New York State Psychiatric Institute, New York City, NY 10032 and , 1 New York University, New York City, NY 10003, USA
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Abstract |
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Introduction |
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Support for these arguments has come from a variety of evidence, including behavioral data from the remember (recollection)/know (familiarity) paradigm (Tulving, 1985), neuropsychological studies of amnestic individuals with damage to the medial temporal lobe memory system (Cermak et al., 1992
), memory studies of patients with localized frontal lobe lesions (Janowsky et al., 1989
), event-related brain potential (ERP) investigations (Rugg et al., 1998
), and neuroimaging investigations of blood flow during a variety of memory tasks (Schacter and Buckner, 1998
; Henson et al., 1999
).
The ERP technique is particularly well-suited for the study of these phenomena, as it is non-invasive, does not require averaging over long time periods as is necessary with some neuroimaging techniques, and, most important, is able to track the brain's processing of information in real time (on a millisecond time scale). In addition, this technique provides information concerning the scalp distribution of peaks and troughs in the ERP waveform. Such topographic differences are quite important, as a difference in scalp distribution between two states of awareness, such as familiarity and recollection, implies that different brain generator configurations gave rise to the electrical activity recorded at the scalp. This kind of result would be strong evidence in favor of the view that familiarity and recollection are cognitively distinct, and depend on at least partially non-overlapping brain systems (Squire and Knowlton, 2000). However, the relationship between the two processes could take the form of independence, exclusivity or redundancy (Jones, 1987
; Joordens and Merikle, 1993
; Knowlton and Squire, 1995
), all of which might lead to topographic differences (see Discussion below).
ERP investigators have recorded brain electrical activity in an attempt to disentangle the roles that familiarity and recollection play in a variety of memory-related phenomena (Smith, 1993; Trott et al., 1997
, 1999
; Rugg et al., 1998
; Senkfor and Van Petten, 1998
; Wilding and Rugg, 1996
, 1997
) [reviewed by a number of authors (Johnson, 1995
; Rugg, 1995
; Friedman and Johnson, 2000
)]. In a commonly used paradigm (labeled sequential response), subjects are asked to study verbal items for a subsequent memory test. These items can be presented, for example, in two different lists (Trott et al., 1997
), or by male and female voices (Wilding and Rugg, 1996
). At test, subjects are asked to discriminate, via choice, speeded and accurate reaction times, between old and new items. For any item that is judged old, the subjects are then asked to provide a source memory judgment, e.g. was the item presented during the first or second list? In male or female voice? In this procedure, the ERPs are averaged to correctly recognized old items (i.e. hits) according to whether the source was or was not correctly judged. As correct retrieval of the initial learning context (i.e. source) is considered a hallmark of recollection, the assumption is made that the electrical activity associated with a hit trial on which the source is also correctly judged reflects brain activity recorded during a recollective response. On the other hand, the ERP associated with a hit trial on which the source is not judged correctly presumably reflects brain activity obtained during a response based on familiarity alone. However, other explanations are viable, such as misattribution of the initial learning context, or the retrieval of non-diagnostic contextual information (Mulligan and Hirshman, 1997
).
Two kinds of ERP old/new effects have been observed consistently in the sequential response paradigm described earlier, as well as in other direct memory tasks such as the three-button source memory (source 1, source 2, new) (Senkfor and Van Petten, 1998), and two-button exclusion (target old; nontarget old or new) (Wilding and Rugg, 1997
) recognition memory paradigms. The first old/new effect, with an onset at
300 ms, and a duration of ~400500 ms, has a posterior scalp distribution and tends to be somewhat left lateralized with words as stimuli. The second, either coincident with (Wilding and Rugg, 1997
) or subsequent to (Trott et al., 1997
) the posterior old/new effect is of long duration (to the end of the recording epoch) and has a right-sided, prefrontal scalp distribution. Trott et al. (Trott et al., 1999
) have interpreted the early, posterior old/new effect as being consistent with the retrieval of item content (perhaps devoid of contextual information). The late, prefrontal old/new effect has been interpreted as reflecting the search for and/or retrieval of contextual information (Wilding and Rugg, 1996
). Trott et al. (Trott et al., 1999
) have also suggested that item retrieval and contextual retrieval might be subserved, respectively, by medial temporal and right prefrontal cortical mechanisms [see also (Wilding and Rugg, 1996
)]. The medial temporal lobe interpretation is based on the fact that in dense amnesia due to medial temporal lobe dysfunction, the early, posterior old/new effect is absent or reduced (Johnson, 1995
). The prefrontal interpretation is based, in part, on a large amount of functional neuroimaging data that suggest a role for the right prefrontal cortex in the retrieval of episodic memories (Buckner and Tulving, 1995
; Fletcher et al., 1998
; Wagner et al., 1998
).
