Planning and realization of complex intentions in traumatic brain injury and normal aging
Introduction
In the last few years, there has been an enormous increase of research interest in prospective memory, i.e., the processes and skills required to support the delayed fulfilment of a previously planned intention (see Ellis & Kvavilashvili, 2000). Interest in prospective memory is largely based on its significant relevance in everyday life, especially in older adults and neuropsychological patients (see Kliegel & Martin, 2003). Particularly those persons appear to have considerable difficulties in prospective remembering.
Several studies suggest that prospective memory declines early in age. For example, Dobbs and Rule (1987) and Mäntyla and Nilsson (1997) demonstrated in their studies with large samples of participants between 30 and 80 years that prospective memory seems to decline linearly from the 5th decade. Huppert, Johnson, and Nickson (2000) also found a linear decline in prospective memory in their large population-based study of participants 65 years and older.
As for prospective memory performance in neuropsychological patients, prospective remembering seems to be disrupted by many neurological and psychiatric disorders. For example, prospective memory impairments are reported for patients with Herpes Simplex Encephalitis (Sgaramella, Borgo, Fenzo, Garofalo, & Toso, 2000), Korsakoff's Syndrome (Brunfaut, Vanoverberghe, & d'Ydewalle, 2000), Parkinson's disease (Bisiacchi, 2000), early dementia (Huppert & Beardsall, 1993; Huppert et al., 2000), schizophrenia (Meissner, Hacker, & Heilemann, 2001; Ouriache, 2000), depression (Rude, Hertel, Jarrold, Covich, & Hedlund, 1999), and brain injury (Groot, Wilson, Evans, & Watson, 2002; Shum, Valentine, & Cutmore, 1999). Moreover, there are indications that there is an association between the severity of prospective memory deficits and the severity of the traumatic brain injury (McCauley & Levin, 2004). Furthermore, it has been demonstrated that for people with traumatic brain injury prospective memory deficits impair everyday functioning (Kinsella et al., 1996) and are the primary obstacles for leading an independent life (Thöne-Otto & Walther, 2001).
To investigate which variables might be related to these deficits in prospective memory performance, theoretically, the delayed realization of an intention has been proposed to be a complex process involving at least four phases (Ellis, 1996; Kliegel, Martin, McDaniel, & Einstein, 2002). In the first phase (i.e., intention formation), one has to form the intention, i.e., to plan which actions shall be performed at what time in the future, and then to encode the plan. According to the way in which performance time is signalled, two kinds of prospective memory tasks have been distinguished (Einstein & McDaniel, 1996). For time-based prospective memory tasks, the intended action is carried out at a particular time or after a certain amount of time has passed; for event-based prospective memory tasks, the intended action is performed when a certain event occurs (Einstein & McDaniel, 1990). In the second phase (i.e., intention retention), one has to keep the intention in mind while working on other tasks. The third phase (i.e., intention re-instantiation) begins when the intended moment for the re-instantiation of the intended action arises. Here, one has to inhibit ongoing activities, and re-instantiate the intended plan. The success in this phase depends heavily on how well one monitors the environment for the (time- or event-related) signal to perform the delayed intention (see Kliegel et al., 2001, Kliegel et al., in press). In the last phase (i.e., intention execution), on one's own initiative, the intended action has to be carried out as previously planned.
As has been suggested from this and similar task analyses (see Burgess & Shallice, 1997; Knight, 1998; Kvavilashvili & Ellis, 1996), prospective memory seems to rely on retrospective memory skills (i.e., the encoding, retention, and retrieval of the intentions) and even more so on executive functions (i.e., planning the intended action, monitoring the environment for the cue to re-instantiate the intention while performing other tasks, inhibiting these other activities at the critical time to perform the intention, switching to the intended action and carrying it out as it was planned). It has been demonstrated that patients with moderate to severe traumatic brain injury have deficient retrospective memory skills, particularly in the acquisition (DeLuca, Schultheis, Madigan, Christodoulou, & Averill, 2000) and retention of information (Vanderploeg, Crowell, & Curtiss, 2001), which might account for prospective memory problems observed in TBI patients.
McDaniel, Glisky, Rubin, Guynn, and Routhieaux (1999) and Kopp and Thöne (2003) explored the role of retrospective memory skills and executive functions for a prospective memory task in older participants or patients with brain injury, respectively. In both studies, using two distinct, rather simple prospective memory tasks, participants were assigned to four groups according to the presence or absence of retrospective memory impairments and/or executive functioning deficits (as identified by neuropsychological tests). Participants with unimpaired executive functions performed better on the prospective memory task than those with executive functioning deficits, regardless of their retrospective memory skills. In contrast, there were no differences between participants with and without retrospective memory deficits. However, Kopp and Thöne (2003) had excluded people from the study who were not able to learn the prospective memory task instructions and allowed for more acquisition trials for individuals with learning deficits. Nevertheless, other findings also suggest that it does not seem to be the most critical part of a prospective memory task to retrospectively recall the content of an intention and that, in fact, recalling an intention content seems be intact even in severe neuropsychological syndromes. Maylor, Smith, Della Sala, and Logie (2002), for example, found that patients with Alzheimer's disease were able to recall prospective memory task instructions after the time to complete the prospective memory task although being impaired on memory tests such as digit span, sentence span and free recall of a word list. Consequently, retrospective memory of intention content seems to be a necessary prerequisite for the delayed realization of this intention, but otherwise executive functions seem to be of even greater importance for the actual re-instantiation and execution of the delayed intention.
