A spatio-temporal comparison of semantic and episodic cued recall

Cognitive Brain Research 7 Ž1998. 119–136

Research report

A spatio-temporal comparison of semantic and episodic cued recall and recognition using event-related brain potentials Ray Johnson Jr. ) , Kurt Kreiter, John Zhu, Britt Russo Department of Psychology, Queens Colleger CUNY, 65-30 Kissena BlÕd., Flushing, NY 11367, USA Accepted 14 April 1998

Abstract The event-related brain potential ŽERP. was used to spatially and temporally map the brain areas active as a function of type of recall Žsemantic vs. episodic. and episodic retrieval mode Žrecall vs. recognition. while difficulty of episodic recall was manipulated. ERPs were recorded from 32 scalp sites in 12 subjects, along with behavioral accuracy and recall speed. The results revealed that different but overlapping patterns of ERP activity were elicited during semantic and episodic recall. Recall of both types of information was characterized by ERP activity over left inferior frontal, central, bilateral temporal and posterior inferior brain areas. Compared to semantic recall, episodic recall elicited more activity over the frontal poles and right frontal scalp. Different but overlapping patterns of ERP activity were also found as a function of episodic retrieval mode. While episodic recall and recognition showed similar activity over the frontal poles and central scalp, there was no left inferior frontal activity elicited during recognition and no large, topographically widespread, late positive component ŽLPC. elicited when the same words were recalled. Manipulation of episodic recall difficulty and analysis of trials when recall failed indicated that these task Ži.e., episodic vs. semantic. and retrieval mode Žrecall vs. recognition. differences in ERP activity were not likely to be due to differences in task difficulty. The results are discussed in terms of processes that the ERP activity may reflect and their similarity to results of PET studies of semantic and episodic retrieval. q 1998 Elsevier Science B.V. All rights reserved. Keywords: Episodic memory; Semantic memory; Recognition; Recall; Event-related potentials; ERPs

1. Introduction Long-term memory is generally viewed as consisting of a collection of separate but interacting systems that comprise two broad categories: explicit and implicit w11x. The explicit category refers to consciously recollected memories while the implicit category refers to a collection of highly specialized stores whose contents do not require conscious access. Explicit memory has been subdivided further into episodic and semantic stores, with the former consisting of personal memories that include specific spatio-temporal information about the context in which the event occurred w43x. Semantic memory, in contrast, consists of a fact-based store for general knowledge that is not associated with contextual information. Retrieval of episodic memories is often assessed with tests that make direct reference to a previous learning ) Corresponding author. Fax: q1-718-997-3257; E-mail: [email protected]

episode Že.g., recognition, recall.. For recognition tests, subjects are exposed to a series of items and, after some delay, are tested with lists that include these ‘old’ items randomly intermixed with new items. The subject’s task is to decide whether each item is old or new. Recall tests require subjects either to generate the old items with no cue Žfree recall. or from a fragment of the item Žcued recall.. Thus, while recall is generally more difficult than recognition, these two retrieval modes differ in the extent to which the subject must generate their own information about items already in memory. In contrast to the large number of behavioral studies, relatively less is known about the brain systems underlying each type of retrieval. In recent years, brain imaging studies using positron emission tomography ŽPET. have provided more specific information on which particular brain areas are involved in retrieving episodic and semantic memories Žsee Refs. w8,10x for reviews.. These results indicate that episodic recognition is associated with increased blood flow in prefrontal cortex, with more activation in right hemisphere than in

0926-6410r98r$ - see front matter q 1998 Elsevier Science B.V. All rights reserved. PII: S 0 9 2 6 - 6 4 1 0 Ž 9 8 . 0 0 0 1 7 - 2

