Compromised naturalistic action performance in amnestic mild cognitive impairment.

Neuropsychology 2015, Vol. 29, No. 2, 320 –333

© 2014 American Psychological Association 0894-4105/15/$12.00 http://dx.doi.org/10.1037/neu0000132

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Compromised Naturalistic Action Performance in Amnestic Mild Cognitive Impairment David A. Gold and Norman W. Park

Angela K. Troyer and Kelly J. Murphy

York University

Baycrest Health Sciences, Toronto, Ontario, Canada and University of Toronto

Objective: Routine naturalistic actions (NAs) are familiar activities that require the production of several actions in a particular order to achieve a specific goal, such as preparing a meal or paying bills. Given that amnestic mild cognitive impairment (aMCI) has been shown to be a risk factor for dementia, a better understanding of the cognitive processes that mediate NA performance is needed in order to facilitate efforts to promote functional autonomy in this population. Method: Performance of 2 highly familiar NAs, and their relationship to measures of episodic memory, semantic knowledge, and executive function was systematically investigated in a sample of healthy older adults (n ⫽ 24) and individuals with aMCI (n ⫽ 24). Results: In general, measures of executive function were related to commission errors, while episodic memory was associated with the omission of supporting actions. However, both errors of omission and commission appeared to draw on a diverse array of cognitive processes. Conclusions: The findings provide preliminary evidence that the cognitive correlates of NA errors may not be as process pure as previously hypothesized in neuropsychological models. A more comprehensive understanding of the cognitive underpinnings of NAs in aMCI could lead to more effective intervention programs to promote functional autonomy and delay dementia onset. Furthermore, NAs may be administered in neurocognitive assessments to identify early changes in everyday functioning and facilitate differential diagnosis between healthy aging and aMCI. Keywords: naturalistic action, cognitive theories of action, instrumental activities of daily living (IADL), amnestic mild cognitive impairment (aMCI), everyday activity performance Supplemental materials: http://dx.doi.org/10.1037/neu0000132.supp

Naturalistic actions are goal-directed activities involving the use and manipulation of objects and tools that require the production of several actions in a particular order to achieve a specific goal. Routine naturalistic action (NA) tasks are familiar activities of daily living that an individual performs such as preparing a cup of tea or wrapping a present (e.g., Schwartz, Segal, Veramonti, Ferraro, & Buxbaum, 2002). Relative to other areas of investigation, there is a paucity of research into the cognitive neuropsychology of goal-directed, multistep activities that individuals perform in the real world (Bettcher & Giovannetti, 2009). Although it is chal-

lenging to study naturalistic tasks in a laboratory setting, doing so represents an important endeavor for researchers to better understand the cognitive processes that underscore everyday activities. Of particular interest to the current study are individuals with amnestic subtypes of mild cognitive impairment (aMCI) because they provide an ideal opportunity to investigate the role of mild memory impairment, and other areas of relative cognitive weakness, in NA performance. As a transition point between healthy aging and dementia of the Alzheimer’s type (DAT; Albert et al., 2011), a better understanding of the cognitive underpinnings of NAs in aMCI could lead to the development of targeted interventions that promote independence in activities of daily living.

This article was published Online First August 25, 2014. David A. Gold and Norman W. Park, Department of Psychology, York University; Angela K. Troyer and Kelly J. Murphy, Neuropsychology and Cognitive Health Program, Baycrest Health Sciences, Toronto, Ontario, Canada and Department of Psychology, University of Toronto. This research was conducted in partial fulfillment of the requirements for David A. Gold’s doctoral degree and was supported in part by the Canadian Institute of Health Research, Natural Sciences and Engineering Research Council, and an Ontario Graduate Scholarship Doctoral Award. The authors thank the anonymous reviewers for their thoughtful suggestions on earlier versions of the manuscript. Correspondence concerning this article should be addressed to David A. Gold, who is now at the Krembil Neuroscience Centre, University Health Network, Neuropsychology Clinic, 4F-409, 399 Bathurst St., Toronto ON M5T 2S8. E-mail: [email protected]

The Centrality of Action Most cognitive theories of NA predict that these activities are represented hierarchically in memory (e.g., Cooper, Schwartz, Yule, & Shallice, 2005). There are a series of nested subgoals below the schema for the highest-level goal of the task that must be carried out in order to complete the task. For example, in the NA task of preparing to send a card (the card preparation task) one of the subgoals is signing the card with a pen. The achievement of the central action of signing the card is accomplished by the supporting actions of taking the pen (a) and card (b), moving the pen toward the card (c), and relinquishing the pen after signing the card (d) to prepare for the achievement of the next subgoal. As this example indicates, crux (central) actions tend to alter the state of an object by 320

NATURALISTIC ACTIONS

interacting with other objects, and have numerous associations with noncrux (supporting) actions (Schwartz, Reed, Montgomery, Palmer, & Mayer, 1991). In contrast, noncrux actions tend to enable or facilitate the completion of a crux, and involve a single action (take, move, give) or object. Analyzing NAs with this level of detail allows us to address specific hypotheses about the cognitive underpinnings of central and supporting actions, and how that may change with age or neurological damage.


The Cognitive Neuropsychology of Naturalistic Actions NA errors are commonly conceptualized as actions of omission (actions that were not performed) and commission (actions that were performed in error by virtue of improper sequencing of steps, misuse or substitution of tools or gestures, and imprecise execution of steps). Recent research has focused on the relationship between neuropsychological deficits and particular error patterns in order to enhance our understanding of the cognitive underpinnings of NA performance and generate theories to explain disruptions in NA performance (see Giovannetti et al., 2012; Hartmann, Goldenberg, Daumüller, & Hermsdörfer, 2005; Schwartz, 2006).

Executive Function and NA Case studies of patients with traumatic brain injury (TBI), or vascular events have revealed that anterior lesions are associated with inefficient performance of NAs, characterized by errors in the ordering of actions, substituting objects for one another, and perseverative loops (Schwartz et al., 1991). Group studies have also supported the relationship between frontal lobe damage and inefficient NA performance (Goldenberg, Hartmann-Schmid, Sürer, Daumüller, & Hermsdörfer, 2007; Schwartz, Montgomery et al., 1998). More recent research with DAT (Giovannetti, Bettcher, Brennan, Libon, Kessler, et al., 2008), vascular dementia (Giovannetti, Schmidt, Gallo, Sestito, & Libon, 2006), schizophrenia (Kessler, Giovannetti, & MacMullen, 2007), and Parkinson’s disease (Giovannetti et al., 2012) indicates that commission errors may be more closely predicted by performance on executive function tasks than memory measures. Despite the observed relationship between executive function and commission errors, questions remain about the predicted error profile from deficits in executive function. For example, individuals with TBI also enact significantly more omission errors than controls, suggesting that impairments in executive function can result in a failure to perform a task, and not just imprecise execution of the task (Schwartz, Montgomery et al., 1998). Executive function, as well as general cognitive function, may play a role in commission errors (Giovannetti et al., 2012). These findings suggest that processes beyond executive function may lead to commission errors.

