Frontal Lobes and Episodic Memory
FRONTAL LOBES AND EPISODIC MEMORY
The idea that the frontal lobes are implicated in memory has a long and controversial history (Luria, 1980; Teuber, 1964). Damage to the frontal lobes can produce memory impairment and sometimes even severe memory loss, but it has proved difficult to specify the nature of the disorder. The scholarly consensus now holds that frontal-lobe damage does not lead to memory deficits in consolidation, storage, and retention of newly acquired information (Petrides, 2000; Moscovitch and Winocur, 2002). Such disorders, which in their most extreme form lead to a profound global amnesia, are associated with damage to the medial temporal lobes, particularly the hippocampus and related structures, and to midline thalamic nuclei (Milner, 1966).
Memory loss following frontal-lobe lesions, on the other hand, involves organizational or strategic aspects of memory that are necessary for devising strategies for encoding, for guiding search at retrieval, for monitoring and verifying memory output, for placing retrieved memories in their proper spatial and temporal contexts, and for using mnemonic information to direct thought and plan future actions. In other words, the frontal lobe's memory functions are consistent with its functions in other domains. It helps organize the raw material that is made available by other structures so that thought and behavior can be goal-directed. If the hippocampus and its related structures can be considered raw memory structures, then the frontal lobes are working-with-memory structures that operate on the input and output of the hippocampal circuit (see Figure 1). We prefer the descriptive term working-with-memory to the more theoretically loaded terms working memory or executive function favored by others (Baddeley, 1986; Goldman-Rakic, 1987; Smith and Jonides, 1998; Stuss and Knight, 2002); this term captures the essence of frontal-lobe contribution to memory but does not commit the user to endorse a working-memory theory that may be flawed or inappropriate (Moscovitch and Winocur, 1992).
Review of Lesions Studies and Memory Tasks
One can best appreciate the contribution of the frontal lobes to memory by comparing the effects of frontal damage on various memory tests with effects of damage to the hippocampus and midline thalamic nuclei. Recognition and recall of isolated random words or pictures are typically normal in patients with frontal lesions but impaired in patients with hippocampal or diencephalic damage (Mayes, 1988; Milner, Petrides, and Smith, 1985). Recall of categorized lists or of logical stories, however, is impaired in frontal patients, presumably because they cannot take advantage of the organizational structure inherent in that material (Incissa della Rochetta, 1986). Deficits may also occur in free recall if normal performance depends on strategic search or retrieval (Janowsky, Shimamura, Kritchevsky, and Squire, 1989; Wheeler, Stuss, and Tulving, 1995; Moscovitch and Winocur, 1995, 2002).
In contrast with memory for target items or facts that can be elicited by cues directly associated with them, memory for spatiotemporal context often requires strategic search. Consider introspectively the difference in the processes involved in answering these two questions: Have you seen Gone with the Wind? What did you do two weekends ago? The first elicits an immediate, automatic reply; the second typically initiates a labored, strategic search. As expected, memory for spatiotemporal context, but not for targets, is impaired after frontal lesions, whereas the reverse is true after hippocampal or midline diencephalic lesions.
Memory for temporal order is poor in frontal patients when it is tested by asking patients to judge the relative recency of a pair of items or to arrange a set of items in the order in which they were presented (Milner, Petrides, and Smith, 1985; Shimamura, Janowsky, and Squire, 1990). The deficit also extends to remote memories that were acquired long before the lesion occured. Defective memory for sources of facts they had learned has also been observed in patients with frontal lesions or frontal dysfunction. They erroneously ascribe the factual information to an incorrect source on tests of source recall and source recognition (Schacter, Harbluk, and McLachlan, 1984; Janowsky, Shimamura, and Squire, 1989b). On the other hand, hippocampal or diencephalic damage leads to deficient memory for targets or facts at long delays but not for their temporal order or for sources at delays in which the facts can be remembered. In other words, their memory for temporal order is no more impaired than, and may be superior to, their memory for facts (Milner, Petrides, and Smith, 1985; Shimamura, Janowsky, and Squire, 1990).
Poor memory for spatiotemporal context that results from impaired strategic processes may also underlie the frontal patient's deficits on a variety of other tests, such as delayed alternation, delayed response, and delayed match-to-sample with a small, repeated set of items (Freedman and Oscar-Berman, 1986; Prisko, 1963; Milner, Petrides, and Smith, 1985). On delayed response, after a short delay the subject must choose one of the items that had been designated as the target. On delayed alternation, the designated target alternates on every trial. In delayed match-to-sample, the subject chooses from a small set of items the one that matches a target that was inspected earlier. On all these tests, frontal patients fail not because they cannot remember the target but because they cannot segregate the current trial (keep the spatiotemporal context distinct) from preceding ones.
