, high cognitive reserve can delay the onset of
a passive (eg, the capacity of neurons) or a active (eg, the abil- clinical symptoms of dementia due to an absolute improvement
ity to optimize performance by recruiting alternative brain net- in cognitive performance, regardless of alterations in the rate of
works) process that allows an individual to cope more age-related cognitive decline. In addition, because individuals
successfully with age-related brain changes.45 This reserve with higher reserve often have higher levels of pathology
capacity, a latent construct often measured by education or before cognitive symptoms appear, the rate of cognitive decline
vocabulary, is thought to reflect the resilience and plasticity after symptom onset may appear accelerated in this group.50,51
of cognitive networks that protect individuals from the negative Figure 2 illustrates how symptoms of dementia may be notice-
effects of aging (or at least allow them to compensate). Similar able at later stages of decline for individuals with high cogni-
to the scaffolding theory of Park and Reuter-Lorenz, the more tive reserve compared to individuals with low cognitive
reserve (or scaffolds) an individual has, the more he or she will reserve even given identical rates of decline.52
be able to successfully cope with disruptions in the aging brain. Education is not the only variable to affect normal aging.
Indices of cognitive reserve have been positively associated Lindenberger and Baltes40,41 found that contrary to the cogni-
with cognitive performance in multiple domains including tive reserve hypothesis, neither education, affluence, nor cogni-
attention and memory46 and is thought to be a protective factor tive ability predicted age-related differences in cognitive
against the expression of age-related cognitive decline. Cogni- abilities, leading them to propose that declines were based on
tive reserve appears to moderate the relation between age- biological and not social factors. They demonstrated that visual
related pathology and cognitive functioning. Examining both and auditory acuity can account for a large percentage of age-
cognitive performance and postmortem brain autopsies in a related variance across cognitive tests, including those asses-
group of older adults, Bennett et al47 found that the relation sing processing speed, reasoning, memory, and fluency. It was
between AD pathology and cognitive function differed by proposed that sensory function, while serving as a general

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78 Journal of Geriatric Psychiatry and Neurology 23(2)

index of neurobiological brain integrity, is also a fundamental Taking a more localized approach, the frontal aging
component of cognitive function. It is intuitive that sensory hypothesis posits that the frontal lobes are particularly sensitive
abilities can have a significant impact on cognitive functioning. to the aging process and that declines in frontal efficiency can
Weale53 demonstrated that the amount of light reaching a account for many of the cognitive deficits associated with
60-year-old retina is only one third of the amount that reaches cognitive aging.76-78 As will be discussed in later sections,
a 10-year-old retina, and imaging studies have demonstrated age-related cognitive changes in multiple domains including
that cortical responses to sensory inputs also decline with executive functioning, language, and memory can be traced
age.54,55 Sensory inefficiency means that more cognitive to inefficiency in frontal-based processes such as strategy
resources and effort need to be put toward stimulus identifica- initiation, retrieval from long-term memory, and effortful pro-
tion, taking these resources away from more complex, cogni- cessing. Although there is consistent evidence of declines in
tive operations such as memory for the stimuli.56-59 This has frontal functioning with normal aging, there is still some
implications for the clinician seeing geriatric patients, as a false disagreement over whether the frontal lobes are preferentially
positive diagnosis of cognitive dysfunction can occur if sensory susceptible to normal aging compared to other regions. For
losses are not taken into account. On a more positive note, older example, Greenwood79 argues that the frontal lobe is not par-
adults derive more sensory benefit from supportive context than ticularly unique in showing age-related changes and suggests
younger adults, suggesting that compensatory processes can help that it may be more appropriate to view aging from a network