Semantic Knowledge and NA Various forms of apraxia and left-hemisphere damage can give rise to impairments in NA enactment by disrupting the knowledge for how to enact a NA, or by degrading the relationship between objects and actions (Hartmann et al., 2005). From an information processing perspective, impaired access to action schema, or a disruption in how schemas activate stored knowledge about the

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target objects could cause a breakdown in NA enactment (Cooper et al., 2005). Some evidence implicates semantic knowledge in the breakdown of NA. Giovannetti, Libon, Buxbaum, and Schwartz (2002) found a relationship between NA errors and a measure of semantic knowledge for tool properties in a sample of mixed dementia patients. Thus, it may be necessary to assess specific elements of the semantic properties of NAs, as opposed to other types of semantic knowledge, to better predict subsequent NA performance (Buxbaum, Veramonti, & Schwartz, 2000; Giovannetti et al., 2002). Nonetheless, the relationship between semantic knowledge and NA errors is not straightforward. For example, individuals with semantic deficits following left-hemisphere stroke enacted similar NA errors as right-hemisphere stroke patients (Buxbaum, Schwartz, & Montgomery, 1998), suggesting that impairments in semantic knowledge may manifest in different types of errors in NA enactment, such as omissions or commissions.

Episodic Memory and NA Episodic memory refers to memory for particular episodes that an individual has previously experienced that are anchored to a particular time and place (Tulving, 2002). Episodic memory may support a more detailed representation of an event, whereas semantic memory may support a more gist-like representation (Moscovitch et al., 2005). Memory for events decay over time, with more precipitous loss of the details or supporting action steps than central actions (Brewer & Dupree, 1983). Rusted and Sheppard (2002) investigated longitudinal changes in a tea-preparation NA task with a sample of patients with DAT and controls. At the beginning of the study, idiosyncratic teamaking routines were identified for each participant and periodically compared to their performance up to 6 years later. Relative to controls, individuals with DAT showed a selective increase in their omission of actions. Well into the course of DAT, memory for the most central actions was relatively better preserved than the supporting actions. However, this important longitudinal investigation did not address the relative role of other cognitive processes that decline in DAT, such as semantic knowledge and executive function. Others have found that individuals with DAT had a higher proportion of omission errors than individuals with other types of dementia involving subcortical vascular pathology (Giovannetti et al., 2006) or Parkinson’s disease (Giovannetti et al., 2012). Measures of episodic memory are consistently associated with omissions in various neurodegenerative and psychiatric populations (e.g., Giovannetti et al., 2006, 2012; Kessler et al., 2007). Although the bulk of evidence supports a relationship between episodic memory and omissions, a recent investigation found that episodic memory was not uniquely predictive of omission errors, but was instead related to the total numbers of errors enacted in a heterogeneous sample of MCI (Seligman, Giovannetti, Sestito, & Libon, 2014). Thus, episodic memory may have a broader role in NA action errors.

Models of NA Errors Schwartz and colleagues concluded that it is not a specific deficit related to a cognitive process or region of the brain that underlies NA breakdown, but rather a general functional deficit; errors are the result of cognitive resources being overwhelmed by

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the demands of the task (Buxbaum et al., 1998; Giovannetti et al., 2002; Schwartz, Montgomery et al., 1998; Schwartz, Buxbaum et al., 1998). Another hypothesis is that different neuropsychological deficits can result in similar patterns of NA errors (Buxbaum et al., 1998) or accomplishment performance (Hartmann et al., 2005). Giovannetti and colleagues (2012) proposed a neuropsychological model of NA error (the Omission-Commission Model) that summarizes the consistent error profiles in their research. According to this model, omission errors are associated with deficits in episodic memory or task knowledge. In contrast, commission errors are associated with executive control processes such as working memory.

MCI and NA Individuals with MCI show subtle decrements across a range of measures of everyday functioning (Griffith et al., 2003; SchmitterEdgecombe, McAlister, & Weakley, 2012; Seelye, SchmitterEdgecombe, Cook, & Crandall, 2013). Individuals with MCI (including single and multidomain, amnestic and nonamnestic MCI subtypes) perform NAs more efficiently than individuals with DAT, though not as well as controls (Giovannetti, Bettcher, Brennan, Libon, Burke, et al., 2008). In particular, MCI individuals made relatively more commission than omission errors compared to the more evenly distributed pattern of omission and commission errors seen with a DAT group. The authors concluded that individuals with MCI have preserved semantic memory for NAs, but difficulty implementing task knowledge in the smooth execution of action steps (Giovannetti, Bettcher, Brennan, Libon, Burke, et al., 2008). Relationships between cognitive measures and NA errors were not examined in this investigation. Thus, we do not know if subtle semantic memory impairments or other cognitive weaknesses may be contributing to NA errors in MCI groups. A follow-up study with a similar MCI group did not find unique relationships between cognitive measures and errors of omission or commission (Seligman et al., 2014). This finding did not support the Omission-Commission Model of NAs, and the authors concluded that it may have been due to low error rates in MCI groups. The cognitive underpinnings of the inefficient NA enactment in MCI populations remain unclear.

Current Study The cognitive processes associated with NA error patterns in healthy older adults and aMCI individuals have not been previously investigated. Because individuals with aMCI have mildly impaired episodic memory, as well as weaker semantic knowledge (Murphy, Rich, & Troyer, 2006) and executive function (Brandt et al., 2009), the relative role of these cognitive processes in NA performance can be better understood within the same population. In general, the relative role of executive function, semantic knowledge, and episodic memory in NA errors has not been elucidated. The literature reviewed suggests that NAs draw on the integrity of a diverse range of cognitive processes beyond the demonstrated associations between episodic memory and errors of omissions, and executive function and errors of commissions. The complexity of the relationship between cognitive processes and error categories may explain some of the inconsistency in the literature. For instance, omissions and commissions may be associated with

similar cognitive processes, but these errors may differentially recruit unique cognitive substrates. Are the cognitive substrates of NA errors less process-pure (Jacoby, 1991) than previously believed (Giovannetti et al., 2012)? To evaluate this question and assess the predictions of NA models, we used a regression analysis approach to explore if composite cognitive measures could predict unique variability over and above their mutual contribution to errors of omission and commission. The current study sought to investigate the nature of NA performance in an aMCI population using a detailed system of scoring (Gold & Park, 2009) that analyzes NA performance as a function of the centrality of actions (crux and noncrux). In her earlier work, Schwartz and colleagues (1991) examined actions as a function of centrality, but this approach has not been applied in the group studies described thereafter (e.g., Schwartz, Montgomery et al., 1998). Models of NA errors have not addressed the centrality of action. We chose to examine the crux and noncrux actions structure in NAs to address hypotheses about the memory representation for NAs. Previous research indicates that individuals with medial temporal lobe (MTL) damage, such as those with aMCI, show greater impairment in memory for autobiographical details relative to gist information (e.g., Murphy, Troyer, Levine, & Moscovitch, 2008). Other findings also implicate MTL structures in retrieving past events as well as envisioning details of future events (Addis, Sacchetti, Ally, Budson, & Schacter, 2009). We hypothesized that the episodic representation of a NA corresponded with some of the detailed elements of the central goal structure of the NA, but more strongly with the detailed supporting elements of action that are not subserved by semantic memory. These detailed elements may underlie the specific order and execution of noncrux actions, the associations between crux and noncrux actions within a subgoal, and aspects of crux action that must be retrieved from memory in order to enact a NA efficiently. As such, we hypothesized that episodic memory weakness could lead to errors of omission or commission (Gold & Park, 2009). For instance, in the card preparation task, the crux action of signing the card may be omitted due to a failure to retrieve that step from memory or difficulties sequencing the task. Thus, we did not anticipate that individuals with aMCI would experience a selective decline in noncrux actions, but rather a subtle decline in the detailed aspects of both crux and noncrux action because their hierarchical representation for NAs would be intact. We hypothesized that episodic memory would contribute unique variability in the prediction of noncrux omissions, over and above the contribution of semantic knowledge and executive function. If the central elements of these well-practiced NAs have more of a gist-like representation, we predicted that crux omissions would be associated with semantic knowledge as well as episodic memory. Consistent with previous findings, we hypothesized that executive function would uniquely predict both crux and noncrux commission errors, but that episodic memory would also be related to errors of commission. We anticipated that the aMCI group would show a relative balance between errors of omission and commission, consistent with the profile found in DAT. We predicted that individuals with aMCI would accomplish fewer crux and noncrux actions than healthy controls due to decrements in episodic memory, together with mild weaknesses in semantic memory and executive function.