Because differences in scalp distribution of an ERP component imply differences in the intracranial generators of those components, one would predict that the scalp distribution of the ERP old/new effect associated with correct source judgments should differ from that associated with incorrect source judgments. This is based on the assumption that retrieving the source correctly involves both familiarity and recollection and hence both the medial temporal and frontal lobes, whereas a failure to retrieve the source involves familiarity only and hence does not receive a contribution from the frontal lobes. However, in the two investigations where this was tested directly (Wilding and Rugg, 1996; Trott et al., 1999
) and correctly by normalizing the data (McCarthy and Wood, 1985
; Ruchkin et al., 1999
), the old/new effects associated with these two behavioral outcomes did not differ in scalp topography. Thus, strong evidence for differential effects of familiarity and recollection on the ERP waveforms has not been obtained to date [however, Rugg and co-workers provided evidence in a paradigm that did not include a source memory component (Rugg et al., 1998
)].
To deal with some of the problems associated with threebutton and sequential response source memory paradigms, one can employ the inclusion/exclusion paradigm developed by Jacoby (Jacoby, 1991). In this task, subjects are asked to study a list of words, e.g. some read and some heard, and then make old/new (inclusion) or heard/not heard (exclusion) choice responses at test. During the exclusion test, for not-heard stimuli, two classes of items need to be excluded, those that were read (referred to as nontarget old items), and new items. Hence, a selective response is made to only one class of studied items (target old), while the other class of studied items (nontarget old) or new items receive the same response. Performance on the exclusion task can only be above chance levels if the two classes of old items can be distinguished; old/new discrimination will not be sufficient. In addition, the assumption is made that responding on the basis of familiarity alone will not yield accurate performance, because target old and nontarget old items are equally familiar. In the exclusion test, which pits recollection against familiarity, subjects must make covert source judgments in order to perform accurately. Therefore, accurate performance on the exclusion task is assumed to be based on the retrieval of contextual information. We will refer hereafter to these two types of recognition memory procedures, inclusion and exclusion, as, respectively, item and source memory tasks.
Wilding and Rugg were the first to record ERPs during a source memory exclusion paradigm (Wilding and Rugg, 1997). Subjects in their investigation studied auditorily presented words delivered by either a male or female speaker. At test, subjects were required to respond to one class of old items (either originally spoken in a male or female voice; designated the target) with one response button and to the other category of old items (designated the nontarget) and new items with the other response button. Given sufficient numbers of trials, this procedure enables ERP averages to be formed to correctly recognized targets and nontargets (both old items), correctly rejected new items and new false alarms, as well as to nontarget false alarms and target misses. Wilding and Rugg recorded the early posterior old/new effect, and the late prefrontal old/new effect to correct trials, but not in association with misses and false alarms (Wilding and Rugg, 1997
). Thus, Wilding and Rugg concluded that both effects reflect processes associated with the recollection of an item in its study context (p. 125).
Two potential difficulties can be raised with respect to the Wilding and Rugg data (Wilding and Rugg, 1997). First, they did not incorporate a simple, old/new recognition or item memory task, so that a direct comparison between the old/new effects from the two tasks could not be made. Hence, they could not have determined whether the two old/new effects were specific to the source paradigm (in which retrieval of context was necessary) or would also have occurred in an item memory paradigm in which source retrieval was unnecessary for above- chance performance. Second, the ERPs to false alarms were averaged across both new and nontarget items that attracted a target judgment. As nontarget items are truly old, whereas new items have never been seen before, this averaging scheme may have precluded the possibility of observing a familiarity effect for old nontarget items that have been assigned to the incorrect category.