overcome some aspects of age-related sensory degradation.57,58 rather than localization approach. She posits that aging may not
Intraindividual variability also needs to be taken into simply affect 1 region but rather alter the dynamic of a more
account when assessing the cognitive functioning of older complex processing network that spans several brain regions.
adults. For example, the effects of time-of-day on cognitive Addressing age-related changes in specific cognitive
functioning have been well established with the general finding processes, the inhibitory control hypothesis suggests that
that for older adults, cognitive abilities peak in the morning and decreased efficiency in inhibitory processes can explain age-
gradually decline over the course of the day.60,61 Older adults related changes in certain cognitive abilities such as working
tend to be more active and energetic in the mornings and show memory.76,80 The ability to inhibit or suppress task-irrelevant
greater medication and appointment adherence during these stimuli is thought to rely on the frontal lobes, and impairments
hours.62 However, this is not to say that older adults should call in these processes can lead to deficits on interference-sensitive
it a day after lunch. Ryan et al63 demonstrated that drinking caf- tasks. For example, if irrelevant information is allowed to enter
feinated coffee can actually minimize this decline and lead to working memory, there is a heightened susceptibility to dis-
improved cognitive performance in the afternoon. traction, especially when presented with multiple sources of
information (eg, following a conversation in a crowded room).
Within the memory domain, older adults show increasing sus-
ceptibility to retrieval interference compared to younger adults,
Theories of Aging
particularly when facts share the same concepts and compete
Although there is no question that normal aging is accompa- with each other at retrieval, termed the ‘‘fan effect.’’ The fan
nied by changes in cognitive abilities, there is still debate about effect, named after its conceptual likeness to a folding fan,
what specific mechanisms, if any, underlie these changes. refers to the finding that as the number of facts associated with
There are several theories that have suggested a single, funda- a particular concept (ie, the size of the fan) increases, speed and
mental mechanism that can account for much of the decline in accuracy in retrieving these facts from memory decreases.
cognitive function across domains. These theories range in Thus, as the size of the fan increases, so does the amount of
explanation from the neurochemical (eg, the dopamine theory interference from irrelevant information in memory. Older
of aging) to the localized (eg, the frontal hypothesis of aging) adults are more susceptible to the fan effect, suggesting an
to the process level (eg, theories of processing speed and age-related decrease in the inhibitory mechanisms required to
inhibition). These theories are not mutually exclusive, given screen out conceptually relevant but nontarget information.81,82
that they attempt to explain different levels at which cognitive Many complex cognitive tasks rely on inhibitory processes to
abilities can be affected. Examples of some current theories of suppress irrelevant information, clear away information that
cognitive aging are addressed below. is no longer useful, and override the production of dominant but
At the neurochemical level, the dopamine hypothesis of inappropriate responses. Inhibition is particularly important on
aging posits that age-related dysregulation in the dopamine sys- tasks requiring an individual to sustain goal-directed activity.
tem mediates the cognitive deficits associated with normal Such tasks include those involving problem solving, working
aging.64 There is substantial evidence suggesting that normal memory, set-shifting, and selective attention.
aging is accompanied by dopamine dysregulation in multiple Also addressing age-related changes in processing, the
areas including the striatum and the frontal cortex65-69 and speed of processing hypothesis proposes that a large portion
fluctuations in dopamine levels can significantly affect cogni- of age-related variance on cognitive tasks can be accounted for
tion.70,71 Several studies have demonstrated that dopamine by declines in the speed in which older adults process informa-
markers are a strong predictor of cognitive performance, partic- tion.83,84 Increasing age is associated with a decrease in the
ularly executive functioning abilities, in normal aging.72-75 speed with which cognitive processes can be executed, leading