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R. Johnson Jr. et al.r CognitiÕe Brain Research 7 (1998) 119–136

the left, anterior cingulate cortex, bilateral precuneus, parietal cortex and cerebellum, particularly left hemisphere. Episodic recall has been found to produce a similar pattern of brain activation, although cued recall tasks have been reported to produce more activity in left prefrontal areas than recognition w5–7,31,40x. A recent PET study comparing recall and recognition of paired associates in the same subjects revealed that recall was associated with greater blood flow in anterior cingulate cortex, cerebellum and subcortical areas than recognition w9x. In contrast, recall of items from semantic memory was associated with increased blood flow in left inferior prefrontal cortex and anterior cingulate cortex w10x. Further, in word-stem cued recall paradigms, cerebellar activation has also been reported w5,7x. Although blood flow studies provide good information regarding the location of activated brain areas, they provide no information on the temporal course of these activations. Because of their high temporal resolution and ability to reveal even momentary changes in patterns of brain activation, the event-related brain potential ŽERP. technique is ideally suited to provide insights into the timing of the neural processes underlying retrieval of information from long-term memory. Consequently, a number of ERP studies have demonstrated differential ERP responses depending on the study status of the items being recognized. That is, correctly recognized old words elicit a larger late positive component ŽLPC. in the interval between 400–900 ms than previously unstudied Ži.e., new. words Žsee Refs. w19,36x for reviews.. More important, this ‘oldrnew effect’ does not occur when old words are miscategorized as new or when new words are miscategorized as old w14,20,39,45x, a finding consistent with the idea that the oldrnew effect reflects an explicit memory process. Recent ERP studies have found that the oldrnew effect consists of at least three subcomponents that differ in their spatial and temporal properties: Ž1. a brief left frontal subcomponent Ž400– 500 ms. w20,39,41x, whose function is not known; Ž2. a left parietal – occipital subcom ponent Ž 500 – 900 m s . w20,26,37,39,41,42,45,46x, which Allan and Rugg w2x suggested was related to conscious recollection of studied items; and Ž3. a right frontal subcomponent Ž500–1000 ms., which has been suggested to represent either the retrieval of contextual information or processes that operate on the retrieved information w20,45,46x. As noted by Johnson et al. w20x, these three patterns of ERP activity are spatially similar to the areas of increased blood flow in left frontal, precuneus and right frontal cortices, respectively, observed in PET studies of episodic recognition. While recognition-related processes have been well studied by ERP researchers, recall has received considerably less attention. Only two recent reports describe the recall-related ERP activity elicited in a word-stem cued recall paradigm w1,2x. In both studies, subjects were given lists of word stems, only half of which could be completed with a word from a previously studied list. Subjects were

instructed to first perform an episodic memory retrieval task Ži.e., try to recall a word from the studied list. and, if that retrieval attempt failed, to then perform a semantic memory retrieval task Ži.e., retrieve the first word that came to mind.. These authors reported that the sole ERP effect was a long-lasting Ži.e., 300–1400 ms. positive shift, maximal over anterior scalp, that was elicited during episodic retrieval relative to semantic retrieval. In a follow-up study, Allan and Rugg w2x compared the ERP activity associated with recall and recognition. They replicated their earlier recall finding and showed that the distribution of the sustained frontal positivity elicited during the cued recall task was different from the sustained positivity elicited during recognition. While the results from Allan et al. w1x and Alan and Rugg w2x suggest that the ERP activity elicited during episodic retrieval is dependent on the type of cue Ži.e., word stem vs. the entire word., some questions remain due to the nature of their experimental design. That is, their design is confounded since, on the semantic retrieval trials, subjects performed two different and successive retrieval tasks Ži.e., an episodic retrieval task of unspecified duration followed by a semantic retrieval task of unspecified duration.. Thus, although frequently used in behavioral paradigms, this design creates considerable problems in ERP studies, which provide a continuous record of brain activity. This procedure therefore confounds ERP results since the averages will contain the ERP activity related to the initial episodic retrieval task in addition to that of the subsequent semantic retrieval task. Further, the extent and timing of the overlapping brain activity would vary randomly from trial to trial depending on when the subjects decided to quit the episodic retrieval task, introducing an unknown amount of overlap between the episodic- and semantic-related ERP activity. To complicate further any interpretations of the mixed-trial data, both studies w1,2x introduced another possible confound. That is, on trials when episodic recall was successful Ži.e., those not followed by semantic retrieval operations., subjects were required to perform another, different task since they had to make an overt oldrnew recognition judgment shortly after the end of the recording epoch. Because subjects knew that, on the episodic recall trials, they would soon be asked to make the oldrnew judgment, there is no way of determining if, or how often, subjects actually waited to make this judgment, particularly since they could just as easily make that decision while awaiting the end of the epoch. Consequently, with this unblocked experimental design, the ERP averages designed to reveal semantic memory retrieval may well be contaminated with the brain activity associated with episodic retrieval processes and contamination of the episodic recall averages with the brain activity associated with the oldrnew judgment cannot be ruled out. Thus, given that subjects generally performed more than one task on a given trial, there is no way either to disentangle the ERP activity associated with each


