Jane Martin, Clara Li
Normal Cognitive Aging*
This chapter provides an overview of the principal features of cognitive functioning in normal aging adults. The first part of this chapter considers intelligence and the importance of estimating premorbid intellectual ability to detect discrepancies in functioning, followed by the concept of cognitive reserve being protective as we age. The cognitive functions of attention and processing speed, memory, verbal abilities, and executive functions are discussed before a final section regarding the lifestyle factors associated with cognitive functioning. “Normal” in the present context refers to older adults with no discernible mental illness and whose physical health is typical of their age group.
Intelligence and Aging
The U.S. Bureau of the Census1 projected that between 2010 and 2050, the United States is expected to experience rapid growth in its older population and, in 2050, the number of Americans aged 65 years and older is estimated to be 88.5 million. According to the Alzheimer’s Association,2 an estimated 5.2 million Americans would have had Alzheimer disease in 2014, including approximately 200,000 individuals younger than age 65 years who have younger onset Alzheimer’s. Thus, cognitive studies of older adults are an important area of research. There is a need to understand what is normal or typical aging in contrast to the development of a disease process and to understand what factors contribute to improved cognitive status with increasing age.
Literature on cognitive aging is based on studies of performance on standardized intelligence and neuropsychological tests. “IQ” refers to a derived score used in many test batteries designed to measure a hypothesized general ability, intelligence. The accepted definition is that general intelligence, or g, is a measure of overall ability on all types of intellectual tasks. General intelligence can be more specifically divided into the concepts of fluid intelligence and crystallized intelligence.3 Fluid intelligence is the primary factor of most intelligence tests, measuring the degree to which an individual can solve novel problems without any previous training. On the other hand, crystallized intelligence is the amount of knowledge and information from the world that one brings to the testing situation. It has been established that fluid intelligence declines in older adults, and crystallized intelligence is well preserved. The general theory is that fluid intelligence increases throughout childhood into young adulthood, but then plateaus and eventually declines; crystallized intelligence increases from childhood into late adulthood.3
Because a multitude of cognitive functions are assessed in an intelligence battery, and IQ scores represent a composite of performances on different kinds of items, the meaningfulness of IQ is often questioned.4 The only widely agreed on value of IQ tests is that IQ scores are good predictors of educational achievement and, consequently, occupational outcome. The argument about the usefulness of IQ scores is that a composite score does not highlight important information that is only obtainable by examining discrete scores. Consequently, most widely used tests, such as the Wechsler Adult Intelligence Scale (WAIS-IV),5 now include measures of more discrete factors and domains. Even with limitations, IQ scores help provide a baseline of overall intellectual functioning from which to assess performance on cognitive tests as we age.
Premorbid Ability
Lezak and colleagues have cautioned that an estimate of premorbid ability should never be based on a single test score, but should take into account as much information about the individual as possible.4 Thus, a good premorbid estimation of intelligence in adults uses current performance on tasks thought to be fairly resistant to neurologic change and demographics, such as educational and occupational attainment. This approach uses test scores obtained in the formal testing session of “hold” tests—that is, tests that tap abilities considered resistant to the effects of cerebral insult.6 Aspects of cognitive functioning that involve overlearned activities change very little in the course of aging, whereas functions that involve processing speed, processing unfamiliar information, complex problem solving, and delayed recall of information typically decline with age.7 On the WAIS-IV,5 tests such as vocabulary and information are considered relatively resistant to the effects of aging and thus are useful hold tests to help estimate overall premorbid levels of cognitive functioning. However, there are limitations that must be considered. For example, the information subtest reflects an individual’s general fund of information, and the score may be misleading, because this test is strongly affected by level of education. Scores on word reading tests, such as the National Adult Reading Test (NART),8 developed in Britain, and the subsequent American National Adult Reading Test (AMNART),9 for use in the United States, correlate highly with IQ and have been found to be relatively resistant to cerebral insult.6 However, the AMNART is not useful for an aphasic individual or someone with visual or articulatory problems. Again, the practice of using many sources of information to estimate an individual’s premorbid level of cognitive functioning is essential.