Method


Participants and Group Assignment Individuals with memory complaints were recruited from the Memory Intervention Program at Baycrest Centre for Geriatric Care, community talks, and advertisements. The control group was recruited from the Baycrest Volunteer Participant Database, community talks, and advertisements. Interested individuals were contacted by telephone for a health and memory interview. The 48 participants were required to meet the study criteria listed subsequently, as determined by consensus opinion of two clinical neuropsychologists (AT and KM) reviewing the cognitive test results from the diagnostic battery together with clinical history (see Figure 1 for a flow of the participants through the study criteria). Fluency in English. Participants were required to be relatively fluent in their comprehension of English as assessed by

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self-report on a 7-point Likert-type scale (must be at least highly fluent, 6 out of 7) and from clinical impressions during interview. No apraxia. Given that participants would be enacting NAs, they were required to perform within normal limits (20/20) on an apraxia screening test (Almeida, Black, & Roy, 2002). Participants had to: a) pantomime five transitive gestures (tool-based; e.g., show me how to brush your hair with a comb); b) five intransitive gestures (communication-based; e.g., show me how to wave to someone); and c) perform delayed imitation of another five transitive and five intransitive gestures without error. Visual ability. Participants were required to have a relatively intact ability to perceive objects in the visual-spatial domain, as defined by performance within normal limits (⬎16/20) on the perceptual screen and incomplete letters subtests of the Visual Object and Spatial Perception battery (VOSP; Warrington & James, 1991).

Participants Screened for Study (n = 66) Fluency in English? (2 participants who rated themselves as highly fluent in English were excluded from the study because English was not their first language and performance on the verbal measures in the diagnostic battery was > 2 SD lower than performance on non-verbal measures)

No Apraxia? Intact Visual Ability? Medical Psychiatric Criteria? (3 participants removed for elevated depression or anxiety on HADS)

Subjective Cognitive Complaint? (n = 34)

No Subjective Cognitive Complaint? (n = 27)

Diagnostic Cognitive Battery (3 participants excluded for scoring significantly below expected performance on one or more of the measures)

Control Group (n =24) Objective Memory Impairment? (4 participants excluded because they scored below age and education corrected normative scores on only one out of the three memory measures, and 1 participant was excluded for showing a cognitive profile more consistent with non-amnestic MCI)

Normal General Cognitive Status? (3 participants were removed for having global cognitive decline)

Largely Intact Functional Activities? (2 participants were removed for no longer having relatively intact IADL) No Dementia? Cognitive Complaint Not Better Explained by Medical Condition? aMCI (n = 24; aMCIsd if only memory impaired, n = 10, aMCImd if one or more cognitive domains also below expected, n = 14) Figure 1.

Summary of the flow of participants through the study.

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Medical/psychiatric criteria. Participants were excluded if they had a history of conditions that could affect cognition (e.g., TBI, metabolic disorders, autoimmune conditions, cardio/cerebrovascular disease, neurological conditions, etc.), including previous drug or alcohol abuse, medication use that can significantly alter cognition, or current elevated anxiety or depression as defined by a score greater than seven on either the depression or anxiety subscales of the Hospital Anxiety and Depression Scale (HADS; Zigmond & Snaith, 1983).


Diagnostic Cognitive Battery To classify potential participants as MCI or control, the following cognitive domains were assessed: (a) general cognitive functioning (Mini Mental Status Exam, MMSE; Folstein, Folstein, & McHugh, 1975); (b) estimated verbal IQ (Wechsler Adult Intelligence Scale III, WAIS-III Vocabulary; Wechsler, 1997); (c) simple attention and working memory (WAIS-III Digit Span Forward & Backward; Wechsler, 1997); (d) graphomotor processing speed (Delis-Kaplan Executive Function System, DKEFS Trail Making Test Number Sequencing; Delis, Kaplan, & Kramer, 2001); (e) complex attention (DKEFS Trail Making Test Number-Letter Switching; Delis et al., 2001); (f) visuospatial construction (ReyOsterrieth Complex Figure, ROCF Copy; Spreen & Strauss, 1998); (g) confrontation naming (Boston Naming Test, BNT; Kaplan, Goodglass, & Weintraub, 1983); (h) list learning and retention (Hopkins Verbal Learning Test—Revised, HVLT-R; Brandt & Benedict, 2001); (i) immediate and delayed recall of a story (Logical Memory I and II; Wechsler, 1987); and (j) immediate incidental recall of a complex figure (ROCF Immediate Recall; Spreen & Strauss, 1998).

Diagnostic Criteria for aMCI Petersen (2004) criteria for aMCI were adopted for group classification, consistent with previous investigations in this clinic (Murphy et al., 2008; Troyer et al., 2008) and the most recent diagnostic criteria (Albert et al., 2011). Subjective memory/cognitive complaint. Participants were required to have a self-reported change in cognitive functioning, corroborated by an informant (only one individual did not have an informant that could corroborate memory decline). As determined by interview, the memory decline had to be gradual (as opposed to sudden), stable (as opposed to fluctuating), and at least 6 months in duration. The clinical history was carefully reviewed in conjunction with test results from the diagnostic cognitive battery to ensure that psychiatric or medical conditions (other than possible incipient Alzheimer’s disease) did not account for the memory decline. Objective memory impairment for age. Memory impairment was defined as obtaining scores on at least two of the three memory measures (HVLT-R, Logical Memory, ROCF immediate recall) that were considerably lower than expected based on age, education, and estimated verbal IQ (WAIS-III Vocabulary). The relative deficit in memory was also considered in light of other areas of cognition assessed, such as simple attention, working memory, and processing speed to ensure that other more rudimentary cognitive weaknesses could not better explain the relative memory impairment. A specific cut-off score was not implemented

in order to accommodate intraindividual variability and clinical judgment (Petersen, 2004). On average, participants in the aMCI group fell more than two SDs below their mean estimated verbal IQ on the indices of memory (see Table 1). In addition, the aMCI group scored significantly lower on the memory measures than the controls. Normal general cognitive status for age and education. Participants did not show decrements across all cognitive domains assessed. This judgment was made based on the MMSE score, as well as overall performance on the diagnostic cognitive battery relative to age, education, vocational history, and health status. Largely intact functional activities. Participants had intact basic activities of daily living and generally intact IADLs as assessed by self-report and informant-ratings for all but one individual who lived independently in the community, but did not have an informant available (Lawton & Brody, 1969). No dementia. Participants did not meet established criteria for dementia (American Psychiatric Association, 2000). By definition, all aMCI participants showed impairment in the memory domain. Ten of these participants did not show impairment in any other domain (i.e., had single-domain aMCI; aMCIsd), and 14 participants had additional mild impairments in either visuospatial, language, or executive domains (i.e., had multipledomain aMCI; aMCImd). Because no a priori hypotheses were made about the role of additional areas of cognitive decline in aMCI, and the small sample size precluded any meaningful comparisons, the single- and multiple-domain aMCI groups were not examined separately.