To counteract these shortcomings, the current experimental design included both item and source memory tasks. Subjects studied pictures outlined in either red or green and were asked to remember the pictures and their associated colors for a subsequent memory test. They then received old/new recognition (item) and target/other (source) memory test blocks. At test, all pictures were presented outlined in black. During the item memory test, subjects made speeded and accurate old (either red or green)/new judgments, whereas during source memory they made target/other (nontarget, new) judgments. There were sufficient numbers of error trials to separately evaluate ERP averages for target misses and nontarget false alarms. It was expected that during both item memory and source memory blocks, posterior old/new effects of similar magnitude and scalp distribution would be recorded, whereas brain electrical activity related to source search and/or retrieval would be observed only during the source memory task, or would be dramatically reduced during the item memory task. If familiarity is evident in the ERP waveforms, then it was expected that robust old/new effects would be observed not only for correct target and nontarget old trials, but also for old target and nontarget trials on which the source had not been retrieved (i.e. respectively, target misses and nontarget false alarms). In addition, if familiarity and recollection reflect somewhat independent states of consciousness, based on at least partially non-overlapping brain networks, another expectation was that ERP scalp distribution would differ during the source memory portion of the paradigm between old items associated with correct and incorrect covert source categorizations.
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Materials and Methods |
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Sixteen subjects (11 female) between the ages of 20 and 26 were recruited by notices posted within the Columbia Presbyterian Medical Center community. All subjects reported themselves to be in good health and to have no major medical, neurological or psychiatric problems. All subjects signed informed consent, were native English speakers and received payment for their participation.
Stimuli and Procedures
The experimental stimuli were 312 unambiguous line drawings of common objects that were divided into six lists of 52 items each, with lists carefully constructed so that they were equated on category membership, concept agreement, name agreement, familiarity and visual complexity [normative data bases (Snodgrass and Vanderwart, 1980; Berman et al., 1989
; Cycowicz et al., 1997
)]. Statistical analysis of the variables characterizing the picture sets revealed no significant differences among lists (P > 0.10). An additional 52 pictures from the same normative sources, not used in the experimental phases, were used for practice study and test blocks, and as fillers. The experiment was divided into six phases. Each phase consisted of one study and two test blocks (item recognition, and source recognition). In each phase, one of the six lists of pictures was used, with the order of list presentation randomized across phases separately for each subject. Of the 52 pictures in a list, 32 were randomly assigned to the study block, while the remaining 20 were assigned as foils to the test block.
In the study block, the subject viewed 36 pictures (half outlined in green and half in red), including four fillers, two of which were presented at the beginning and two at the end of the block to avoid primacy and recency effects (subjects were not tested on these fillers). For each subject, the picture's color was randomly assigned. To ensure that the subject attended to the picture's color, s/he was asked whether the picture was red or green by pressing one of two buttons. The subject was asked to memorize both the picture and its associated color for a subsequent memory test.
In the item recognition memory test block, the subject viewed a total of 26 pictures outlined in black; 14 new and 12 old (six previously presented in red and six in green). Subjects were asked to press one response button if the item was old and the other if it was new. The numbers of old items differed between the two tasks in order to approximately equate the probability of an old (in the item memory task) or target (in the source memory task) response. During item memory, the proportion of old items was 0.46 (12 of 26) while in source memory, the proportion of target items was 0.38 (10 of 26). Hence, in the source memory test block, the subject viewed a total of 26 pictures outlined in black: 6 new and 20 old (10 previously presented in red and 10 in green). In half of these test blocks, red was defined as the target and, in the other half, green was defined as the target. The subject was asked to press one button if s/he thought the picture was seen during study in the target color, and a second button if s/he thought the picture had been presented during study in the nontarget color, or was new (i.e. had not been seen during study). Figure 1 depicts schematically examples of study and test trial sequences.
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To counterbalance order effects, in half the sessions, item memory preceded source memory testing and, in the other half, source memory preceded item memory testing. Subjects were not informed prior to the study-block which test block would be administered first, or which color would be the target. The sequence of stimuli was separately randomized for each subject.