specific task or to determine with certainty which ERP activity reflected episodic retrieval and which reflected semantic retrieval. Given that PET studies routinely reveal increased blood flow in a variety of brain areas during semantic and episodic recall, we hypothesized that, when the effects of each type of retrieval were disentangled, more complex patterns of ERP activity would be found than have been reported previously. Also, it was expected that different retrieval modes Ži.e., recall vs. recognition. would be associated with different patterns of ERP activity. Thus, the purpose of the present study was to characterize the timing and topography of the ERP activity associated with semantic and episodic cued recall and to compare the brain activity across retrieval modes by comparing recall- and recognition-related ERP activity. In order to observe each type of retrieval individually, without introducing the confounds outlined above, a blocked experimental design was used in which the ERP activity associated with retrieval from the different explicit memory systems Ži.e., episodic vs. semantic. and both retrieval modes Ži.e., recall vs. recognition. was elicited in different conditions. The use of a blocked experimental design also permitted us to compare the brain activity elicited by successful and unsuccessful retrieval. The data reported here were collected as part of a larger study on source memory that involved having subjects learn a word list to level of 90% free recall prior to the recording session. Comparing the recall-related ERP activity elicited by this well-learned ‘Home’ list with that elicited by the list acquired during the experimental session allowed us to characterize the presence and extent of any effects of retrieval difficulty on ERP activity.

2. Materials and method 2.1. Subjects Sixteen graduate and undergraduate students Ž10 females. at Queens College were paid US$10.00rh for their participation. The data from four subjects were discarded since, due to excessive eye movements, they did not have a sufficient number of artifact-free trials in each average category. The ages of the remaining 12 subjects Ž8 females. ranged from 21 to 32 Žmean s 25.4 years.. All were right-handed native English speakers who had normal or corrected-to-normal vision. Subjects were thoroughly briefed about the nature of the experiment and signed informed consent was obtained from each in accord with Queens College Institutional Review Board procedures. 2.2. Experimental design and procedure One week before the experimental session, subjects were given a list of 80 unrelated words to memorize