Control Group Control participants (n ⫽ 24) performed within the expected range based on age and education corrected published normative data for all measures in the diagnostic cognitive battery, and were independent in their daily functioning as assessed by LawtonBrody IADL items during interview.

Materials NAs. The NA tasks consisted of preparing: a sandwich, coffee using a drip filter machine, and a card to be mailed. NA performance was measured using an adaptation of the Action Coding System (ACS; Schwartz et al., 1991), which categorized actions as crux or noncrux (Gold & Park, 2009; Park et al., 2012). Consistent with previous research (Giovannetti et al., 2002), errors were classified at the level of type (omission, reversal, perseveration, object substitution, gesture substitution, grasp-spatial misestimation, tool omission, quality, and action addition). These error types comprised the broader measure of the rates of omission (any action that was not attempted) and commission (any error committed excluding omissions and action additions). Scoring of the NAs was developed through pilot testing of the tasks to determine the most frequent pattern of enacting the NAs (Park et al., 2012), consistent with the approach of others (Joe, Ferraro, & Schwartz, 2002). Scoring protocols, listing the crux and noncrux actions for each NA, were developed by having three or more researchers independently view the task analyses (NAs) to identify the crux and noncrux actions involved in each task (for more details see Park et al., 2012). The crux and noncrux designations


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Table 1 Demographic and Descriptive Cognitive Information for Sample Group


Control (n ⫽ 24)

Age (range) Education (years) Gender (F:M) MMSEⴱ HADS Anxiety HADS Depression VOSP Screen VOSP Letters WAIS-III Vocabulary age SS WAIS-III Digit Span age SS ROCF Copy age SSⴱ ROCF Immediate Recall age SSⴱ HVLT-R Total (trials 1–3) age SSⴱ HVLT-R Delay Recall age SSⴱ WMS-R LM Immediate Recall age SSⴱ WMS-R LM Delay Recall age SSⴱ DKEFS Trails Number age SSⴱ DKEFS Trails Switch age SSⴱ BNT Total age SSⴱ

aMCI (n ⫽ 24)

Effect size

M

SD

M

SD

77.04 (66–87) 15.79 13:11 29.29 4.42 2.83 19.92 19.54 15.42 12.63 10.25 11.67 12.00 11.71 13.21 13.17 13.08 13.50 13.25

4.42 3.78

78.08 (67–88) 15.33 11:13 27.92 3.83 2.36 19.92 19.50 14.71 12.00 7.35 5.92 6.38 4.50 7.52 7.87 10.42 10.79 10.46

6.06 3.76

0.75 2.59 1.79 0.28 0.78 2.69 2.92 3.14 3.00 1.89 2.03 2.41 2.35 2.30 0.98 3.21

1.64 2.53 1.45 0.28 0.83 2.76 2.93 2.47 2.02 2.30 2.75 2.73 2.93 3.05 3.53 3.41

d

1.07 0.23 0.29 0.00 0.05 0.26 0.22 1.03 2.25 2.67 2.96 2.21 2.00 0.98 1.05 0.84

Note. aMCI ⫽ amnestic mild cognitive impairment; age SS ⫽ age corrected scaled score; MMSE ⫽ Mini Mental Status Exam; HADS ⫽ Hospital Anxiety and Depression Scale; VOSP ⫽ Visual Object and Space Perception Battery; WAIS-III ⫽ Wechsler Adult Intelligence Scale-III; ROCF ⫽ Rey-Osterrieth Complex Figure Test; HVLT-R ⫽ Hopkins Verbal Learning Test-Revised; WMS-R LM ⫽ Wechsler Memory Scale-Revised Logical Memory Subtest; D-KEFS ⫽ Delis-Kaplan Executive Function System; and BNT ⫽ Boston Naming Test. ⴱ Significant difference between control and aMCI group (p ⬍ .003).

from each reviewer were compared, and any discrepancies were reexamined until agreement was reached. The three NAs used in our study had an average of 15.67 (SD ⫽ 4.50) crux actions and 42.67 (SD ⫽ 8.50) noncrux actions. Each NA had an average of 6.33 (SD ⫽ 1.53) tools/items present, and 3.33 (SD ⫽ 0.58) distracter objects present that were either physically similar to a target object (a spatula instead of a fork) or semantically similar (tape for a stapler).

Cognitive measures not used in the diagnosis of aMCI. Descriptive performance on the composite measures of executive function, semantic knowledge, and episodic memory is summarized in Table 2. Executive function. DKEFS tower test. This test assesses planning and problemsolving abilities, as well as strategy formation, inhibition, and monitoring (Delis et al., 2001). The measure of interest was the

Table 2 Cognitive Measures Not Used in the Diagnosis of AMCI Group Control (n ⫽ 24) Composite variable Memory

Semantic knowledge Executive function

Test ⴱ

BVMT-R Item score BVMT-R Associative scoreⴱ Word-Word Item score Word-Word Associative score DKEFS Category Fluencyⴱ Function subtest Manipulation subtest DKEFS Phonemic Fluency DKEFS Tower Achievement Score ROCF Q score

aMCI (n ⫽ 24)

Effect size

M

SD

M

SD

d

12.67 20.17 61.63 39.57 38.17 18.54 11.45 43.54 18.37 11.92

4.17 3.53 26.72 28.82 6.90 .97 1.74 8.53 4.76 4.31

6.25 10.79 56.04 23.17 29.67 18.20 10.08 41.50 15.38 10.92

3.14 5.81 28.67 21.29 8.13 1.14 2.16 10.62 4.29 4.58

1.74 1.95 0.20 0.65 1.13 0.32 0.70 0.21 0.66 0.22

Note. aMCI ⫽ amnestic mild cognitive impairment; BVMT-R ⫽ Brief Visual Memory Test-Revised, trials 1– 4 item and associative memory score (Troyer et al., 2008); Word-Word ⫽ Word-word association task item and associative memory score (Troyer et al., 2011); D-KEFS ⫽ Delis-Kaplan Executive Function System (Delis et al., 2001); Function-Manipulation Triplets Test (Buxbaum & Saffran, 2002); ROCF Q score ⫽ Rey-Osterrieth Complex Figure Test Q score (Bylsma et al., 1997). ⴱ Significant difference between control and aMCI group (p ⬍ .005).