Impaired performance by frontal patients on self-ordered pointing tests may have a similar cause (Petrides and Milner, 1982). In these tests, subjects are required to point to one of a set of words, line drawings, or designs that appear on a sheet of paper. On each subsequent trial, new sheets are presented with the same items arranged differently, and the subject is required to point to a different item each time. There are as many trials as there are items. Apart from remembering the items and keeping spatiotemporal context distinct, subjects performing this test need to monitor their responses and use their memory of them to plan future actions. Monitoring and planning are both prototypical frontal functions that are applied to memory and may be impaired by frontal lesions. Another way to interpret these results is to say that the test requires monitoring information that is held in working memory (Petrides, 2000).
Impaired estimation of frequency of occurrence is also associated with frontal lesions (Smith and Milner, 1988). In one test of this association, items are repeated a number of times and the subject's task is to estimate the number of repetitions. It is not clear whether the deficit on this test is a symptom of a general deficit in cognitive estimation that accompanies frontal damage (Shallice and Evans, 1978) or whether it also results from a failure to search memory strategically.
Although the formation and retrieval of new associations are not dependent on the frontal lobes, learning conditional associations is (Petrides and Milner, 1982). The difference between the two tests highlights the distinction between memories elicited directly by cues associated with them, a process that involves the hippocampus, and memories for which additional extra-cue, strategic processes are necessary and involve the frontal lobes. In learning new associations, a single cue such as a light is paired with a unique response such as an arm movement, which it eventually elicits. In conditional associative learning, all cues and potential responses are present in the situation and typically resemble one another. For example, a set of six lights is presented, each of which needs to be associated with one of six movements that the subject has mastered. The cue, one of the lights, does not elicit the response, the designated movement, but only provides the occasion for the subject to select from among potential responses the one that is appropriate for one particular cue, another one for another cue, and so on. That is, the subject must determine which light is associated with which movement. Response selection and monitoring, both strategic frontal functions, are key elements of this task. Patients with frontal lesions have difficulty learning only conditional associations, whereas patients with hippocampal lesions have difficulty forming new associations.
Less consistent effects of frontal lesions are found on other memory tests, such as release from proactive inhibition (PI) and "feeling-of-knowing" judgments. In release from PI, four different lists of words from the same semantic category are presented, followed by a list from a different category. Recall, which is tested after each list, declines from the first to the fourth list as PI builds up, but recall recovers to baseline levels on the fifth trial. Release from PI occurs at retrieval. It is not surprising, therefore, that deficits in release from PI have been reported in patients with frontal lesions (Moscovitch, 1982); these are most reliable, however, when a severe memory disorder accompanies frontal dysfunction (Freedman and Cermak, 1986; Janowsky, Shimamura, Kritchevsky, and Squire, 1989).
"Feeling of knowing" is an aspect of metamemory, the knowledge about one's own memory. It refers to a person's belief that he or she would know the correct answer to a memory question. In testing the accuracy of feeling-of-knowing judgments, Janowsky, Shimamura, and Squire (1989a) gave subjects a cued recall test for information they had learned earlier. For those items they failed to recall, subjects were asked to rate their feeling of knowing, their likelihood of recognizing the correct answer among a number of alternatives. Because this metamemory test involves goal-directed search and monitoring, it was expected that patients with frontal lesions would perform poorly on it. Although some deficits were found, the impairment, as in release from PI, was most reliable and far-reaching in patients who had severe memory problems in addition to frontal dysfunction (Shimamura, Janowsky, and Squire, 1990).
Defective performance on memory tests sensitive to frontal lesions is noted in people with neurological conditions associated with frontal dysfunction—that is, with signs of impaired frontal functions though there is no evidence of direct frontal damage. Among those are patients with Parkinson's and Huntington's diseases, the neuropathology of which affects basal ganglia structures that are part of the "complex loop" that connects them to the frontal lobes (Brown and Marsden, 1990; Saint-Cyr, Taylor, and Lang, 1988) and that may be needed for maintaining dopamine levels in the prefrontal cortex. Declines in performance on frontal-sensitive tests also occur in the elderly, presumably because their frontal lobes deteriorate with age (Moscovitch and Winocur, 1992), and in patients with schizophrenia, both because of frontal deterioration and impaired dopamine function.