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ŽHome list.. On the day of the recording session, subjects were required to demonstrate successful recall of at least 90% of the 80 Home list words in order to begin the experiment. During the experiment, subjects learned a second list of 80 unrelated items ŽLab list.. Episodic recall was tested in two conditions in which subjects were presented with word stems that, in separate series, they were to complete with a word from the Home or Lab list. Semantic recall was tested in a third condition in which subjects completed the word stems with the first word that came to mind. Each cued-recall condition used a unique and non-overlapping list of 80 three-letter word stems, with each stem belonging to at least three English words. Thus, subjects could not complete a stem in the semantic series with a word from either episodic list and there was no interference between the two episodic lists. After electrode placement, subjects were seated in a dimly lighted room in front of a computer monitor. In different series, subjects were instructed to complete the randomly ordered 80 three-letter word stems with words either from the Home list ŽEpisodic-Easy. or with the first word that came to mind ŽSemantic.. The word stems were presented on the CRT and subjects were instructed to press one button on a response box as soon as they retrieved a proper completion and then to remember their answer. The key press, whenever it occurred, terminated the presentation of the stem stimulus, which could remain on the screen for a maximum of 4 s. Between 500 and 1000 ms after the end of this 4-s interval, the stem stimulus reappeared in red letters, signalling subjects to respond verbally with the word that they recalled. Overall, trial duration averaged 8.5 s Žrange 8–9 s.. Next, subjects learned a second list of 80 words ŽLab list. in four alternating study and recognition test series, using different lists of new words in each recognition test. In the study series, words were presented Žwhite on a black background. for 300 ms with an average inter-trial interval ŽITI. of 2750 ms and the subjects’ task was to try to remember the words. Encoding strategy was not controlled during learning of the Lab list because it could not be controlled definitively for the Home list. Following a short break Žapproximately 2 min., subjects’ recognition memory was tested in a series containing 80 old and 80 new words Ž300 ms duration, 2750 ms average ITI.. The subjects’ task was to decide whether each word was old or new and press one of two buttons with their left and right thumbs as quickly as possible. After the fourth recognition test, subjects performed a cued recall task on the Lab list words, using the same procedure as in the recall conditions described above. The word lists were drawn from 10 lists constructed by randomly selecting words, consisting of 4–7 upper case letters, from a master list. All 10 lists balanced for word frequency. Item effects were obviated by dividing subjects randomly into two groups such that one-half learned one list as the Home list and another list as the Lab list, with

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the list assignments reversed for the other half. A third list, having the same characteristics as the other two, was used to provide word stems for the semantic recall condition. The pairing of responding hand with the old and new response buttons was counterbalanced across subjects.

2.3. ERP recordings and quantification ERP activity was recorded from 32 sites, all referred to a left mastoid electrode ŽM1., using tin electrodes embedded in an elasticized cap. The sites ŽFp1, Fp2, F7, F3, Fz, F4, F8, Fc5, Fc1, Fc2, Fc6, T7, C3, Cz, C4, T8, Cp5, Cp1, Cp2, Cp6, P7, P3, Pz, P4, P8, O1, O2, Cb1, Cb2, M2, E1, E2. were located in accord with the American Electroencephalographic Society guidelines w3x. To reduce the presence of electromyographic artifacts, the Cb1 and Cb2 electrodes were placed 1.2 cm above their standard International 10–20 System locations. Eye movements ŽEOG. were recorded from above ŽFP1. and 2 cm below the outer canthus of the left eye ŽE1. and trials contaminated with EOG artifacts Žsignals greater than 50 mV during any 6 sampling points. were excluded from the averages. Subjects were grounded with a forehead electrode. During averaging, all scalp-recorded activity was digitally re-referenced to an average of the M1 and M2 Žleft and right mastoid, respectively. sites. The EEG was amplified 20,000 times with a bandpass of 0.01–35 Hz Žy3 dBroctave.. The EEG sampling rate was 100 Hz and the sampling epoch was 2150 ms for recognition series and 4150 ms for recall series, beginning 150 ms prior to stimulus onset. To maximize the number of artifact-free trials, the averages for the recall conditions were restricted to 2 s post-stimulus. ERP activity was quantified in one of two ways. For questions regarding the behavior of specific components, waveform areas were quantified over temporal epochs designed to capture maximally the activity of that particular component. For questions concerning the onset andror timing of different patterns of ERP activity, waveform areas were calculated in successive 100-ms intervals over the interval of interest. For both methods, activity in the 150-ms baseline was subtracted from the measures. The area data from each type of analysis were analyzed in separate two-way repeated-measures ANOVAs using the factors: Condition ŽSemantic, Episodic-Easy, Episodic-Difficult. and Electrode Ž31.. Similar ANOVAs were done within the episodic conditions to compare the ERP activity elicited on completed and uncompleted stem trials. Additional repeated-measures ANOVAs were done on the RT and accuracy data using the same design, without the electrode factor. In all cases, ANOVA results were corrected using the Greenhouse–Geisser epsilon correction procedure and only the epsilon-corrected df, rounded down to the nearest whole number, are presented.