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Achievement Score—the number of moves used to achieve the modeled tower. DKEFS phonemic fluency. This test has been shown to be a measure of executive function because generating words on the basis of lexical representations is unusual, relying on the generation of strategies, efficient organization of verbal retrieval, selfmonitoring, and inhibition (for a review see Henry & Crawford, 2004). Raw scores were reported consistent with standardized administration. ROCF Q score. This measure was designed to capture the strategic approach to copying a complex figure (Bylsma, Carison, Schretlen, Zonderman, & Resnick, 1997). The most strategic approach is to perceive the complex figure as comprised of a number of discrete units, and copy it accordingly (for reviews see Spreen & Strauss, 1998; Troyer & Wishart, 1997). The total units and order were summed to yield a score out of 24, consistent with standardized scoring protocols (Bylsma et al., 1997). Semantic knowledge. DKEFS category fluency. Category fluency has been demonstrated to draw on permanent semantic representations of objects, facts, and other concepts such as words and their meaning (Henry & Crawford, 2004). Raw scores were reported consistent with standardized administration. Function–Manipulation Triplets Test. To assess memory for the semantics of action, the Function–Manipulation Triplets Test was used (Buxbaum & Saffran, 2002). In this test, a series of 20 word triplets of common objects such as shower, oven, and dishwasher were presented. In the first condition participants were asked to identify the two objects that were most similar in function (shower and dishwasher). In the second condition, 14 word triplets were presented serially, and participants were asked to identify the two objects that were most similar in how the objects were manipulated (oven and dishwasher). Raw scores reflected the total questions answered correctly for the function subtest and manipulation subtest. Episodic memory. BVMT-R item and associative memory score. Memory for six geometric figures and their locations was assessed over three learning trials and a delayed recall trial through standard administration of the BVMT-R (Benedict, 1997). Each trial was scored separately for item memory (i.e., the total number of accurately drawn figures), and associative memory (i.e., the total number of recognizable figures produced in the correct location; see Troyer et al., 2008 for detailed procedure). Word-word association task. This test was designed to compare item versus associative memory using verbal stimuli (for details see Troyer, D’Souza, Vandermorris, & Murphy, 2011). Briefly, 48 semantically unrelated word pairs were presented individually at study on a computer screen twice. At test, participants were instructed to discriminate between pairs that were previously presented (i.e., intact pairs) and those that were not (i.e., recombined or new pairs). Associative memory was calculated as the proportion of endorsed intact pairs minus endorsed recombined pairs. Item memory was the proportion of endorsed recombined items divided by one minus the associative memory score (Troyer et al., 2011).

Procedure The institutional review boards of York University and Baycrest Centre for Geriatric Care approved this study, and all participants provided informed consent. Participants were tested individually either in a quiet testing room at Baycrest or in their home, based on their preference. All participants completed the diagnostic neuropsychology battery and experimental cognitive tests during the first hour and a half of the testing session. Rest breaks were offered. In the last 30 minutes, participants performed the NAs, counterbalanced for order of presentation. Participants completed a familiarity questionnaire to ensure that the activities were routine. Criteria for familiarity required that the participant perform the activity weekly and at least 48 times per year. Of the three potential NAs (preparing coffee, a card, or a sandwich) two were selected for enactment based on the greatest familiarity for each participant, and these were counterbalanced for order of presentation. All participants met criteria for completing the task of preparing a card (n ⫽ 48), whereas there was a relatively even split in the natural frequency of preparing coffee (n ⫽ 22) or a sandwich (n ⫽ 26). The presentation of the materials for each NA was standardized, with an equal number of target objects and distracters placed to the participant’s right and left side from a seated position. Participants were instructed that “all the materials you need to complete the task are in front of you, but there may be some additional materials that you do not need to complete the task. Please try to enact the task to the best of your abilities.” For the card preparation task, participants were instructed to “mail a letter to your friend John Doe, thanking him for inviting you to a party.” For the coffee preparation task, participants were asked to “make a cup of coffee in the same way you normally would.” For the sandwich preparation task, participants were instructed to “prepare a sandwich with cold-cuts and mustard.”

Primary Dependent Variables NA enactment. An accomplishment score was derived, representing either the total crux or noncrux actions completed correctly, divided by the total number of crux or noncrux actions in either of the two NA protocols that an individual performed (proportions were used in all calculations to adjust for the different number of crux and noncrux actions in each of the tasks). The omission or commission rate represented the total number of omission or commission errors of an action type (separately for crux and noncrux), divided by the total number of crux or noncrux actions in either of the two NA protocols that an individual performed.

Statistical Analyses The data was approximately normally distributed and fulfilled requirements for analyses of variance (ANOVA). The alpha level was set at 0.05, with a pairwise Bonferroni-adjusted error rate for multiple comparisons. The study was adequately powered to detect small to medium main effects (f2 ⫽ .13) and interactions (f2 ⫽ .17). Approach to multiple regression. Consistent with other approaches (Giovannetti et al., 2012; Tan, Hultsch, & Strauss, 2009),



raw scores on the experimental executive function, semantic knowledge, and memory measures were collapsed across group and converted into z-scores and then averaged, yielding composite scores in the cognitive domains of executive function, semantic knowledge, and episodic memory. The standardized composite cognitive variables were entered simultaneously into the regression in the first block of Model 1. Group and interaction terms of group were entered simultaneously in the next block to determine if the groups differed in their relationship with any of the cognitive predictors and to explore the interactive effect on the dependent variables (omission and commission rate). If Model 2 contributed significant variability over and above Model 1, the significant interaction terms were examined separately by group to interpret: (a) the differential effects of the cognitive composite variables on the predicted dependent variables, and (b) the unique variance of a composite predictor variable over and above the variability accounted for by the composite variables together (Aiken & West, 1991). The regression analyses were adequately powered to detect effects in the medium range (.21–24), and in the medium to large range (.34) for interactions. Second order part correlations (ra(b.c)) were used to assess the unique variability that a predictor variable contributed, removing the shared variability with the other two composite variables. This approach was chosen in order to control for the potential overestimation of the beta coefficient weights caused by the influence of multicollinearity on multiple regressions with interaction terms (Tabachnick & Fidell, 2006). As predicted, and shown in the intercorrelation matrix (see Table 3), the predictor variables were often moderately correlated with one another. A summary of the regression models can be found in Table 4, and a summary of the regression coefficients can be found in the online supplemental materials (Tables S1-S5).

Results Sample Characteristics Sample characteristics and performance on the diagnostic cognitive battery for the aMCI and healthy control groups are summarized in Table 1. As shown, the groups did not differ on any of the demographic variables, measures of mood (HADS), visual perception (VOSP), estimated verbal IQ (WAIS-III Vocabulary), or simple attention (WAIS-III Digit Span). The groups differed in terms of general cognitive functioning (MMSE, though both groups were still within normative cut-off score for intact general cognitive functioning), constructional praxis (ROCF Copy), graphomotor processing speed and sequencing (DKEFS Number

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and Switching), and confrontation naming (BNT), with the largest effect sizes in measures of verbal and visual learning and retention (ROCF Immediate Recall, HVLT-R, and WMS-R). No differences were found in NA performance by task (coffee, card, sandwich), place of testing (home or Baycrest), or any of the interactions of these terms by group (all p values ⬎ .196, ␩p2 ⬍ .05).

Interrater Reliability Interrater reliability was assessed using an independent rater who scored 30% of the NAs (see Gold & Park, 2009). Analyses were conducted on the primary independent measures using a two-way mixed-model intraclass correlation coefficient (ICC; Shrout & Fleiss, 1979). The ICC for the accomplishment score was 0.95 for crux actions, F(35, 35) ⫽ 23.65, p ⬍ .001, and 0.91 for noncrux actions, F(35, 35) ⫽ 19.51, p ⬍ .001. The ICC for the omission rate was 0.92 for crux actions, F(35, 35) ⫽ 21.91, p ⬍ .001, and 0.91 for noncrux actions, F(35, 35) ⫽ 19.78, p ⬍ .001. Finally, the ICC for the commission rate was 0.95 for crux actions, F(35, 35) ⫽ 24.33, p ⬍ .001, and 0.92 for noncrux actions, F(35, 35) ⫽ 20.68, p ⬍ .001.