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Drag and Bieliauskas 79

to impairments in various cognitive functions, including Domain-Specific Cognitive Changes


working memory, free recall, and verbal fluency, although to
different extents depending on task complexity and domain.
Mental Status
Verhaeghen et al85 demonstrated that age-related slowing is
minimal for low-complexity verbal tasks but increases for ver- A mental status measure widely used to briefly assess global
bal multiplicative tasks and low-complexity visuospatial tasks. cognitive functioning in the older adult population is the
Age-related slowing was largest for a multiplicative visuospa- Mini-Mental State Examination (MMSE). MMSE scores
tial processing task. Processing speed effects can occur via decline with normal aging, although change is relatively mini-
2 mechanisms. Slowed processing speed can lead to cognitive mal until the later decades. Score variability also increases
deficits because time-limited processes cannot be executed with age.90 Although a threshold of 24/30 is frequently used
efficiently enough within a given time frame (the limited time to screen for dementia, it has been suggested that higher cut
mechanism) and also because the relevant products of earlier scores are more clinically useful in detecting possible cognitive
processing may be lost by the time they are needed after later impairment.91 Roper et al92 found that in a sample of geriatric
processes are complete (the simultaneity mechanism).83,84 inpatients, a cut-off of 26 yielded the highest diagnostic accu-
Although there is no doubt that processing speed declines with racy in detecting brain dysfunction.
age, there has been debate over whether it can explain signifi- Education and IQ also affect MMSE and need to be taken
cant variance across cognitive domains.86 While inferences into account when assessing mental status scores.93 Crum90
based on cross-sectional data have demonstrated up to 71% demonstrated that in a large group of both younger and older
of shared variance between age-related processing speed and adults, individuals with less education tended to demonstrate
memory changes,87 longitudinal studies have suggested a more lower scores and also a wider variability in scores. In this study,
modest role of processing speed in cognitive aging. A longitu- the median MMSE scores for individuals with 5 to 8 years of
dinal study by Lemke and Zimprich88 found that age-related schooling was 26, compared to a median score of 29 for those
changes in processing speed accounted for only 37% of the with at least 9 years of school. It has been suggested that for
variance in age-related memory changes, which is lower than elderly individuals with a high school education and beyond,
expected based on cross-sectional data. Sliwinski and a score of 26 or below warrants further investigation into pos-
Buschke89 demonstrated that while cross-sectional analyses sible dementia.94 In addition, given the positive correlation
show that processing speed accounted for between 70% and between MMSE scores and IQ levels, caution needs to be taken
100% of age differences in various cognitive abilities, this when interpreting low MMSE scores in certain populations, as
drops to 6% to 29% when longitudinal analyses were used. low MMSE scores may not necessarily reflect cognitive
Thus, focusing on cross-sectional differences rather than long- decline in individuals with a below-average IQ (ie, 89 and
itudinal changes can lead to overestimates of shared variance. below).95
While processing speed can account for substantial variance Given that MMSE scores can be influenced by age, educa-
in age-related cognitive functioning, other factors certainly tion, and IQ, it has been suggested that comparing scores over
need to be taken into account. This is the case with all theories time may be more useful in detecting dementia than a single-
of aging, as no single theory has been able to fully account for point evaluation, as a score of 20 may not necessarily indicate
all of the variance associated with cognitive aging across all cognitive decline in certain populations.96 This is consistent
cognitive domains. It may be, however, that different theories with more general suggestions that serial assessment is more
are better able to explain age-related changes in different reliable in detecting cognitive decline (particularly in the inci-
cognitive processes. pient stages of a neurodegenerative process) than single-point
Although the above theories predict that cognitive decline in assessments.97,98 Eslinger et al99 found that a decline of 3 or
normal aging is caused by a single mechanism and a common more points on the MMSE over a 6-year period was predictive
cause, each of these theories is not necessarily mutually exclu- of poorer health, depressive symptoms, and lower neuropsy-
sive. For example, it is possible that dopamine dysregulation is chological scores, suggesting that declines of 3 or more may
the primary cause of age-related frontal dysfunction, given that signify a departure from healthy aging. Other studies have
the frontal lobes are a main target of efferent striatal and ventral examined specific subcomponents of the MMSE for use in clin-
tegmental dopaminergic pathways. Frontal-based dopamine dys- ical practice. For example, it has been demonstrated that the
regulation may then lead to declines in processing speed and most predictive combination of MMSE subtests for cognitive
inhibition.72 Thus, it may be that normal aging is accompanied impairment in individuals 60 years and older was the summed
by multiple physiological and cognitive changes across a variety scores of time orientation and serial sevens.100 Those individ-
of levels, including any and all of the above mechanisms. This uals who had a summed score of above 7/10 were likely to
illustrates the need for a single unifying theory that can explain score above a 24 cut-off in the full battery, suggesting that these
the interrelated mechanisms of cognitive aging across these dif- 2 subtests alone can be informative if time is limited. The
ferent levels. In addition, none of the above theories makes delayed recall portion of the MMSE may also be of interest
explicit predictions regarding functional activations, and future in those individuals with suspected memory impairment. In a
models of cognitive aging will need to incorporate possible group of healthy older adults, Chandler et al101 demonstrated
explanations for age-related functional changes. that the majority of individuals remembered 2 to 3 of the

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80 Journal of Geriatric Psychiatry and Neurology 23(2)