2.4. Analyses of component scalp topographies The topographic characteristics of the ERP were displayed visually by calculating contour maps of the voltages and current source densities ŽCSD. using the spherical spline method of Perrin et al. w28x. The CSDs were calculated on ERP waveform areas within specified windows Žrelative to the 150-ms baseline. using data from all 32 sites. CSD analyses, which provide reference-free images of scalp ERP activity with increased spatial resolution, reveal the presence of generator activity located near the foci indicated in the maps. Hence, a comparison of CSD and isopotential Ži.e., voltage. maps provides an indication of the relative contribution of local and more distant neural sources to the ERP waveform. The presence of possible topographic differences between conditions, signifying that different patterns of neural generator activity were present, is revealed by significant interactions between the experimental effects and the electrode factor in an ANOVA. In some cases, however, significant interactions can result from amplitude differences alone, with no change in scalp distribution w23x. Thus, topographic profile comparisons were used to determine whether amplitude measurements, obtained at different latencies or in different experimental conditions, reflected the presence of more than one pattern of brain activity. To ensure that the topographic comparisons were confined to shapes alone, the amplitude data in each profile comparison were first scaled so that the root-meansquare ŽRMS. of the across-subject average amplitudes from the different conditions were the same Žw23x and see Refs. w17,18x.. If topographic differences remain after scaling the data, this is revealed by a significant interaction between the two factors Že.g., electrode and task. in a Greenhouse–Geisser epsilon-corrected ANOVA. Note that, since the topographic profile comparisons are calculated on voltage measures, topographic differences should be referred to the waveforms andror potential maps, and not to the CSD maps.

3. Results 3.1. BehaÕioral data As shown in Table 1, cued-recall performance differed significantly across conditions w F Ž1,18. s 102.8, p 0.00001x. Planned comparisons revealed that significantly more word stems were completed in the Semantic condition than in the Episodic-Home condition w F Ž1,11. s 53.6, p - 0.00005x, which in turn elicited more successful completions than the Episodic-Lab list stems w F Ž1,11. s 178.2, p - 0.00001x. Note that, since each list consisted of a unique set of word stems, performance differences between the two episodic recall lists should not be affected by interference from other episodically learned words.


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Table 1 Mean ŽS.D.. percent recall and recognition performance and reaction time Žms. as a function of condition Episodic-Difficult ŽLab list.

Episodic-Easy ŽHome list.

Semantic

Recall % Correct completions Reaction time

47.9 Ž11.5. 1476 Ž789.

76.3 Ž9.7. 1083 Ž688.

95.9 Ž3.3. 819 Ž428.

Recognition % Hits Reaction time % Hits—false alarms

70.2 Ž11.9. 701 Ž176. 55.1 Ž10.2.

There were also significant differences in recall speed, as measured by RT, across conditions w F Ž1,20. s 49.9, p 0.00001x ŽTable 1.. Planned comparisons showed that word stems elicited faster completions in the Semantic condition than in the Episodic-Home condition w F Ž1,11. s 44.2, p 0.00005x, which in turn elicited faster completions than the

Episodic-Lab list stems w F Ž1,11. s 79.5, p - 0.00001x. On the basis on these performance differences, the recall conditions for the Home and Lab list words will be referred to as the Episodic-Easy and Episodic-Difficult conditions, respectively. To determine if there were performance differences across retrieval modes, an ANOVA was

Fig. 1. Across-subject ERP averages elicited by the word stems at 31 electrode sites in the Semantic Žsolid lines., Episodic-Easy Ždotted lines. and Episodic-Difficult Ždashed lines. cued recall conditions. In this and subsequent figures, stimulus onset is denoted by the vertical line in each waveform frame and positive voltages are represented by downward deflections.