EEG Recording
EEG (5 s time constant; 50 Hz upper cutoff; 200 Hz digitization rate) was recorded (Sensorium Amplifiers) continuously using an Electrocap (Electrocap International) from 62 scalp sites, including left and right mastoids, referred to nosetip, from extended 1020 system placements (Nuwer et al., 1998). Vertical EOG was recorded bipolarly from electrodes placed on the supraorbital and infraorbital ridges of the right eye, and horizontal EOG was recorded bipolarly from electrodes placed on the outer canthi of the two eyes. Trials containing eye movement artifact were corrected off-line using the procedure developed by Gratton et al. (Gratton et al., 1983). Trials were epoched off-line with 100 ms pre- and 1900 ms post-stimulus periods.
Data Analyses
ERPs were averaged to correctly recognized old and new items during the item memory test blocks, and to correctly recognized target and nontarget old items, as well as new items during the source memory test blocks. When 10 or more trials were available for a given subject and condition, ERP averages were also computed to error trials (e.g. false alarms and misses during the item memory and source memory test phases).
Maps of surface potential activity were computed using a third-order spherical spline interpolation algorithm (Perrin et al., 1989), which uses the average reference (Scherg, 1990
) rather than, for example, the nose or mastoids as reference sites. With this method, the scalp distribution of an ERP component is not influenced as heavily by the reference site used for the original recordings. To compare scalp distributions of ERP surface potential activity between conditions, the data were normalized using the root mean square method described by McCarthy and Wood (McCarthy and Wood, 1985
). This manipulation removes overall amplitude differences between conditions to allow a comparison of the shape of the distribution across the scalp. A significant difference in scalp distribution is revealed as an interaction of a particular variable with electrode location.
The BMDP-4V (repeated measures ANOVA) computer program was used for all analyses. The GreenhouseGeisser epsilon () correction (Jennings and Wood, 1976
) was used where appropriate. Uncorrected degrees of freedom are reported below along with the epsilon value; the P values reflect the epsilon correction. Where appropriate, significant main effects and interactions were followed-up with post hoc analyses using the Tukey honestly significant difference (HSD) test. In addition, two types of planned comparisons were performed, described in the Results section below.
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Results |
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During the study phase, subjects were highly accurate in detecting red (mean percent correct = 98.4) and green (mean percent correct = 98.2) items. Mean reaction time (RT) did not differ between these two response categories (P > 0.10; mean red = 609.5 ms; mean green = 608.2 ms), suggesting that, during the study phase, items outlined in red and green were processed similarly.
Preliminary analyses indicated that there was no difference in memory test performance between pictures outlined in red and green. Therefore, all subsequent analyses were performed on data collapsed across these two classes of stimuli. Table 1 presents the behavioral data during the item memory and source memory tasks. As can be observed, subjects performed well above chance during both types of memory tests, although discrimination (Pr) (Snodgrass and Corwin, 1988
) was significantly lower during the source memory compared to the item memory blocks, as confirmed by t-test [tPr(15) = 6.31, P < 0.0001]. Similarly, the false alarm rate was higher during source memory compared to item memory blocks [tFA(15) = 4.70, P < 0.0001], but there was no difference in the bias measure (Br) (Snodgrass and Corwin, 1988
) [tBr(15) = 1.55, P > 0.10]. Values of Br <0.5 indicate that subjects responded conservatively i.e. they chose to respond new when uncertain.
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As for the behavioral data during the study phase, there were no systematic differences between the ERPs elicited by pictures outlined in red and green, suggesting that they were processed similarly by the brain.
Memory Test Waveforms
For the item memory task, the analysis comprised hit (correct old) trials (M = 60.7 trials) and correct rejection (correct new) trials (M = 78.0) but neither type of error trial (false alarms or misses) because they occurred too infrequently to provide stable data. For the source memory task, the analysis comprised target old trials (M = 45.3), nontarget old trials (M = 45.0), new trials (M = 34.1), target incorrect trials (M = 14.1) and nontarget incorrect trials (M = 13.7). There were too few new error trials in the source memory task (i.e. false alarms) to permit statistical analysis.