3 words after a delay. Recall of 0 or 1 words occurred in only Task-switching is thought to rely on control processes related
3% of healthy individuals compared to 87% of individuals with to executive functioning and has been associated with activity
AD within the 50 to 75 age group. Thus, good recall (ie, 2 to in the medial and dorsolateral prefrontal cortex and frontopar-
3 words) is the norm in most cases of normal aging and ietal white matter tracts.121,122
anything below this may be indicative of memory impairment.
Executive Functioning
Attention Executive functioning can be conceptualized as a higher order
We are faced with situations in daily life that rely on multiple cognitive construct that is involved in the self-regulation of
aspects of attention, such as navigating through a grocery store goal-directed behavior and the effective organization and use
armed with a grocery list or talking on the phone while cooking of large amounts of information. Executive functions are
dinner. Even a short drive in an unfamiliar location requires diverse but share a common dependence on the prefrontal cor-
multiple aspects of attention, some of which may be affected tex, which is in itself a heterogeneous structure with extensive
by normal aging. Sustained attention is needed over such a connectivity to other areas of the brain. Nevertheless, age-
10-minute drive, as is selective attention to ignore the adver- related decrements are often found on tasks requiring executive
tisements on the side of the road, divided attention to listen functioning processes, which is consistent with the frontal
to an ongoing conversation in the car, and task-switching to aging hypothesis. Such tasks include those assessing planning,
shift attention from the written directions to the road ahead. inhibition, set-shifting, and verbal fluency.123-126 It has been
In fact, motor vehicle accident rates have been related to per- suggested that executive functioning decrements may be
formance on measures of attention, particularly those assessing related to a failure to implement the necessary strategies to suc-
switching of selective attention.102 Thus, age-related declines cessfully execute these tasks.127 The self-initiation of strategic
in certain aspects of attention may reduce the efficiency to processes is thought to rely on the integrity of the prefrontal
operate in complex situations. cortex.128-130 A failure to initiate appropriate strategies can
Sustained attention is the ability to maintain attention and have significant effects on other cognitive processes (eg, mem-
vigilance over time and is considered a simple attentional pro- ory recall) as will be discussed in later sections.
cess that is relatively unaffected by normal aging.103,104 Inhibi- Elderkin-Thompson et al131 recently reported that prefrontal
tion and selective attention are also important components of structural volume explained variability in executive function-
attention. As discussed previously, normal aging leads to ing performance better than chronological age, suggesting that
changes in inhibitory control, which affects the ability to focus prefrontal integrity mediates age-related executive functioning
on relevant information while inhibiting task-irrelevant infor- changes. Similarly, Gunning-Dixon and Raz132 demonstrated
mation, termed selective attention. Selective attention can be that set-shifting ability correlated negatively with prefrontal
measured by tasks such the Stroop Interference Test, which volume in older adults. It should be noted that in this study, var-
requires an individual to focus on task-relevant stimuli proper- ious executive function tasks were associated with various pre-
ties (ie, naming the colors of printed words) while inhibiting frontal structures, illustrating the heterogeneity of the executive
prepotent responses (ie, reading the words regardless of the functioning construct. Further illustrating the diversity within
color). Selective attention is generally thought to be age-sensi- this domain, Treitz et al133 demonstrated that executive func-
tive,105-108 although these findings are not entirely consis- tioning does not decline unitarily, as normal aging differen-
tent.109 Decreases in inhibitory control resulting in increased tially affects executive subcomponents. In addition, this study
disinhibition and distractibility have been associated with demonstrated that executive functioning does not decline line-
altered prefrontal functioning.78,110 arly across the life span, as there is a sharp decline in executive
Older adults also have difficulty when required to concur- functioning abilities after the age of 60.
rently attend to and process information from multiple sources, One area of executive functioning with significant real-
termed divided attention. While this dual-tasking can have neg- world implications is working memory. Working memory is
ative effects on cognitive functioning even in younger adults, often confused with short-term memory, which is the mainte-
older adults are particularly susceptible to the negative effects nance of information in memory over a short period of
of divided attention and can show significant decrements in time (eg, keeping a telephone number in mind while walking
performance on tasks such as short-term memory, associative to the kitchen phone). Working memory, in contrast, requires
memory, and recognition memory under divided attention.111- the active manipulation and processing of information (eg, sub-
116
Although divided attention can affect even simple cognitive tracting a dollar amount from a bill total). Normal aging has a
processes such as tone recognition, age-related decrements are greater impact on working memory than on short-term mem-
generally more pronounced for complex tasks.106 Similar to ory.89,134,135 This may be because working memory places
divided attention, task-switching is the ability to switch rapidly greater demands on cognitive resources, as it requires informa-
among different skills or tasks and also shows age tion processing in addition to basic storage. Consistent with
effects.117,118 Task-switching deficits may be related to general this, increases in working memory task complexity magnifies
effects of slowing or an inability to disengage attention from age-related decrements. For example, age differences are
1 task and shift attention to refocus on another task.119,120 more pronounced for a taxing n-back task than for a simple