Accomplishment Performance To evaluate the accomplishment score (shown in Figure 2), a mixed-design ANOVA with the between-subjects factor of group (aMCI, control) and the within-subjects factor of action type (crux, noncrux) was conducted. There was a significant within-subjects effect of action type, F(1, 46) ⫽ 95.62, p ⬍ .001, ␩p2 ⫽ .68, whereby more crux actions (M ⫽ 89%, SE ⫽ 1.13) were accomplished than noncrux actions (M ⫽ 81%, SE ⫽ 1.34), but no group by action interaction, F(1, 46) ⬍ 1, p ⫽ .822, ␩p2 ⫽ .001. There was a significant main effect of group F(1, 46) ⫽ 15.86, p ⬍ .001, ␩p2 ⫽ .26. The aMCI group (M ⫽ 84%, SE ⫽ 2.08) accomplished significantly less crux actions than the control group (M ⫽ 94%, SE ⫽ 0.87), t(46) ⫽ 4.20, p ⬍ .001, d ⫽ 1.21. The aMCI group (M ⫽ 77%, SE ⫽ 0.87) also accomplished less noncrux actions compared to the controls (M ⫽ 86%, SE ⫽ 1.46), t(46) ⫽ 3.41, p ⫽ .001, d ⫽ 1.03). Thus, the aMCI group correctly enacted significantly fewer crux actions and noncrux actions than the control group.

Error Rate Analysis To evaluate the error rates (shown in Figure 3), a mixed-design ANOVA with the between-subjects factor of group (aMCI, control) and the within-subjects factors of error type (omission, com-

Table 3 Intercorrelation Matrix for Multiple Regression Terms

Executive composite Memory composite Semantic composite

Crux omission

Noncrux omission

Crux commission

Noncrux commission

Executive composite

Memory composite

Semantic composite

⫺.25 ⫺.41ⴱ ⫺.45ⴱ

⫺.09 ⫺.43ⴱ ⫺.29

⫺.42ⴱ ⫺.38 ⫺.17

⫺.37 ⫺.41ⴱ ⫺.34

— .21 .37

— — .54ⴱ

— — —

Note. Pearson correlation values for predictor and outcome variables for multiple regressions (n ⫽ 48). ⴱ p ⬍ .004.


328 Table 4 Summary of NA Regression Models

Predictors (ra(b.c)) Dependent variable

Model

R2

Adj. R2

SE

⌬ R2

F

Sig.

Executive

Semantic

Memory

1 2 1 2 1 2 1 1 2

.27 .41 .21 .27 .29 .45 .37 .27 .42

.22 .30 .15 .14 .24 .35 .32 .22 .32

.06 .06 .08 .08 .10 .09 .09 .09 .08

— .14 — .06 — .16 — — .15

5.38 2.35 3.83 0.88 5.88 2.96 8.51 5.39 2.29

.003ⴱⴱ .185 .016ⴱ .487 .002ⴱⴱ .031ⴱ .000ⴱⴱ .003ⴱⴱ .051

⫺.10 — .02 — ⫺.37ⴱⴱ ⫺.29ⴱ ⴚ.40ⴱⴱ, .04 ⫺.28ⴱ —

⫺.22 — ⫺.06 — .17 .18 — ⫺.05 —

⫺.22 — ⫺.35ⴱ — ⫺.34ⴱⴱ .05 — ⫺.27ⴱ —

Crux omission Noncrux omission Crux commission

Note. n ⫽ 48, except in interaction n ⫽ 24. In the interaction term, the bolded value is for aMCI and regular font for controls. ⴱ p ⬍ .05. ⴱⴱ p ⬍ .01.

mission) and action type (crux, noncrux) was conducted. There was a significant within-subjects effect of action type, F(1, 46) ⫽ 40.23, p ⬍ .001, ␩p2 ⫽ .46, whereby a higher proportion of noncrux actions (M ⫽ 12%, SE ⫽ 0.82) were performed in error than crux actions (M ⫽ 8%, SE ⫽ 0.83). We did not find a within-subjects effect of error type, F(1, 46) ⬍ 1, p ⫽ .555, ␩p2 ⫽ .01, nor did we find an interaction of error type by action type, F(1, 46) ⫽ 2.38, p ⫽ .130, ␩p2 ⫽ .05, or group by error type by action type, F(1, 46) ⬍ 1, p ⫽ .951, ␩p2 ⫽ .004. Thus, we did not find a difference between the aMCI and control group in their likelihood of making either type of error as a function of the centrality of the action. However, there was a significant main effect of group, F(1, 46) ⫽ 28.66, p ⬍ .001, ␩p2 ⫽ .38. The aMCI group (M ⫽ 12%, SE ⫽ 1.61) had significantly more crux omissions than controls (M ⫽ 5%, SE ⫽ 0.89), t(46) ⫽ ⫺3.42, p ⫽ .001, d ⫽ 0.99, as well as significantly more noncrux omissions (17%, SE ⫽ 2.05) relative to controls (M ⫽ 10%, SE ⫽ 1.43), t(46) ⫽ ⫺2.76, p ⫽ .008, d ⫽ 0.78. The aMCI group (13%, SE ⫽ 2.44) also had significantly

more crux commissions relative to controls (M ⫽ 4%, SE ⫽ 1.03), t(46) ⫽ ⫺3.62, p ⫽ .001, d ⫽ 1.05, as well as significantly more noncrux commissions (16%, SE ⫽ 2.30) relative to controls (M ⫽ 6%, SE ⫽ 0.61), t(46) ⫽ ⫺4.35, p ⫽ .001, d ⫽ 1.26. Taken together the aMCI group enacted significantly more errors than controls, with both groups enacting a higher proportion of errors on the noncrux actions relative to crux actions. The pattern of errors indicated that both errors of omission and commission were equally likely to occur.

The Association Between Cognitive Variables and NA Crux omission. Model 1 accounted for 22% of the variability in the crux omission rate. None of the composite variables contributed significant unique variability, suggesting that they mutually predicted crux omissions. Lower scores on the composite measures of executive function (ra(b.c) ⫽ .10), semantic knowledge

100 90 80 % of Actions Accomplished


Crux commission interaction Noncrux commission

70 60 Crux

50 Noncrux

40 30 20 10 0 Control

aMCI Group

Figure 2. Mean percentage of actions accomplished (⫹/⫺SE). The aMCI group accomplished significantly fewer crux and noncrux actions than controls.

Figure 3. Mean percentage of actions performed (⫹/⫺SE) by error type (omission, commission) and action type (crux, noncrux). The aMCI group enacted significantly more errors than controls, yielding a balanced error profile of elevated omissions and commissions.



(ra(b.c) ⫽ .22), and episodic memory (ra(b.c) ⫽ ⫺.22) were each associated with higher crux omission rates (see Table S1). Noncrux omission. Model 1 accounted for 15% of the variability in the noncrux omission rate. Only episodic memory contributed significant unique variability (ra(b.c) ⫽ .35). Crux commission. Model 1 accounted for 24% of the variability in the crux commission rate. Only episodic memory contributed significant unique variability (ra(b.c) ⫽ .35). Model 2 contributed unique variability over and above Model 1, leading to the investigation of the significant interaction term separately by group. Crux commission interaction. Model 2 significantly accounted for 32% of the variability in the crux commission rate. There was a significant interaction of group by executive composite. The executive composite was a significant unique predictor for the aMCI group (ra(b.c) ⫽ .40), but not for controls (ra(b.c) ⫽ .04). Noncrux commission. Model 1 accounted for 22% of the variability in the noncrux commission rate. Executive function contributed significant unique variability (ra(b.c) ⫽ .28), as did episodic memory (ra(b.c) ⫽ .27).