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done to compare percent recognition, corrected for guessing Ži.e., Hits—false alarms., during the first recognition test with percent recall of the Lab list words Žobtained after the fourth recognition series.. This test revealed that recall of Lab list words was only marginally worse than corrected recognition performance Ži.e., 38.3% vs. 44.1%. w F Ž1,11. s 4.0, p s 0.07x. However, retrieval speed, as indicated by RT, was more than twice as fast during recognition as during recall Ži.e., 701 ms vs. 1476 ms. w F Ž1,11. s 110.9, p - 0.00001x. 3.2. ERP data 3.2.1. Semantic Õs. episodic recall A complex pattern of ERP activity was elicited between 200 and 2000 ms by the word stems in all three cued recall conditions ŽFig. 1.. These data reveal that, despite significant differences in behavioral accuracy and speed, the ERPs elicited in all three recall conditions were quite similar. In all three conditions, the waveforms were characterized by: Ž1. a negative peak, between 250 and 600

ms, maximal at Cz; Ž2. a negative peak, between 300 and 700 ms, maximal over left inferior frontal scalp, Ž3. a negative slow wave, between 300 and 1000 ms, maximal over the frontal poles; Ž4. a positive peak at 600 ms that was bilaterally symmetrical and maximal over midline parietal scalp; Ž5. a large amplitude and long duration negative slow wave, maximal over cerebellar scalp Ži.e., Cb1, Cb2., that began at 400 ms, peaked around 1000 ms and slowly decreased to the end of the epoch; Ž6. a late positive wave, maximal over right frontal scalp, with an onset Ž600–800 ms. and offset Ž1400–2000 ms. that varied across conditions; and Ž7. a late negative slow wave between 1000 and 2000 ms that was maximal over left superior frontal scalp Ži.e., Fc5.. One difference between the ERPs elicited during semantic and episodic recall was in the duration of the negative wave that was maximal over medial frontal scalp Ži.e., Fp1, Fp2, F3, Fz, F4, Fc1, Fc2. between 300 and 1000 ms. In all recall conditions, this activity peaked at about 500 ms and was asymmetrical, being somewhat larger to the left of the midline. While this negativity

Fig. 2. Across-subject isopotential maps showing the distribution of positive Žunshaded. and negative Žshaded. voltages, based on the ERPs elicited at all 32 channels in the cued recall conditions ŽSemantic, CRS; Episodic-Easy, CRH; Episodic-Difficult, CRL., and for the uncompleted stem trials in the Episodic-Difficult condition ŽCRL-U.. Electrode positions are indicated by dots and the difference between contour lines is 1.0 mV. The maps are 1108 projections, with the electrodes on the circumference corresponding to E1, E2, M1, M2, Cb1, Cb2.

R. Johnson Jr. et al.r CognitiÕe Brain Research 7 (1998) 119–136 Table 2 Summary of topographic profile comparison results between semantic and episodic memory recall conditions Latency interval 600–690

700–790

800–890

900–990

Semantic Õs. Episodic-Easy a F 1.1 3.3 df 2,30 2,29 p 0.35 0.049

500–590

4.8 2,31 0.015

3.9 2,30 0.030

2.5 2,29 0.10

Semantic Õs. Episodic-Difficult a F -1 -1 3.4 df 2,31 p 0.49 0.40 0.046

3.2 3,31 0.050

1.5 2,31 0.24

a

Comparisons calculated using all 31 electrodes. All df ’s Greehouse–Geisser corrected and rounded down to the nearest whole number.

declined rapidly after peaking and disappeared by 700 ms during semantic recall, in both episodic recall conditions, it continued at peak amplitude for another 400 ms before declining and disappearing between 900 and 1200 ms.