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Drag and Bieliauskas 81

digit-span task.136 Thus, an older adult may be able to write tasks than on recall tasks, suggesting that the information is
down a simple phone message with ease but have more diffi- available in memory but not easily accessible.113,148,149 Thus,
culty when trying to remember and calculate prices while gro- older adults may properly encode and store information but
cery shopping. Working memory impairments can also lead to struggle when asked to retrieve this information. A recognition
difficulty following long and complex instructions or answer- format, such as a multiple-choice test, relies less on strategic
ing multiple-choice questions, as older adults may not be able search and retrieval, as one can rely solely on more automatic
to remember and process this complex information as well as processes of familiarity to make a recognition decision. In addi-
their younger counterparts. tion, a recognition format provides more context compared to a
It has been suggested that age-related declines in working recall format, such as essay writing. When recall demands are
memory may stem from decrements in attentional control and eliminated with a recognition format, age effects are
inhibition that cause working memory processes to be parti- attenuated.
cularly vulnerable to interference. It may be that passive main- It is thought that deficits in effortful memory processes arise
tenance processes are also affected by this interference but primarily due to inefficiency of the frontal lobes to engage in
older adults can recruit compensatory brain regions to support the self-initiation of strategic processes at both encoding and
performance. However, when more taxing manipulation pro- retrieval, consistent with the frontal aging hypothesis. Episodic
cesses are needed, the available resources cannot meet memory is particularly poor when the task demands significant
demands, leading to deficits in performance.137 cognitive resources or when cues or environmental support are
unavailable, necessitating self-imposed organization and strat-
egy.150,151 While older adults may have the capability for good
Memory memory, they may not always initiate the necessary processes
Aging does not lead to a global memory decline but rather has and strategies needed to optimize their abilities.38,152 Thus, it
differential affects on specific aspects of memory. Memory is has been proposed that age differences in memory can be
not a unitary construct and can be parsed into several dissoci- explained by degree to which self-initiated processes are neces-
able subcomponents including explicit and implicit memory, sary.21 These initiation processes are dependent on the frontal
semantic and episodic memory, and encoding and retrieval pro- lobes, and it has been suggested that deficits in frontal pro-
cesses, all of which show dissociations in normal aging. cesses (eg, working memory) mediate age-related declines in
episodic memory,9 consistent with the frontal aging hypothesis.
Episodic memory. Episodic memory is defined as the con- Neuroimaging evidence also supports the role of the frontal
scious recollection of experienced events, such as a 21st birth- lobes in age-related memory changes as reduced functional
day party, a phone conversation from last week, or a word list activation in prefrontal regions has been associated with poorer
from 30 minutes ago. In general, episodic memory declines memory performance in older adults.144,153,154
with age,138-140 although it has been demonstrated that effortful
components of memory are more affected by aging compared Semantic memory. Semantic memory, often referred to as
to more familiarity-based, automatic components.141 crystallized intelligence, refers to the store of factual know-
Aging can affect the encoding of new information, particu- ledge in memory. Examples of information that can be stored
larly when effortful or strategic processes are required.142 For in semantic memory include definitions of words, historical
example, younger adults benefit from levels of processing facts, and the names of all 50 state capitals. Semantic memory
manipulations more than older adults, suggesting that older actually increases with age as individuals accrue knowledge
adults encode the meaning of new information less thor- over their life span,155-159 although it may decline in the very
oughly.143 Neuroimaging has shown age-related decreases in later decade.160,161 This is in contrast to fluid intelligence,
functional activity in the medial temporal lobes and left pre- defined as active problem solving ability in tasks in which solu-
frontal cortex at encoding, which has been associated with tions cannot simply be derived from formal training or prior
poorer subsequent memory performance.17,144,145 knowledge.162 Fluid intelligence is age-sensitive.32,163 Seman-
Retrieval of information from memory is also affected by tic memory does not show age-related decline and actually
the degree to which effortful processes are needed. Recognition increases with age. Park et al164 demonstrated that while fluid
memory, which is relatively passive and nonstrategic, is less processes such as working memory, processing speed, and
affected by normal aging than recollection, which requires memory recall decline with age, world knowledge as measured
more effortful processing.113,146 It is not surprising that aging by vocabulary abilities actually increases across the life span.
differentially affects recall ability, as recall tasks require Figure 3, adapted from Park et al, illustrates how semantic abil-
greater processing capacity, which is already limited via the ities such as vocabulary increase with age while more fluid
normal aging process.147 Recall tasks require an individual to abilities such as working memory and processing speed show
screen out irrelevant information from memory, making the a reverse pattern. This increase in semantic memory is associ-
recall process much more difficult than recognition, where the ated with the accumulation of factual knowledge over the life
information options are already provided. Although both rec- span. Thus, a lifetime of experiences gives older adults the
ognition and recall tasks can be sensitive to normal aging, older important advantage of increased wisdom over their younger
adults fare much better on yes-no or forced-choice recognition counterparts. While semantic knowledge can often appear

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82 Journal of Geriatric Psychiatry and Neurology 23(2)

individual’s behavior without intentional retrieval or conscious


Cognitive changes associated with recollection of this experience.172,173 For example, asking an
normal aging individual to recollect what he or she ate for dinner requires
an active search through memory. By contrast, one can swim
backstroke without consciously recalling what he or she has
learned in swim lessons, illustrating a type of implicit memory
termed procedural memory. Implicit memory is relatively unaf-
Standard scores

fected by aging compared to explicit memory.138,139,174,175


Although some age-related implicit priming deficits have been
demonstrated (more so for perceptual than conceptual
priming), these age-related effects are much less than what is
found for explicit tasks.176,177
20−29 30−39 40−49 50−59 60−69 70−79 80−89

Age (in years)