Figure 2 depicts the grand mean ERPs associated with correct old and new responses during the item (left) and source (right) memory tasks. For ease of viewing, the data are shown at 24 of the 62 scalp locations on a schematic figure of the head. These electrode sites provide good coverage of the scalp, and capture the major effects of interest. For the source memory task, the ERPs elicited by target and nontarget old items are depicted. As can be seen, the waveforms are characterized by a series of early negative and positive visual evoked potential components (largest at the occipital scalp sites) between about 100 and 300 ms that do not appear to differ between the item and source memory waveforms. The ERPs elicited by both new and old items are characterized by a large-amplitude positive component (at ~500 ms peak latency). This positivity is also larger for old compared to new items in both tasks, and most likely can be identified with the posterior old/new effect observed by previous investigators during similar kinds of memory tasks (Wilding and Rugg, 1996
; Trott et al., 1999
). The ERPs elicited by target and nontarget old items in the source memory task do not appear to differ dramatically.
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The ERP data were quantified using averaged voltages corresponding to areas of difference observed in the grand mean and individual subject mean ERPs. These spanned the early posterior and late posterior old/new effects. For each of these old/new effects, two windows were defined. For the early old/new effect, these values were 260360 ms and 415615 ms [roughly corresponding to the N400 and P3b portions of the waveform observed in many previous ERP studies of recognition memory (Wilding and Rugg, 1996; Senkfor and Van Petten, 1998
; Paller et al., 1999
; Trott et al., 1999
)]. Hereafter, these will be referred to as early1 and early2. For the late old/new effect, the measurement windows were 700950 ms and 9551200 ms. Hereafter, these will be referred to as late1 and late2. To assess the effects discerned from visual analysis above, a series of ANOVAs was performed. To capture any anterior/posterior and/or left/right asymmetries, these analyses were performed on the data recorded from 24 scalp sites along saggital (left, midline, right) and anterior/posterior planes. The 24 scalp sites included on the left, FP1, F3, FC3, C3, CP3, P3, PO1 and O1; on the midline, FPz, Fz, Cz, CPz, Pz, Poz and Oz; on the right, FP2, F4, FC4, C4, CP4, P4, PO2 and O2.
Because of the long latency of the Old/New and Task effects observed in Figures 25, all of the analyses described below were also performed on two additional measurement intervals, 12051500 and 15051800 ms. The great majority of significant effects were identical to those observed for the late1 and late2 indices (and will not be discussed further), suggesting that, from ~900 ms onwards, the latency regions encompassed by the late negativity reflected functionally and topographically homogeneous brain activity. The first analysis employed the data for the ERPs associated with correct old and new responses from the item memory task and the ERPs associated with correct target old and new responses from the source memory task. The results of the Task (Item memory, Source memory) by Old/New by Saggital Plane (left, midline, right) by Anterior/Posterior (Frontal Pole, Frontal, Fronto-central, Central, Centro-parietal, Parietal, Parieto-occipital, Occipital) ANOVA on these data are presented in Table 3
. Three-way interactions of Task and/or Old/New with Electrode Location (as manifested by interactions with Saggital Plane and Anterior/Posterior Region) are only considered in the scalp topography section below, after normalization of the data to enable unequivocal interpretation (Table 4
). The main effects of Saggital Plane and Anterior/Posterior Region were not interpreted as, by themselves, they do not reflect memory- related differences.
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To summarize briefly, the early, posterior Old/New effect did not differ between item and source memory tasks, whereas, for the later negative Old/New effect, greater amplitudes were consistently elicited during the source memory procedure. Moreover, differences between tasks were larger at posterior scalp sites with no evidence of the robust left/right asymmetries or right-sided prefrontal old/new effects that have been observed previously (Wilding and Rugg, 1996; Trott et al., 1999
).
In the second analysis, using planned comparisons, the ERPs from the source memory task elicited by old items associated with the same response hand (depicted in the first two columns of Figure 5) were compared between correct and incorrect source judgments. The ANOVAs were constructed identically to those described above. The Target Correct versus Nontarget Incorrect by Saggital Plane by Anterior/Posterior Region revealed no reliable main or interaction effects with Condition, as was also the case for the Nontarget Correct by Target Incorrect by Saggital Plane by Anterior/Posterior Region ANOVA (Fs < 2.69, Ps > 0.10), indicating that these classes of old items did not differ.