Even normal young adults may show deficits on frontal tests under conditions that deplete cognitive resources. Because frontal functions are strategic—which implies that voluntary, often conscious, control is an integral part of them—they demand substantial cognitive, attentional resources if they are to operate effectively (Moscovitch and Umilta, 1990). In contrast, the operations of the hippocampus can be run off relatively automatically once the appropriate input is received. Experiments reported in the literature suggest that general interference at the time of retrieval affects primarily performance on tests that are sensitive to frontal function, such as word fluency, recall of categorized lists, and list differentiation. A series of experiments designed to test this hypothesis further has confirmed that a sequential, finger-tapping encoding-and-retrieval task interfered with performance on frontal-sensitive tests, such as recall of categorized lists, release from PI, and phonemic fluency (Moscovitch, 1994). Similar divided-attention effects are observed on tests of source, but not item memory (Moscovitch, Fernandes, and Troyer, 2002). To affect memory on nonfrontal tests such as free recall and recognition of lists of random word the interference at retrieval must be material-specific in the sense that the interfering task consists of material that is similar to that of the target, memory task. In such cases, it is believed that the locus of interference is for access to representational systems in posterior neo-cortex (Moscovitch et al., 2002).
All the memory tests mentioned so far are explicit tests that require conscious recollection of the past for successful performance. In contrast, on implicit tests, memory is inferred from the effects of experience or practice on performance without requiring the individual to refer to the past. Since the frontal lobes are working-with-memory structures, they should be implicated on tests of implicit memory. Indeed, frontal lesions or dysfunctions lead to impaired performance on those tests that are not simply stimulus-driven but require strategic search or application of organized rules or procedures. Thus, patients with frontal lesions or dysfunction have difficulty mastering the Tower of Hanoi, a cognitive puzzle whose solution depends on the application of a sequential, iterative rule (Owen et al., 1990; Shallice, 1982; St. Cyr, Taylor, and Lang, 1988). Frontal patients may also be impaired on other implicit tests, such as learning to read geometrically transformed script and completing word stems after being exposed to target words (Winocur, Moscovitch, and Stuss, 1996; Nyberg, Winocur, and Moscovitch, 1997). The results suggest that the frontal lobes are implicated on implicit tests that have a selection or generative component, but not on tests that are purely perceptually driven (Gabrieli et al., 1999). The extent of frontal involvement on implicit tests is still uncertain. A great deal of work on amnesic patients with hippocampal or diencephalic lesions shows that their performance on a variety of implicit tests appears mostly unscathed, suggesting that these structures are involved only with conscious recollection (Moscovitch, 1982; Moscovitch and Umilta, 1991).
Many of the features of frontal-lobe memory disorders are observable in an especially severe and striking form in confabulating patients with aneurysms or infarcts of the anterior communicating artery. Admittedly, the lesions that typically affect the ventromedial and orbital regions of the frontal lobes also involve other structures in the basal forebrain such as the anterior cingulate, the septum, and the anterior hypothalamus. Nonetheless, the memory symptoms displayed by these patients indicate frontal rather than hippocampal circuit damage. When tested formally, their recognition on tests that do not involve strategic search is relatively well preserved, a result that distinguishes them from amnesic patients with hippocampal damage. However, their ability to search memory and to place events in a proper spatiotemporal context is nearly lost. That loss likely accounts for their tendency to confabulate or make up patently false, often contradictory, and occasionally bizarre or fantastic stories.
For example, one patient who had been in the hospital for months claimed he was still at his office. When asked to account for the beds in his room, he suggested that they were brought in to deal with an epidemic. When such patients confabulate, they do not intentionally lie but inadvertently combine true memories whose spatiotemporal context they have lost. According to Schnider and his collaborators (1996; 2000), such temporal confusion is due to difficulty suppressing information that no longer is relevant and focusing on that which is. It is as if the non-frontal memory system, in response to situational cues, spews out loosely associated memories in a quasi-ordered fashion. Lacking intact frontal lobes, these patients cannot evaluate this output or impose a sensible organization on it. Their memory deficits, therefore, are not restricted to recently acquired memories but extend to remote, personal memories and even to historical information on events that occurred before they were born (Moscovitch and Melo, 1997). Their memory is intact only for events and activities, such as their job routines, that are stored as self-organized and self-contained schemata that depend little on supervision by the frontal lobes for their operation (Moscovitch, 1989).