Premorbid estimation of overall intellectual functioning is important to establish to compare current performance against some standard measure. However, comparing an individual’s performance to a general population average score is misleading because it is only useful if the individual matches the population in terms of demographic measures, such as IQ and education. For example, average performance may be considered functioning at a normal level for one individual and may represent a significant decline for another individual. Thus, a more useful approach is to compare an individual’s current performance against an individualized standard. Only in this way can deficits or a diagnosis be discerned. Because premorbid neuropsychological test data are rarely available, it becomes necessary to estimate an individual’s premorbid level of intellectual functioning against which present test scores can be compared to determine a change in cognitive functioning. Assessing a deficit involves comparing an individual’s present performance on cognitive tests to an estimate of the individual’s original ability level (premorbid level) and evaluating the discrepancies.4
Cognitive Reserve
The concept of cognitive reserve10–12 proposes that there are differences in how individuals are able to compensate once pathology disrupts the brain networks that normally underlie performance. Thus, variability exists across individuals in their ability to compensate for cognitive changes as they age. The cognitive reserve model evolved in response to the fact that often there is no direct relationship between the degree of brain pathology that disrupts performance and the degree of disruption in actual performance across individuals. In other words, individuals with a similar degree of brain pathology often differ in their clinical presentation of functional ability. Reserve may represent naturally occurring individual differences in the ability to perform a task or deal with increases in task difficulty. These differences may be due to innate intellectual ability, such as IQ, and/or they may be altered by experiences of education, occupation, or leisure activities.11,12 Stern and associates11,12 have suggested that higher neural reserve might mean that brain networks that are more efficient or more flexible in the presence of increased demand may be less susceptible to disruption. This model suggests that the brain actively attempts to compensate for the challenge represented by brain disease and hypothesizes that adults with higher initial cognitive ability are better able to compensate for the effects of aging and dementia.10,12 However, the cognitive or neural mechanism that underlies cognitive reserve remains unknown. Research in the area of cognitive reserve has recently focused on using functional brain imaging (fMRI) to identify networks that might mediate cognitive reserve.12 Stern and coworkers have proposed two forms of neural mechanisms that underlie cognitive reserve, neural reserve and neural compensation. Neural reserve refers to the idea that reserve may be associated with individual differences in the utility of preexisting cognitive networks. Neural compensation refers to the idea that some individuals may be better able to use compensatory resources than others.12 Recent neuroimaging studies have supported the view that older cognitively normal adults, with higher cognitive reserve, have neural networks that operate more efficiently when task demands increase.12,13
According to the cognitive reserve model, impairments in cognition become apparent after a reserve is depleted. Individuals with less reserve are likely to exhibit clinical impairments because they have relatively fewer resources to maintain them in the course of normal aging and disease-related changes, whereas individuals with more initial reserve can function longer without obvious clinical impairments because their supply of resources is greater.14 The initial level of cognitive reserve may be determined by numerous factors, such as innate intellectual ability and differences in cognitive activity as the brain matures throughout the life span. It has been found that early education and higher levels of intellectual ability and activity are associated with slower cognitive decline as individuals age.12,14–17 Fritsch and associates14 found that IQ and education had direct effects on global cognitive functioning, episodic memory, and processing speed, but that other midlife factors, such as occupational demands, were not significant predictors of late life cognition. Studies of the relationship between childhood intelligence and cognitive decline in later life have found that individuals with lower childhood mental ability experience greater cognitive decline than those with higher childhood mental ability, suggesting that higher premorbid cognitive ability is protective of decline in later life.15 Kliegel and coworkers16 found that early education and lifelong intellectual activities seem to be important to cognitive performance in old age; higher early education and the greater number of intellectual activities continued throughout life served as a buffer against becoming cognitively impaired. Cognitive reserve research suggests that an active engaged lifestyle, emphasizing mental activity and educational pursuits in early life, has a positive impact on cognitive functioning in later life. Thus, individuals whose baseline cognitive functioning is at higher levels and who have an engaged lifestyle, which typically includes interpersonal relationships and productive activities, will likely show less cognitive decline with age. Cognitive reserve is not a fixed entity but can change across the life span, depending on exposure and behavior, which suggests that changes in lifestyle, even later in life, can provide cognitive reserve against age- or disease-related pathology.12
Attention and Processing Speed
Attention relates to one’s ability to focus and concentrate on a given stimuli for a sustained period of time. Attention is a complex process that allows one to filter stimuli from the environment, hold and manipulate information, and respond appropriately.6 Models of attention typically divide attention into various processes, such as alertness and arousal, selective attention, divided attention, and sustained attention. There is a limited amount of information that the brain can process at a given time. Attention allows one to function effectively by selecting the specific information to be processed and filtering out the unnecessary information.
It is difficult to assess pure attention because many tests of attention overlap with tests of executive function, verbal and visual skills, motor speed, information processing speed, and memory. Traditional methods of assessing attention involve timed tasks and tests of working memory. The Wechsler subtest, digit span,5 is a common method for assessing attention span for immediate verbal recall of numbers. Digit span involves the examiner reading progressively longer strings of digits for the individual to repeat forward, backward, and in sequence. Thus, repeating and manipulating the digits requires auditory attention and is dependent on short-term memory retention. Another commonly used test to assess attention is the Continuous Performance Test of Attention (CPTA).18 The CPTA is administered on a computer and consists of the individual seeing and listening to a series of letters and tap with a finger each time the target letter is presented.