In the third analysis, a series of planned comparisons on the data from the source memory task contrasted separately the ERPs associated with old items (target correct, target incorrect, nontarget correct, nontarget incorrect) with the ERPs elicited by correctly categorized new items, in order to determine if each yielded robust old/new effects. Again, the ANOVAs were identical to those detailed immediately above (Old/New by Saggital Plane by Anterior/Posterior Region). With the exception of the early1 window, which did not consistently produce reliable old/new effects, the four ANOVAs revealed significant old/new main effects for each of the remaining three measurement windows [Fs(1,15) > 5.26, Ps < 0.05]. Primarily for the two late indices, the ANOVAs also revealed significant Old/New by Saggital Plane [Fs(2,30) > 4.9, Ps < 0.05] or Old/New by Anterior/ Posterior Region [Fs(7,105) > 5.0, Ps < 0.05] interactions. Post hoc testing of the Old/New by Saggital Plane interaction indicated that the differences between old and new ERPs were greatest at the midline; for the Old/New by Anterior/Posterior Region interaction, post hoc tests revealed that the old/new differences were greatest between parietal and occipital scalp.
In brief, whether an old item was associated with a correct or incorrect source judgment, the early and late posterior indices could not be differentiated on the basis of amplitude. Further, robust old/new effects were found for both correct and incorrect target and nontarget items in the source memory task. Again, no reliable left/right asymmetries or right-sided, prefrontal old/new effects were observed.
Scalp Topography
Figure 6 depicts the old minus new difference waveforms for correct old/new decisions in the item memory task and correct and incorrect judgments in the source memory task. As can be observed, for the early, posterior old/new effect, the waveforms associated with incorrect source judgments show a more posterior scalp distribution than those associated with correct judgments of source, or with correct old/new judgments in the item recognition task. The late, negative old/new effect is markedly larger in the source memory task. Both of these effects can be clearly observed in Figure 7
, which depicts the surface potential (SP) maps for the four measurement windows, early1 through late2, and are based on the data depicted in Figure 6
. The three rows depict, respectively, the scalp distributions associated with correctly recognized old pictures during the item memory task, correctly recognized old pictures (with correct source judgments) during the source memory task, and old pictures whose source was incorrectly judged. The distributions depicted in the latter two rows were computed on the ERPs collapsed across target and nontarget items. This was done to increase the signal-to-noise ratio and was based on the fact that there were no differences between target and nontargets (whether correct or incorrect) for any of the amplitude analyses. Moreover, separate Target and Nontarget ANOVAs on the normalized data revealed identical differences in scalp distribution between correct and incorrect trials as reported below for the collapsed data. The topography of the early1 phase is characterized by an anterior scalp distribution during both item memory and source memory trials in which the initial color was correctly judged. By contrast, the scalp distribution associated with source memory trials for which color was incorrectly judged shows a more posterior distribution. Similarly, the topographies of the early2 index associated with item and correct source memory trials are more frontally oriented than those associated with incorrect source memory judgments. The distributions for the late1 and late2 measurements associated with both types of source memory trials show highly focused negative activity over parieto-occipital scalp sites and, unlike the two early indices, do not appear to differ for correct and incorrect source memory trials. On the other hand, the late1 index for item memory trials is not nearly as large or as clearly focal as those recorded during the source memory task.
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To determine whether the scalp distributions of the early and late posterior old/new effects differed between the item and source memory tasks, a second analysis was performed, in which the normalized data were compared between the first and second rows depicted in Figure 7 (bottom of Table 4
). The two early indices did not differ topographically between tasks, as can clearly be observed in Figures 6 and 7
. However, the Task by Electrode Location interaction was significant for the late1 index, but not for the late2 interval. As can be seen by inspection of Figures 5 and 6
, although late1 negative activity was clearly posteriorly distributed, the largest differences between tasks (as assessed by post hoc testing) occurred for the positive aspect of the distributions over frontal scalp locations. The item task showed relatively greater positivity at these sites than the source memory task.
In summary, unlike the amplitude data, the topographic data suggest that there is an ERP sign of recollection, because there was a reliable trend for the early, posterior old/new effects associated with correct source judgments to be more frontally oriented than those associated with incorrect source judgments. As observed in Figure 7, the scalp distribution of the late1 index of negative activity associated with trials on which a covert source judgment had to be made differed from that associated with trials on which no such source judgment was necessary (item memory), suggesting that the processes reflected by this activity differed in the two tasks.
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Discussion |
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The Early, Posterior Old/New effect.