Familiarity. Familiarity is a feeling of recognition in the
absence of contextual details. For example, you may recognize
Vocabulary Long−term memory a person as familiar but may be unable to recall specific details
Processing speed Working memory about who he or she is or where you met him or her. This is in
contrast to recollection, which is the effortful retrieval of spe-
Figure 3. Differential effects of normal aging on processing intensive cific contextual information.178 Familiarity thought to rely on
tasks and verbal knowledge abilities. Adapted with permission from the entorhinal cortex is relatively unaffected by the aging pro-
Park et al.164 cess compared to recollection, which is thought to be more
hippocampal-dependent.179-183 In addition, while prefrontal
impaired in older adults at first glance due to difficulties with and parietal regions are involved in both familiarity and recol-
word finding and name retrieval, these difficulties are associ- lection, within these general brain regions, distinct subregions
ated more with problems retrieving this information rather than have been shown to be functionally specialized for each pro-
an actual semantic deficit. cess.184,185 Typically familiarity and recollection processes
work together to support recognition memory; however, older
adults may tend to overrely on their feelings of familiarity
Autobiographical memory. Related to episodic memory, auto-
when they are experiencing recollection failures, which can
biographical memory is memory for one’s own life events in the
have detrimental effects (eg, false memories). Reliance on
past. There is some debate regarding whether autobiographical
familiarity as a compensatory mechanism for poor recall has
memory and episodic memory are synonymous, as they both
also been supported by neuroimaging evidence.186
involve conscious recollection of an experienced event.165
However, it has been suggested by some researchers that auto-
Flashbulb memory. Flashbulb memory, a special type of auto-
biographical memory is characterized by greater personal rele-
biographical memory, is a vivid recollection of an emotionally
vance, emotional content, and a longer period of time between
salient event that is generally more durable than memory for
encoding and retrieval.166,167 Another difference is that episodic
everyday experiences. For example, people frequently claim
recollection involves reexperiencing the personal event, whereas
to have vivid memories for events such as the assassination
autobiographical memory is primarily defined by the content of
of John F. Kennedy and the Challenger explosion. Flashbulb
the memory (ie, memories involving the rememberer) but does
memories by definition are stable over long periods of time
not necessitate the same reliving of the past as episodic mem-
(ie, 5 decades or more) and differ from other memories in the
ories do.167 Compared to semantic information (eg, knowing that
amount of personal importance attached to the events and the
Paris is the capital of France), autobiographical memories (eg,
amount of rehearsal.187 Flashbulb memories are unique from
remembering a summer vacation in Paris) are more sensitive
other remote episodic memories for everyday events in that the
to normal aging.168,169 Compared to younger adults, older adults
ability to recall flashbulb memories is relatively unaffected by
tend to recall autobiographical memories that are more semantic
aging and is not related to frontal functioning.188 In addition,
in nature and contain factual information rather than episodic
memory for the source of news in flashbulb memories is
and time- and place-specific details.169,170 This is consistent with
relatively impervious to the aging process.189,190
the findings that episodic but not semantic memory declines with
age. Autobiographical memory retrieval has been associated
False memory. In general, older adults are more susceptible to
with bilateral hippocampal activation in older adults, compared
false memories than their younger counterparts.191 This may be
to left hippocampal activation found in young adults,171 consis-
because older adults counteract recollection failures with an
tent with age-related delateralization.
overreliance on familiarity or gist-based memory, which is less
vulnerable to aging than recollection.192 An inability to recall
Implicit memory. Implicit memory is a form of memory in specific episodic details (eg, memory of seeing the word on the
which a previous experience indirectly influences an computer screen) to counter these feelings of familiarity leads