Attentional processes, like other cognitive functioning, change over the course of the life span, but attention is particularly vulnerable to the process of aging. Moreover, the effects of aging on attention are related to the complexity of the task. Attention on simple tasks, such as the digit span task, is relatively well preserved into the 80s. On the other hand, on tasks that require divided attention, older adults respond more slowly and make more errors. In normal aging, there is typically a decline in sustained and selective attention and an increase in distractibility.19
With regard to aging and cognition, attention is a prerequisite for healthy memory functioning. Attention is necessary in the process of encoding information for future retrieval from memory and, as we age, the complex processes of encoding and retrieving information require greater attentional resources. Intact attention is also required for the processing of information; processing speed is the rate at which one can process information. Cognitive processing speed refers to how fast a person can execute the mental operations needed to complete the task at hand.20 It is widely believed that the age-related slowing in processing speed underlies declines in other cognitive areas, including memory and executive functioning.21 It is often difficult to assess pure processing speed because many tasks also reflect a visual and/or motor component. Timed tests can measure processing speed and also help the examiner to gain a better understanding of attentional deficits.22 Slowed processing speed is demonstrated in slower reaction times and in a longer than average performance time.6 One test frequently used to assess processing speed is the Trail Making Test, Part A.6 This is a timed sequencing test that requires individuals to draw a line from one number to the next in numeric order. Timed visual scanning tasks, requiring a target letter, number, or symbol to be identified, are also used to assess processing speed.
The processing speed theory proposes that the decline seen in memory and other cognitive processes with normal aging is due, in part, to slow processing speed. It has been estimated that older adults’ response time is approximately 1.5 times slower than that of younger adults.23 It is hypothesized that slower processing speed affects cognition in two ways, the limited time mechanism and the simultaneity mechanism.24 The limited time mechanism occurs when relevant cognitive processes are performed too slowly and therefore cannot be accomplished in the expected time. The simultaneity mechanism occurs when slower processing reduces the amount of information available for later processing to be completed. In other words, relevant information may not be accessible when it is needed because it was not encoded. However, slower processing speed associated with normal aging does not affect an individual’s performance across all tasks. Processing speed has a stronger relationship to tasks of fluid intelligence than crystallized intelligence. Slower processing speed in older adults accounts for the decline in fluid ability (e.g., memory, spatial ability) with aging, but not crystallized ability (e.g., verbal ability).25 Longitudinal data on cognitive performance across the life span have suggested that the decline in processing speed performance begins at an earlier age and progresses at a steeper rate compared to memory functioning, which declines later in life.26
Memory
Memory is commonly thought of as the ability to recall past events and learned information. However, aside from remembering information from the past, memory includes memory for future events (remembering an appointment), autobiographical information, and keeping track of information in the present (e.g., a conversation or reading prose). Memory can be discussed in terms of the complex processes whereby the individual encodes, stores, and retrieves information. Memory can also be divided into the length of time the items have been mentally stored—thus, the distinction between short-term memory and long-term memory. In addition, memory can be organized by the type of material being stored, such as visual or verbal or autobiographical information. Similar to other areas of cognitive functioning, different aspects of memory differ in how they change with aging.
Working Memory (Short-Term Memory)
Working memory or short-term memory is seen as a limited capacity store for retaining information over the short term (seconds to 1 to 2 minutes) and for performing mental operations on the contents.6 Immediate memory, the first stage of short-term memory, temporarily holds information and may also be thought of as one’s immediate attention span. The recognized limited capacity store of approximately seven bits of information27 requires that information is transferred from short-term memory to a more permanent store for later recall. Baddeley and Hitch have proposed a model that divides short-term or working memory into two systems—one phonologic, for processing language (verbal) information, and one visual-spatial, for processing visual information.28–30 This model holds that short-term memory is controlled by a limited capacity attentional system and thus is organized by a so-called central executive. The central executive assigns information to be remembered to the visuospatial sketch pad (for memory of visual and spatial information) or the phonologic loop (for verbal materials). The overall concept is that more specialized storage systems exist in the limited short-term store that distinguish between verbal and visual information to be stored. Through rehearsal in working memory (e.g., repetition), copies of the information are sent for long-term storage. Regardless of the particular memory model, the overall idea is that short-term memory is a temporary holding ground for information that can be processed or encoded into long-term memory.