This old/new activity appears highly similar to the posterior old/new effects recorded by others in recognition memory paradigms with (Wilding and Rugg, 1996, 1997
; Senkfor and Van Petten, 1998
; Trott et al., 1999
) and without (Rugg and Nagy, 1989
; Friedman et al., 1993) a source memory component. In previous source memory investigations, however, this activity has been larger when associated with a hit trial for which the source was correctly judged compared to a hit trial on which the source was incorrectly judged (Wilding and Rugg, 1996
; Senkfor and Van Petten, 1998
; Trott et al., 1999
). On this basis, Wilding and Rugg concluded that it reflected recollection, as the hallmark of a recollective response is the retrieval of the context associated with the initial learning episode (Wilding and Rugg, 1996
). Even though this early old/new activity has been found to be greater for correct than for incorrect source judgments, no differences in scalp distribution of this activity have been observed between the ERPs associated with correct and incorrect source judgments (Wilding and Rugg, 1996
; Trott et al., 1999
). As some two-process theorists argue for distinct cognitive and neurological aspects for familiarity and recollection, the failure to find topographic differences between trials presumably based on recollection (hit + source correct) and those presumably based on familiarity (hit + source incorrect) argue against an effect of familiarity on the ERP waveforms. In the current data, considering magnitude alone, the early old/new effect also does not appear to qualify as a sign of recollection, as it was as large in association with correct as it was with incorrect source judgments. On the other hand, based on scalp topography, the current data provide more compelling evidence for these two processes ERPs on trials for which source was correctly attributed showed more frontally oriented scalp topographies than those on trials for which source was incorrectly judged (or not retrieved) during the source memory task.
These data suggest that the more posterior scalp topography associated with error trials might reflect a decision based on familiarity. Although there were instances when only a posterior scalp distribution was observed (error trials during the source memory task; see Fig. 7), there were no instances of a purely frontal scalp topography. Moreover, during item memory blocks, in which both familiarity and recollection are assumed to work in concert (Jacoby et al., 1993
), the scalp distribution of the old/new effect associated with correctly recognized pictures showed both frontal and posterior aspects. Therefore, the data argue for a redundant relationship between familiarity and recollection, such that recollection always includes familiarity, but familiarity can occur in the absence of recollection [for discussion see (Jones, 1987
; Jacoby et al., 1993
; Joordens and Merikle, 1993
; Knowlton and Squire, 1995
; Cowan and Stadler, 1996
)].
For our interpretation to be viable, it must be assumed that the lack of frontal scalp activity indicates a lack of a frontal lobe contribution to the early old/new effect, whereas the presence of such activity on correct trials implies the presence of a frontal lobe generator. Although, based on scalp distribution alone these assumptions are tenuous, the current data are consistent with a large variety of neuropsychological (Schacter, 1987) and neuroimaging data (Nolde et al., 1998
) that have demonstrated contributions of the prefrontal cortex to reinstatement of the initial learning context, a critical sign of recollection-based retrieval.
The early old/new effect onset occurred several hundred milliseconds prior to the old/new decision in item memory blocks and the target/nontarget decision in source memory blocks. Hence, the relationship between the onset and peak of the early old/new activity and the generation of mean reaction time raises the possibility that it could be one of the brain events causally related to the decision to respond (Ritter et al., 1972). If this were the case during source memory blocks, these data would suggest that sufficient information about source to render a target/nontarget decision would have been available during the interval when the early old/new effect was active at the scalp. On this basis, the early old/new effect could reflect, at least in part, some aspect of recollection. The fact that this early, posterior old/new activity is absent or reduced in patients with dense amnesia due to lesions of the medial temporal lobes (Johnson, 1995
), patients whose ability to recollect is severely compromised, is consistent with this interpretation.