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Drag and Bieliauskas 83

to higher rates of false memories in older adults.193 For exam- (eg, remembering to take the toast out of the oven and the
ple, Dywan and Jacoby194 demonstrated that older adults are scrambled eggs off the stove), older adults have increased sus-
more susceptible to the false fame effect. In false fame para- ceptibility to prospective memory errors.210 Prospective mem-
digms, nonfamous names evoke a sense of familiarity because ory deficits are thought to reflect a problem remembering to
they have previously been presented. Without a specific recol- carry out a task when it needs to be done rather than a deficit
lection of this exposure, this familiarity can mistakenly be in planning or an inability to carry out the task itself.211 Older
attributed to fame (eg, that name sounds familiar, he or she adults’ prospective memories often fare better in naturalistic
must be famous). Behavioral evidence has suggested that false settings outside of the laboratory, perhaps because they have
memories are mediated by frontal functioning,195 perhaps via a learned to set up external cues and rely less on their own mem-
more liberal response bias and an impairment in frontal inhibi- ory abilities. For example, older adults are better than their
tory processes. Neuroimaging has also shown that areas of the younger counterparts when asked to mail a postcard, log in to
middle and superior temporal gyrus are associated with false an electronic organizer, or attend an appointment.212-214
memories in older adults, which suggests a tendency to rely Maylor215 demonstrated that older adults perform better on a
on gist-based process mediated by this region.196,197 prospective memory task when it was conjoined with another
routine event, suggesting that mnemonic strategies like leaving
Source memory. Source memory is thought of as memory for evening medications by a toothbrush will help with prospective
the spatial, temporal, or social characteristics of the specific memory abilities.
conditions or context under which a memory is acquired. Mem-
ory for contextual details is affected by normal aging more so
than memory for gist or content.198-200 For example, you may
Language
easily recognize the woman standing in line in front of you in Although specific language abilities are relatively unaffected in
the grocery store, but it is much more difficult to remember normal aging, language difficulties may arise due to changes in
whether you know her from church or from the library. When frontal or sensory processes. Most language problems are due
only simple recognition is required, older adults can rely on to retrieval difficulties rather than a loss of semantic informa-
familiarity and gist; however, when more contextual informa- tion.216,217 For example, while older adults may have more dif-
tion needs to be recalled, memory often fails. In a study by ficulty finding the right word they want to use, their semantic
Schacter et al,201 older adults could adequately remember new knowledge of linguistic rules does not decline.218,219
facts over a delay but often forgot where they had learned them. There is some evidence of mild declines in naming abilities,
One hypothesis is that age-related source memory deficits stem although again this is typically thought to be related more to
from a failure to spontaneously bind contextual details with word-finding difficulties rather than a loss of semantic infor-
other content components of the memory.202 When individuals mation.217,220,221 During natural discourse, older adults tend
are oriented to the relationship between an item and its context to demonstrate more word-finding difficulties, as evidenced
at encoding, source memory improves.203 Thus, source mem- by filled pauses (‘‘um’’), ambiguous references, and word
ory deficits may arise from an inability to self-initiate the nec- retrieval errors.222 Oftentimes, older adults experience word-
essary encoding strategies to bind contextual details to memory finding problems despite certainty that they know the word,
for the item itself, consistent with the frontal aging hypothesis. commonly called a tip-of-the-tongue experience (TOT).216,223
Source memory deficits have been associated with reduced Tip-of-the-tongue experiences are thought to reflect a deficit
recruitment of frontal and hippocampal regions during encod- in phonological retrieval rather than access to lexical informa-
ing.204 Further illustrating frontal involvement in source mem- tion.224,225 Specifically, conceptual representations of the
ory, correlations between source memory and performance on meaning of words and sentences are well preserved with nor-
measures of frontal functioning have been reported in older mal aging, but older adults have difficulty accessing the phono-
adults.203,205,206 logical information necessary for word retrieval.226-229
Because of this phonological deficit, providing phonological
Prospective memory. We rely heavily on prospective memory cues or phonologically related words will be more helpful to
in everyday life to remember to carry out events in the future resolve TOTs than providing semantic cues.230 Thus, an older
such as sending a birthday card to a friend or remembering to adult may fail to retrieve the name of the mountain with car-
send an email after finishing a conversation with a coworker. vings of the presidents, but it is expected that phonological cue
Prospective memory can be time-based (eg, remembering to such as ‘‘ru-’’ should help resolve the TOT experience more so
take medications at noon) or event-based (eg, remembering than a semantic cue such as ‘‘South Dakota.’’ It has been
to take medications with lunch). Age-related declines in pro- demonstrated that TOTs are greater for proper names more
spective memory have been widely demonstrated.138,207-209 so than other types of words.231,232 Imaging has suggested that
Prospective memory requires significant self-initiated retrieval, age-related increases in TOT are associated with atrophy of the
as one needs to ‘‘remember to remember’’ and with age, inter- left insula, an area of language system important for phonolo-
nal cues and self-initiated processes become less reliable. gical production.233
When external cues are limited (such as in the laboratory Other language changes accompanying normal aging are
setting) or when multiple actions must be kept in memory thought to reflect frontal inefficiency rather than pure language

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84 Journal of Geriatric Psychiatry and Neurology 23(2)