Working memory is typically assessed by asking an individual to recall or repeat back words, letters, or numbers, often with sequences of varying length. Using this method, short-term memory span shows only a slight age effect.4 However, short-term memory becomes vulnerable to aging when the task becomes more complex and requires mental manipulation. For example, on Wechsler’s subtest, digit span, individuals are presented with progressively longer strings of numbers verbally and are asked to recall immediately digits in a forward order, reverse order, and in sequence from lowest to highest. It is when the task requires more than attention span and individuals have to recall the numbers backward and in sequence, thus manipulating the material, that older adults perform disproportionately weaker than younger adults.4
The issue of how aging affects short-term or working memory is associated with the level of complexity of the particular task and presence of a distracting task. Older adults have been found to have difficulty suppressing irrelevant information from the recent past.31 Difficulties in processing due to changes in inhibitory control result in increased difficulty for selecting relevant information on which to focus in working memory, as well as difficulty in shifting focus while ignoring distracting information.32 Although working memory capacity is an important facet in the process of learning new information, attention and processing speed are inextricably linked to one’s ability to learn. In daily life, older adults perform cognitively best when they focus on one task at a time because attention and processing speed are not divided. Simple memory strategies, such as writing down information or rehearsing information aloud, can help compensate for memory changes as we age. Such mental techniques aid older adults’ ability to move information from short-term to long-term memory. It is important to note that short-term memory decline is part of normal aging, and generally these age-related changes do not affect daily functioning in the disruptive way that the presence of dementia affects daily functioning.
Long-Term Memory
Long-term memory refers to the acquisition of new information that is available for access at a later point in time and involves the processes of encoding, storage, and retrieval of information. Although long-term memory typically means memory for information from the past, it also involves memory for future events or what is termed prospective memory. An example of prospective memory is remembering a future physician’s appointment or remembering to take medication; it requires that a memory be maintained about what must be done before the action takes place. Despite numerous theories about the stages of memory or processing levels, the dual system conceptualization of two long-term memory systems (explicit and implicit) provides a useful model for clinical use to understand patterns of functioning and deficits.4,6,30,33 Explicit memory refers to the intentional recollection of previous experiences; an individual consciously attempts to recall information and events. To assess explicit memory, verbal or visual information (e.g., words or pictures) is presented and, after a delay, the individual is asked to recall the material through simple recall or a recognition task. Implicit memory, on the other hand, relates to knowledge that is observable in performance, but without the awareness that one holds this information. For example, the ability to ride a bicycle does not depend on the conscious awareness of the particular skills involved in the activity.
Explicit Memory.
Explicit memory, often referred to as declarative memory, can further be divided into episodic memory and semantic memory. Episodic memory refers to the ability to recollect everyday experiences.34 More specifically, episodic memory is the conscious recollection of personal events, along with the specific time and place (context) that they occurred. Episodic material includes autobiographical information, such as the birth of a child or graduation from high school, and includes personal information, such as a meal from the previous day or a recent golf game. These are memories that relate to an individual’s own unique experience and include the details of “when and where” an event occurred. Most memory tests assess episodic memory and usually involve a free recall (retrieval), cued recall, and recognition trial and rely on an individual’s ability to recollect the material to which he or she was previously exposed.6 Compared to younger adults, older adults typically perform better on recognition tasks as opposed to recall tasks. Recognition requires less cognitive effort because a target or cue is provided as a prompt to aid recall, as opposed to a recall task, which requires an individual to recall the material to which she or he was previously exposed, without any prompt. Overall, older adults are most disadvantaged when tests use explicit memory, in particular episodic memory, compared to younger adults.35,36
Semantic memory is an individual’s knowledge about the world and includes memory of the meanings of words (vocabulary), facts, and concepts and, contrary to episodic memory, is not context-dependent. Knowledge is remembered regardless of when and where it was learned, such as word definitions or knowing the years when WWII occurred. Tests that assess semantic memory include vocabulary and word identification tests (e.g., AMNART),9 category fluency tasks (e.g., Animal Naming Test),37 and confrontational or object naming tests (e.g., Boston Naming Test).38 When most older adults report memory complaints, they are often referring to their difficulty in remembering words and names of objects and people.39
Tests that require recall of semantically unrelated material, such as the Rey Auditory-Verbal Learning Test (RAVLT)40 word lists, are seen as more difficult because they require more effortful strategies for encoding and retrieval than story recall tests, such as Wechsler’s Logical Memory (WMS-IV, Logical Memory)41 or semantically related word lists, such as the California Verbal Learning Test (CVLT-II).42 When information is presented in a context, or words on a list belong to a category and are semantically related, the material presented is already organized in a meaningful way, which aids the recall processes. These memory tests include delayed recall and recognition trials to discern whether a deficit relates to the storage rather than retrieval of information.4