Discussion This study was the first systematic investigation to reveal that individuals with aMCI perform frequently enacted NAs less efficiently than healthy age-matched controls. We hypothesized that episodic memory weakness would lead to mild decrements in recalling the detailed elements of the crux and noncrux actions at the time of enactment. Individuals with aMCI accomplished both fewer crux and noncrux actions than controls, and had more omissions and commissions than controls. The similarity between the groups in their patterns of accomplishment performance and error profiles as a function of the centrality of the actions (Figures 2 and 3) suggests that the hierarchical structure for NAs is intact in aMCI individuals. We hypothesized that NA errors are related to the integrity of multiple cognitive processes, but that omissions draw more strongly on episodic memory abilities and commission errors are more closely related to executive function. Crux omission errors were related to multiple cognitive operations for both groups, while noncrux omissions were associated with episodic memory. It is interesting that crux commissions were also related to episodic memory for both groups, and were uniquely related to executive function processes in the aMCI group. Noncrux commissions were also related to episodic memory and executive function in both groups. Our findings highlight the role of episodic memory in the enactment of NA errors for both healthy older adults and individuals with aMCI, consistent with recent findings with NAs (Seligman et al., 2014) and more broadly with measures of IADL (e.g., Farias et al., 2006; Teng, Becker, Woo, Cummings, & Lu, 2010). Previous research indicated that individuals with MCI enact a higher proportion of commissions relative to omissions, leading to the conclusion that individuals with MCI show impairments in the smooth execution of NAs, but not a loss of task knowledge (Giovannetti, Bettcher, Brennan, Libon, Burke, et al., 2008). This is consistent with mounting evidence that individuals with aMCI and MCI enact performance-based IADL tasks less efficiently than controls (Bangen et al., 2010; Burton, Strauss, Bunce, Hunter, & Hultsch, 2009; Schmitter-Edgecombe et al., 2012). The relatively

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higher omission error rates in our study compared to those reported by Giovannetti, Bettcher, Brennan, Libon, Burke, et al. (2008) may be a consequence of differences in the composition of the samples in the two studies. In the current study all aMCI participants had memory impairment, whereas 40% of their MCI sample were memory impaired. Previous research with NAs has shown that higher omission error rates are associated with lower scores on standardized memory tests (for a review, see Giovannetti et al., 2012). Accordingly, one would anticipate higher omission error rates would be obtained in our study compared to Giovannetti, Bettcher, Brennan, Libon, Burke, et al. (2008). More generally, the different patterns of errors observed in the two studies is consistent with the finding that subtypes of MCI differ in their underlying neuropathology and likelihood of progressing to different types of dementia (Albert et al., 2011), as well as their characteristic patterns of everyday activity difficulties (e.g., Gold, 2012). Our NA enactment condition did not have the complex conditions of the NAT (Schwartz et al., 2002), with items hidden from view or performing two tasks simultaneously. Although speculative, it may explain why their control groups and low error producers enact more commissions than omissions (e.g., Schwartz, 2006). It is also possible that minor differences in scoring procedures between research groups could help explain this finding, as Giovannetti and colleagues have an error category for actions that are anticipation omissions, and scored as commission errors. We included a standardized administration with distracter objects to simulate the home environment, and wanted to address certain hypotheses about highly familiar NAs that individuals are currently performing. In other studies, participants may have never performed the NA task previously, or not in the last number of years. Thus, it is also possible that higher commission error rates found in other investigation may be associated with performance of a NA task that is relatively unfamiliar to a participant. Assessing the performance of NAs that vary in familiarity may be a fruitful area of future research. We hypothesized that NAs draw upon a diverse array of cognitive processes, but that distinct elements of cognition would be differentially implicated in different aspects of errors of NA production. Both omission and commission errors were associated with episodic memory, semantic knowledge, and executive function, consistent with theories that predict that NA enactment relies on the integrity of a distributed network of cognitive processes (Hartmann et al., 2005). However, omissions and commissions were also differentially associated with cognitive measures as a function of the centrality of action and group membership. The omission of crux actions was jointly predicted by multiple cognitive operations. This finding extends the demonstrated association between omissions and measures of both episodic memory and general cognitive functioning (Giovannetti, Bettcher, Brennan, Libon, Kessler, et al., 2008) to indicate that semantic knowledge and executive function may also play a role in the omission of crux actions. By contrast, the omission of noncrux actions was uniquely associated with episodic memory in both groups. This relationship was hypothesized to reflect the role of episodic memory in recollecting more detailed elements of a task, a process that declines with age and MTL dysfunction (Salmon, 2012). Thus, there may be two distinct categories of omission errors that other researchers have previously viewed as a single entity: the central action omissions that draw upon multiple cognitive processes, and the


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supporting action omissions that draw more closely upon episodic memory. However, more research is needed to clarify how memory affects central and supporting actions, and if this finding would hold true in different patient populations. Commission errors were also significantly associated with episodic memory for both groups. Crux commission errors were uniquely predicted by the executive composite for the aMCI group, but not for controls. This is consistent with previous research that shows that executive function plays an important role in commission errors for individuals with neurological compromise (e.g., Kessler et al., 2007). However, it extends current findings to highlight the importance of executive function as well as memory processes in the commission of both central and supporting actions in aMCI. A possible interpretation of the observed associations between composite variables and NA error rates may not reflect a specific effect of the cognitive domain in question, but rather functions as a general proxy of disease severity. Two of our findings argue against this interpretation. Group membership did not significantly predict error rates in three of the four regression analyses we reported. As well, we found unique interactions between group membership and select composite variables that were consistent with previous findings (Giovannetti et al., 2012). Comparing NA performance between aMCIsd and aMCImd groups could be an area of future research to better understand the relative role of episodic memory and other areas of relative cognitive weakness such as executive function in NA enactment. The current study was significantly underpowered for such an examination. Nevertheless, exploratory analyses revealed that the subgroups did not differ in their performance on the diagnostic cognitive battery significantly, with the aMCImd group only different than the aMCIsd group in poorer constructional praxis. Despite the limitations, a number of strengths from the study emerge. The investigation was comprised of a well-defined sample of aMCI individuals that were closely matched to healthy older adults. To our knowledge, this represents the first investigation of NA enactment in a sample of aMCI, and individuals with aMCI were significantly less likely to accomplish both the central and enabling actions of familiar NAs. The aMCI group’s relatively balanced error profile of higher commissions and omissions in our study is more similar to that of a DAT group, but with fewer errors overall (e.g., Giovannetti et al., 2006). Given that aMCI may be a prodromal stage of DAT (for a review see Albert et al., 2011), it would thus be plausible that the error profile also mirrors the transition from the relatively intact NA performance in our sample (e.g., erring on 20% of the actions in our tasks) to the significant impairment in NA enactment found in DAT (Giovannetti, Bettcher, Brennan, Libon, Kessler, et al., 2008). The relationship between executive function and crux commission errors for our aMCI group would be consistent with the characteristic Alzheimer’s neuropathology that progresses from MTL to frontal regions. The finding of a difference in the accomplishment of even the most central actions of our highly familiar NAs suggests that some of the crux and noncrux actions are susceptible to mild decline in aMCI. Further research is needed to specify which aspects of crux and noncrux action are vulnerable to degradation. For instance, errors on the noncrux actions that enable cruxes may lead to poorer NA enactment than errors on the “housekeeping” noncruxes that follow cruxes.