Localization Within the Prefrontal Cortex: Evidence from Lesions and Neuroimaging
Though we have paid little attention so far to localization within the frontal lobes, we do not wish to leave the reader with the impression that the prefrontal cortex is a homogeneous structure; on the contrary, it is a heterogeneous structure consisting of a number of distinct areas with unique projections to and from other brain regions, and with different phylogenetic and ontogenetic histories (Pandya and Barnes, 1986; Petrides and Pandya, 1994). Two large subdivisions of the prefrontal cortex, the orbital and dorsolateral regions, have different functions (Milner, Petrides, and Smith, 1985), one more emotional and motivational and the other more cognitive. Structural and functional neuroimaging has allowed the discernment of specialized functions of even smaller regions within these subdivisions (Goldman-Rakic, 1987, 2002; Petrides, 2000, 2002). Indeed, there is now evidence for regional specialization for many of the functions that contribute to performance on the various tests of frontal function.
Brodmann areas 6 and 8 (premotor cortex) are implicated in response selection and inhibition, a key feature of conditional associative learning, and retrieval from remote memory (Moscovitch and Winocur, 2002). Areas 46/9 (dorsolateral prefrontal cortex) is for manipulating and operating on information held in working memory or retrieved from long-term memory, as on tests of self-ordered pointing, where monitoring is a crucial component. This region is also important for initiating effective retrieval strategies and monitoring the outcome of implementing them (i.e. retrieval output). The ventrolateral prefrontal cortex, area 47, is important for specifying the cues needed for retrieval (Fletcher and Hensen, 2001). Perhaps it is for this reason that the extent of activation of this area at encoding can predict subsequent memory performance (Wagner et al., 1998) and therefore plays a role in simple recognition (Petrides, 2000). This region also comes into play on tests of conceptual priming, with less activation for material that has been primed (Schacter and Buckner, 1998). The ventromedial prefrontal cortex is important for inhibiting or preventing the expression or behavioral impact of activated memories that are anomalous within a given context. The region is a context-dependent criterion-setting device that determines which memories are relevant—the felt rightness of a memory. The function of area 10 in the frontal pole is much debated, with some investigators believing that it is crucial for allowing one to experience memories as part of oneself and tying them inextricably to conscious, coherent recollection of one's past (Tulving, 2002). Others, however, believe that the role of area 10 is to maintain elaborate retrieval goals and strategies (Fletcher and Hensen, 2001). Still others think it may operate in concert with the verntromedial cortex to endorse memories that are appropriate within a given context. The possible sequential interaction of the regions with each other is displayed in Figure 1.
In addition to regional specificity, there is also lateralization of function within the frontal lobes: Some regions show material specificity with greater left-hemisphere involvement for verbal material and right-hemisphere involvement for spatial material (Milner, Petrides, and Smith., 1985; Petrides, 2000; Kelley et al., 1998). Over and above the material specificity, Tulving and his colleagues (1994) noted a hemispheric encoding/retrieval asymmetry (HERA) in PET studies, with the greater frontal activation on the left during encoding and on the right during retrieval. This pattern has since been observed in numerous functional neuroimaging studies using different techniques (Cabeza and Nyberg, 2000); it cuts across material type in some regions of prefrontal cortex. The reason for this asymmetry is unknown; nor is it clear whether such asymmetries are needed for successful encoding and retrieval. Researchers have debated which aspects of retrieval are associated with right frontal activation: retrieval mode (the establishment of a memory "set" and perhaps setting memory goals and strategies), monitoring (the determination of whether a target item was studied), retrieval success (the accuracy of recall and recognition of items), retrieval task or domain (memory for source or for items), and retrieval effort (how difficult the retrieval task is) (Buckner and Wheeler, 2001; Holding and Rugg, 2000). It seems that as memory retrieval requires more effort, either because the task is more difficult or reflective (Johnson, 2000) or because cognitive resources are limited (as in aging, Cabeza, 2001), both frontal regions are recruited, and the asymmetry is diminished.
Although there has been some progress in identifying the frontal components implicated in encoding and retrieval and isolating them functionally and anatomically, discrepancies and controversies persist in efforts to understand how the different regions interact with one another to yield organized, seamless performance. Future research should also help in deciding between two opposing views of frontal function that have dominated recent theories. One view holds that a common function underlies the operation of all regions in the frontal lobes but that the function expresses itself in diverse ways determined by each region's unique anatomical connections. The other view does not assume a functional link among various regions but argues for true functional independence among them along domain specific lines (Moscovitch and Umlita, 1990; Goldman Rakic, 2002; Petrides, 2002; Stuss and Knight, 2002). The view that prevails will determine our conception of the mechanisms underlying memory, consciousness, and volitional behavior.
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