deficits. For example, older adults tend to produce more off- Practical Applications and
topic speech during natural discourse.234,235 This tangentiality
has been related to performance on an inhibition task, suggest-
Recommendations
ing that it may stem from an inability to inhibit salient but irre- Understanding the normal aging process can have important
levant topics.236,237 Verbal fluency is also age-sensitive, and real-world implications. Although most information is gathered
again this is thought to reflect a frontal-based strategy deficit through artificial studies designed in the laboratory, it has been
rather than a specific language deficit.238,239 Sentence compre- found that these laboratory measures can predict performance
hension and text recall may decline with age, more so for text on real-life tasks, such as managing finances and medications
with greater syntactic complexity.157,240,241 These deficits are and using a pay phone.267
thought to reflect an inability to retain text in working memory, Although practitioners often rely on self-report to assess
leading to comprehension and recall deficits.242 functional abilities, the use of objective cognitive assessment
is also important. Studies have demonstrated a poor correlation
between self-report and objective memory abilities.268,269
Mendes et al270 found that older adults were more likely to
Visuospatial Functioning complain of memory problems than their younger counterparts,
In general, visuospatial abilities decline with age disproportio- and that subjective memory ratings were not associated with
nately to verbal abilities.243-247 For example, compared to their objective cognitive performance. They suggested that older
younger counterparts, older adults demonstrate poorer perfor- adults with intact memory were more likely than younger
mance on performance subtests than on verbal subtests of the adults to rate their memory as poor. It has also been suggested
Wechsler Adult Intelligence Scale.248 Measures of visuospatial that self-report measures do not adequately assess decrements
abilities can be heterogeneous in nature and can include visuos- in daily functioning ability.271 Kempen et al272 found that when
patial attention, visuospatial memory, and visuospatial orienta- daily functioning is objectively measured, older adults tend to
tion, all of which can show age-related effects.249-254 Other overestimate functional ability. Thus, caution should be taken
visuospatial processes affected by aging include mental rota- when relying on self-report to assess cognitive abilities and
tion,255 visuospatial construction,256 complex figure copy,257 daily functioning in older adults, and objective tests should
and visuospatial processing speed.252 In contrast, there is no be used whenever possible. Measures of executive functioning
evidence of age-associated visual neglect.258,259 It is unclear have been associated with daily functioning and can serve as
whether visuospatial information itself is more sensitive to nor- objective screening measures when trying to assess functional
mal aging or whether visuospatial information itself tends to be decline.
more complex (and thus vulnerable to age effects) than verbal Although some degree of decline is invariably associated with
information. normal aging, recent evidence has demonstrated that there may be
One visuospatial task commonly used to estimate visuomo- certain factors that have positive effects on cognitive functioning
tor abilities, visuoconstruction, and planning in older adults is in older age. For example, physical activity and fitness have been
the clock-drawing task. Aging has been associated with an associated with faster reaction times, better cognitive perfor-
increased number of errors on this task.260,261 Older adults mance, lower rates of cognitive decline over time, and a lower risk
often have problems placing the figures on the clock face and of cognitive impairment or dementia273-277 suggesting that cardi-
differentiating the clock hands correctly. Omission errors are orespiratory fitness may serve as a buffer against age-related
rare on this task and may suggest abnormal aging. As a caveat, declines. Healthy eating may also improve cognition, as 1 study
clock-drawing ability has also been positively associated with found that reducing caloric intake by 30% improves scores on
level of education,262 so caution should be taken when using memory tests.278 Even engaging in leisure activities has been
this task with individuals with low education levels. associated with slower rates of age-related cognitive decline.279
It has been suggested that visuospatial deficits on more com- In addition, exercising the mind can also have positive effects.
plex tasks stem from age-related changes in frontal functions, Engagement in cognitively stimulating activities has been associ-
such as working memory, consistent with the frontal aging ated with higher levels of cognitive functioning280-282 and a lower
hypothesis. Libon et al263 demonstrated that visuospatial tasks risk of dementia.283 However, there is debate regarding whether
requiring integrative mental processes such as problem-solving engaging in mental activity actually protects against age-related
and mental transformation were more sensitive to age than decline or whether individuals who are mentally active have
other nonintegrative tasks such as complex figure copy. Perfor- higher absolute levels of cognitive performance (possibly due
mance on these integrative visuospatial tasks was associated to lifelong patterns of intellectual engagement that carry into older
with executive functioning. Not surprisingly, visuospatial abi- age) but show equivalent rates of decline.284-286 Regardless of this
ities can have important functions for daily activities. For debate, if there is an absolute threshold where functioning begins
example, Baldock et al264 demonstrated that visual attention to decline, mental exercise, similar to cognitive reserve, should
and visuospatial memory predicted driving performance in improve an individual’s baseline cognitive abilities and thus pro-
older adults. Older adults are also slower at personal orientation long the time until that critical threshold is reached (see Figure 2).
tasks such as map reading, which can have negative effects on Research illustrating the benefits of mental engagement
way-finding abilities.265,266 would suggest that targeted cognitive training may be one way

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Drag and Bieliauskas 85

to improve cognitive functioning in older adults. Cognitive possible underlying causes of age-related cognitive changes.
interventions have been shown to have positive effects on cog- Despite the general debate in the literature, these processes are
nitive abilities with these effects observable at follow-up even not necessarily mutually exclusive, illustrating the need for a
after a number of years.287-289 However, these improvements single unifying theory that can explain the mechanisms of cog-
are generally limited to only the trained abilities with little nitive aging across different neurochemical, anatomical, and
transfer to other tasks (eg, reference 289), suggesting that these behavioral levels.
interventions do not enhance general cognitive functioning.
Cognitive training also has less effect for older adults than their Declaration of Conflicting Interests
younger counterparts,290 even if older adults are given addi- The authors declared no conflicts of interest with respect to the
tional training.291 Thus, while general mental activity may be authorship and/or publication of this article.
associated with increased cognitive performance, the utility
of specific, targeted cognitive training may be minimal. Funding
Older adults can also mitigate age differences using envi- The authors received no financial support for the research and/or
ronmental support. For example, writing down information that authorship of this article.
is likely to be forgotten, providing prompts at retrieval, and
providing memory cues and contextual information at encod- References
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