A relationship between the medial temporal and frontal lobes that is consistent with the current data has been advanced by Moscovitch (Moscovitch, 1994). In Moscovitch's model, the output of hippocampally mediated retrieval is relayed to a frontal lobe mechanism. This frontal lobe mechanism is then responsible for working with the information retrieved by the hippocampal system. The frontal lobe system serves to make this information conscious and to place it in its particular spatiotemporal context (i.e. source), data that are not necessarily retrieved by the hippocampal system. In Moscovitch's model, the output of the hippocampal system is associated with an automatic, non-strategic judgment of prior occurrence (Moscovitch, 1994). The frontal aspect of this old/new effect (presumably mediated by prefrontal cortex) would be associated with a strategic, effortful search and/or retrieval of at least some source information. That is, the prefrontal cortex is responsible for organizing strategically the output of the hippocampal system. On this view, the current early, posteriorly distributed old/new effect observed in association with error trials would reflect an obligatory recognition response devoid of contextual information (a pure hippocampal retrieval). By contrast, the presence of posterior as well as frontal activity in the scalp distribution associated with correct trials would reflect both an obligatory recognition response and one in which at least some contextual information is retrieved under direction of the prefrontal cortex.
The use of pictures in the current study may have led to the presence of large-amplitude old/new effects in association with error trials. Pictures are known to be remarkably resistant to forgetting, perhaps due to the fact that pictures have distinct sensory codes (Nelson, 1979) and may be encoded both perceptually and semantically (Paivio, 1986
). On these bases, pictorial stimuli may be more likely than words to engender an automatic recognition response, resulting in robust old/new effects for both target misses and nontarget false alarms.
The Late, Posterior Old/New Effect
Unlike previous ERP studies with a source memory component (Wilding and Rugg, 1996, 1997
; Senkfor and Van Petten, 1998
; Trott et al., 1999
; Wilding, 1999
), there was little evidence of a right-lateralized prefrontal old/new effect in these data. Rather, a late-onsetting, symmetrical, parietal-occipital negativity was much more prominent in the source memory compared to the item memory task. The presence of this activity in the current data may be due to differences in experimental paradigms and/or stimulus characteristics. However, the observation of this late, negative old/new effect in the current investigation is most probably not due to the retrieval of pictures per se (as opposed to words) for a few reasons. First, this activity was not observed with old pictures during the item memory task. Second, it was also not observed with new items in either task. Third, previous investigators who also presented pictures during study and test (Friedman, 1990; Schloerscheidt and Rugg, 1997
) did not observe this kind of negative brain activity.
In the current study, pictures outlined in color were presented, while in previous studies words were presented either in the auditory or visual modalities. Therefore, the use of a distinct perceptual attribute to define source (i.e. color) may have led to the presence of the large-amplitude occipital negativity (consistent with visual cortical generators) that would have tended to reduce markedly any frontal positive activity that would have been elicited in this task. This negativity was considerably larger during source memory compared to item memory blocks (and showed a different scalp distribution), suggesting that it reflects the activity of brain generators that have something to do with source search and/or retrieval. As the nature of the contextual information was perceptual (rather than semantic, for example), it is reasonable to assume that this kind of information would have been stored in the cortical regions that originally processed the information (i.e. occipital cortex).
The occipitally focused scalp distribution of the current negativity is compatible with cerebral blood flow data reported by Schacter and colleagues (Schacter et al., 1996), who demonstrated that, in addition to activation of the medial temporal region during retrieval, correct recognition of events originally presented aurally was associated with activation of the superior temporal region (i.e. auditory cortex). Taken together, the results are consistent with the principle that information processed in a given cortical area during study is stored as a representation in similar cortical regions, and is subsequently retrieved from those regions, perhaps under the direction of the prefrontal cortex (Squire and Kandel, 1999
).
The peak latency of the late old/new effect (between ~800 and 900 ms; Figs 2 and 4) is consistent with its potential role in source search and/or retrieval, as peak latency occurred at about the same time as mean reaction time (see Table 2
). As the negative activity onset occurred as the early old/new effect was returning to baseline, one speculative hypothesis is that sufficient time would have elapsed for this late negative activity to have reflected brain activity related to an attempt to reinstate the initial image along with its associated color during source memory blocks (Farah et al., 1988
), i.e. a continued search and/or evaluation of the correctness of the behavioral response. This interpretation would be consistent with the fact that the occipitally prominent negative activity was present even in those ERPs that were associated with trials on which an incorrect, covert source decision had been made (i.e. target misses and nontarget false alarms).
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Conclusions |
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Notes |
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Address correspondence to: Dr Yael M. Cycowicz, Cognitive Electrophysiology Laboratory Unit 6, New York State Psychiatric Institute, 1051 Riverside Drive, New York, NY 10032, USA. Email: yc60{at}columbia.edu.
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References |
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