The study extends current research to refine predictions about the centrality of action, an aspect of NAs that has not been well addressed. We provide preliminary evidence that omissions of the most central actions in a NA may be mediated by multiple operations including detailed memory for the task, an intact understanding of the relationship between the actions and objects, and functions such as planning and problem solving. Rusted and Sheppard (2002) proposed that a degradation of the memory trace for NA underscores its breakdown over time. The current findings refine this conclusion to suggest that the omission of supporting actions is uniquely associated with episodic memory. This is consistent with our hypothesis that the episodic memory representation supports the detailed elements of noncrux action. Episodic memory may play an important role in recalling prior instances of enacting NA tasks, previous actions that have already been performed while the task is enacted, or, even perhaps the task instructions. Others have hypothesized that MTL structures also play a role in the planning process of everyday action (e.g., Seligman et al., 2014). Our pattern of correlations between cognitive variables and errors of omission and commission do not support a general cognitive resource model of NA (Schwartz, 2006). Rather, they are largely consistent with the Omission-Commission Model (Giovannetti et al., 2012), though our findings provide preliminary evidence that could both refine its predictions as a function of the centrality of action, and the range of cognitive processes that mediate error production. We provide evidence that the cognitive correlates of NA errors are not process pure (Jacoby, 1991), but differentially draw on a range of cognitive processes. For instance, although the Omission-Commission Model predicts that episodic memory and task knowledge play an important role in omissions, this study provides evidence that general and action-specific semantic knowledge, as well as elements of executive function, are also related to omitting central actions in aMCI individuals and controls. This finding is consistent with our hypothesis that multiple memory systems may underlie NA performance. Unlike the Omission-Commission model, we hypothesize that higher-level goals are represented more semantically in memory, whereas detailed aspects of action are represented more episodically. Although some support was obtained for this hypothesis, further research is needed to evaluate how different cognitive processes mediate central and supporting actions. Our findings also posit a role for episodic memory in the commission of NAs in healthy elders and those with aMCI. We find that memory and executive control is associated with commission errors, consistent with previous hypotheses (Gold & Park, 2009). It may be the case that there are multiple routes to the same error destination (e.g., Hartmann et al., 2005). For instance, individuals may enact commission errors such as reversing the order of steps in a task, or repeating previously completed steps because of an inability to inhibit a prepotent response, sequence efficiently, or in an attempt to cue themselves (the executive function explanation); or, they may have forgotten that a step had been previously completed or failed to recall a detailed representation of the steps at the time of enacting the task (the memory explanation). It may also be the case that memory and executive function operations are executed in concert such that when a memory failure occurs, or, there are weaknesses in the semantic representation for the task goal, executive processes serve to alert the individual of an up-



coming error. Scenarios such as these have been modeled with complex computer simulations with some degree of success (Cooper et al., 2005). Our regression analyses provide data to support that a commission error is related to the integrity of both executive and memory processes, which may serve to advance future simulation studies and enhance cognitive theories of NA breakdown. The ability to detect differences in the cognitive processes associated with NA error may have been due to our selection of theoretically driven measures about the specific nature of the cognitive deficits that underlie NA breakdown in healthy older adults and aMCI. There is a recognized need for more comprehensive cognitive measures that better capture the cognitive processes associated with NAs (Bettcher et al., 2011; Hartmann et al., 2005). Associative memory selectively declines with age and MTL pathology, and we hypothesize that it may play a role in different elements of NA enactment, but particularly in the recollection of the detailed supporting actions. Beyond assessing task knowledge through script derivation, our findings indicate that it may be important to assess the relationship between the detailed semantics for action and NA errors. While previous executive composites have emphasized the role of working memory, our findings also highlight the role of processes such as generation, planning, and conceptualization that may capture mental control as well as the continued use of strategy and foresight that may also be needed to avoid commission errors. Beyond theoretical implications, our findings have practical implications as well. Efforts to reduce NA omission errors in dementia groups with goal-cuing has produced mixed findings (e.g., Brennan, Giovannetti, Libon, Bettcher, & Duey, 2009). The findings from the current study of higher rates of noncrux errors than crux errors suggest that individuals with aMCI may benefit from cuing of noncrux actions. Future research could also examine if targeted cognitive rehabilitation could impact the frequency of crux and noncrux errors, such as memory interventions for those with a noncrux omission profile. We found that individuals with aMCI have a balanced error profile, whereas those with MCI may have a commissive profile. Future studies may seek to replicate this finding and investigate if informant reports of everyday activity disturbance coincide with these characteristic profiles, an endeavor which could have important clinical implications for identifying early changes in everyday activity that may be pathological in nature. Furthermore, NAs may be administered in neurocognitive assessments to facilitate differential diagnosis between healthy aging and aMCI, a topic that we return to in a separate study.

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Received January 4, 2014 Revision received May 1, 2014 Accepted July 4, 2014 䡲

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Alterations in working memory networks in amnestic mild cognitive impairment.

Biological heterogeneity in ADNI amnestic mild cognitive impairment.

Abstract Word Definition in Patients with Amnestic Mild Cognitive Impairment.

Dynamic working memory performance in individuals with single-domain amnestic mild cognitive impairment.

Neuropathological comparisons of amnestic and nonamnestic mild cognitive impairment.

Olfactory identification in amnestic and non-amnestic mild cognitive impairment and its neuropsychological correlates.

Association of body mass index with amnestic and non-amnestic mild cognitive impairment risk in elderly.

NK Cells are Activated in Amnestic Mild Cognitive Impairment but not in Mild Alzheimer's Disease Patients.

Difference in determinants of caregiver burden between amnestic mild cognitive impairment and mild Alzheimer's disease.

Saccade deficits in amnestic mild cognitive impairment resemble mild Alzheimer's disease.

Sex differences in cognitive training effects of patients with amnestic mild cognitive impairment.

A cognitive electrophysiological signature differentiates amnestic mild cognitive impairment from normal aging.

Lowered performance in working memory and attentional sub-processes are most prominent in multi-domain amnestic mild cognitive impairment subtypes.

Deficits in episodic memory retrieval reveal impaired default mode network connectivity in amnestic mild cognitive impairment.

Abnormal salience network in normal aging and in amnestic mild cognitive impairment and Alzheimer's disease.

Spatial memory impairments in amnestic mild cognitive impairment in a virtual radial arm maze.

Disrupted Causal Connectivity Anchored in the Posterior Cingulate Cortex in Amnestic Mild Cognitive Impairment.

NoGo Semantic Categorization Task Performance and Event-Related Potentials.

Retinal nerve fiber layer thickness in amnestic mild cognitive impairment: Case-control study and meta-analysis.

Abnormal changes of multidimensional surface features using multivariate pattern classification in amnestic mild cognitive impairment patients.

Recognition memory in amnestic-mild cognitive impairment: insights from event-related potentials.

Association between Plasma Leptin and Estrogen in Female Patients of Amnestic Mild Cognitive Impairment.

Relation between aerobic fitness and brain structures in amnestic mild cognitive impairment elderly.

The effect of TOMM40 on spatial navigation in amnestic mild cognitive impairment.