Executive functions are assumed to be, at least in part, based on neuronal processes located in the prefrontal cortex (Burgess, 1997; Levin, Greenberg, & Benton, 1991; Smith & Jonides, 1999). Recent imaging studies have demonstrated an involvement of prefrontal areas in prospective memory tasks (Burgess, Quayle, & Frith, 2001; Okuda et al., 1998; West, Herdon, & Crewdson, 2001). Furthermore, Cockburn (1995), Shallice and Burgess (1991), and Bisiacchi (1996) reported on single cases with focal prefrontal lesions who were impaired in prospective memory tasks. In addition, Shapiro, Shapiro, Russell, and Alper (1998) found that a group of patients with focal prefrontal lesions performed worse on a prospective memory task than a group of patients with focal posterior lesions. In conclusion, there is converging evidence from imaging and lesion studies that prospective memory depends on the functioning of the prefrontal areas.
In accordance with these findings, the deterioration of prospective memory with increasing age is thought to be associated with the age-related decay of prefrontal cortex functions (Glisky, 1996; Kliegel et al., 2003a, Kliegel et al., 2003b; West, 1996). Age-related functional and structural changes appear to be first evident in the prefrontal cortex as compared to other cortical areas, around the age of 50 (for an overview see Salat, Kaye, & Janowsky, 2001; West, 1996). Furthermore, Daigneault, Braun, and Whitaker (1992) and Crawford, Bryan, Luszcz, Obonsawin, and Stewart (2000) demonstrated that executive functions do decline early in old age. Moreover, there are first findings that directly support the hypothesis that age-related decline in prospective memory is linked to age-related deficits in the prefrontal lobe or in executive functioning, respectively. West and Covell (2001) demonstrated that the less efficient prospective memory performance of older people went along with reductions of the amplitude of event-related brain potentials that are thought to reflect frontal neural activity. In addition, Kliegel et al. (2003a), in an hierarchical multiple OLS regression analysis, found that the age-related variance in two prospective memory tasks was completely accounted for by the variance of five executive functions tests: Wisconsin Card Sorting Test (Heaton, Chelune, Talley, Kay, & Curtiss, 1993), Plan-A-Day Test (Funke & Krüger, 1993), Stroop Test (Stroop, 1935), Tower of London (Ward & Allport, 1997), and S-Words Test (Regard, Strauss, & Knapp, 1982).
However, most of the above-mentioned studies exploring the involvement of the prefrontal cortex or executive functions in prospective memory as well as their role in its age- and neuropsychological disease-related decline have employed prospective memory tasks that do not disentangle the outlined phases in the process of the realization of an intended action at an intended time in the future.
Kliegel, McDaniel, and Einstein (2000) have proposed a laboratory procedure that allows for the separate assessment of the four phases of the prospective memory process (i.e., intention formation, intention retention, intention re-instantiation, and intention execution). They found age-related declines in intention formation, intention re-instantiation, and intention execution. Moreover, Kliegel et al. (2002) demonstrated in a multiple linear regression analysis on the data of eighty healthy individuals that approximately 50% of the performance variance during intention formation, intention re-instantiation, and intention execution in their prospective memory task were predicted by executive measures whereas the variance in intention retention was not accounted for by any of these measures. Thus, it seems that only intention formation, intention re-instantiation, and intention execution depend on executive functioning. In consequence, one might expect that only in these phases performance decrements for any individuals with executive functioning deficits should arise—in older adults and in (younger) patients with selective deficits in executive functioning.
Continuing with this line of research, it was one aim of the present study to provide further evidence for this differential effect of executive functioning impairments on intention formation, re-instantiation, and execution. Applying an approach of combining healthy older adults with younger neuropsychological patients and younger healthy controls, the second aim of the study was to investigate if age-related prospective memory decline might be related to executive functioning deficits. Therefore, in the present investigation, a group of patients with a retrospective memory within normal limits but impaired executive functions as a consequence of a traumatic brain injury, a group of healthy older adults and a group of healthy younger adults completed the complex prospective memory task according to Kliegel et al. (2000).
Proceeding from the described previous findings and from the hypothesis that age-related prospective memory decline is associated with the deterioration of executive functioning, it was expected that the patients with the executive functioning deficits and the older healthy adults would perform worse than the younger healthy adults in the intention formation, intention re-instantiation, and intention execution phase of the complex prospective memory task. However, all groups should achieve similar results in the intention retention phase, as healthy older adults were not expected do differ substantially from the younger neuropsychological patient group.
Section snippets
Participants
Forty-seven participants were included in the analyses. Seven participants were former patients of the Day-Care Clinic of Cognitive Neurology of the University of Leipzig who met the inclusion criteria: traumatic brain injury (TBI) at least 6 months prior to the study, retrospective memory within normal limits according to delayed recall indices ⩾85 on the Wechsler Memory Scale-Revised German version (WMS-R; Härting et al., 2000), impaired executive functioning as indicated by age-corrected sum
Participant characteristics
In Table 2, the TBI patients, the older, and the younger control participants are compared for age, gender, verbal intelligence level (as measured by the MWT-B) and for executive functions (as measured by the percentage of possible categories completed of the Wisconsin Card Sorting Test; WCST, Heaton et al., 1993).
Discussion
In summary, the study demonstrated that a group of relatively young traumatic brain injury patients with retrospective memory within normal limits but impaired executive functions and a group of healthy older adults obtained significantly lower scores than a group of healthy younger controls in the intention formation, intention re-instantiation, and intention execution measures of Kliegel et al.'s (2000) complex prospective memory task. In contrast, all three groups performed well and not
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Both authors contributed equally.