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Note that, despite large differences in accuracy of episodic recall across conditions, the magnitude of this negativity was about the same in both episodic conditions. Isopotential maps based on these ERP waveforms were calculated in a series of temporal windows between 200 and 1200 ms ŽFig. 2.. These maps reinforce the idea that the ERPs elicited in all three recall conditions were much the same until 690 ms. After 700 ms, the frontal negativity was limited to more lateral and posterior areas during semantic recall compared to the more widespread distribution evident in the two episodic recall conditions. To evaluate the timing of the topographic differences between the ERPs elicited in the semantic and episodic recall conditions, ANOVAs were performed on the RMS scaled waveform areas calculated in each 100-ms interval between 100 and 1290 ms. As shown in Table 2, significant condition= electrode interactions between the semantic and two episodic conditions were confined to the 600–900 ms epoch, indicating that the pattern of neural generator activity was different for semantic and episodic cued recall only during this interval.

Fig. 3. Across-subject CSD maps based on the ERPs elicited at all 32 channels in the three cued recall conditions ŽSemantic, CRS; Episodic-Easy, CRH; Episodic-Difficult, CRL., and for the uncompleted stem trials in the Episodic-Difficult condition ŽCRL-U.. Unshaded and shaded regions indicate positive and negative current densities, respectively. Electrode positions are indicated by dots. The difference between contour lines corresponds to a density increment of 7 mVrcm2 . The maps are 1108 projections, with the electrodes on the circumference corresponding to E1, E2, M1, M2, Cb1, Cb2.

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A second difference between the waveforms in Fig. 1 is the presence of larger negativities over inferior posterior scalp during semantic recall. An ANOVA on the waveform areas at Cb1 and Cb2 between 700 and 1000 ms revealed that there was significantly more negative slow wave activity during semantic recall compared to the Episodic-Easy condition w F Ž1,11. s 4.7, p s 0.05x, but only borderline greater amplitudes compared to the Episodic-Difficult condition w F Ž1,11. s 4.1, p s 0.07x. A third difference across recall conditions was that the right frontal positivity appeared to peak shortly before the mean RT in each condition. To sharpen spatially the ERP topographies and identify which ERP activity was generated locally, CSD maps were calculated on the waveforms in Fig. 1. As shown in Fig. 3, at 200–300 ms, the early negative peak at Cz appears as a negative current density. In the 300–490-ms interval, this activity increased and a second negative current density appeared, centered over left inferior frontal scalp Ži.e., anterior to F7.. At about the same time, a positive current density, centered posterior to Pz, was increasing centrally and beginning to extend toward both temporal lobes, with more activity over the right than the left hemisphere. Subsequently, in the 500–690-ms interval, the anterior negative current density, while focused over left inferior scalp, increased to include a broad area that included right frontal scalp. In this interval, the posterior positive current

density encompassed both temporal lobes, remaining somewhat larger over the right hemisphere. In the 700– 890-ms interval, the negative current density remained focused over left inferior frontal scalp during semantic recall, while it decreased in activity over medial frontal scalp. The significantly Žsee above. prolonged negativity in the two episodic conditions relative to the semantic condition was apparent in the fact that the negative current density showed a widespread distribution that encompassed the medial portion of the right frontal lobe Ži.e., between 500 and 890 ms.. The activity over temporal lobes also changed at this time as a second focus of positive current density appeared over the inferior right hemisphere. The negative current density over right frontal scalp continued through the 900–1190-ms interval in both episodic conditions, although more so for the EpisodicDifficult condition. Concurrently, the posterior positive current density diminished considerably at the midline. In contrast, the magnitude of the focus over the temporal lobes, and the right temporal lobe in particular, appeared to be directly proportional to the duration of the recall task. That is, temporal lobe activity was least for semantic recall and greatest in the Episodic-Difficult condition. To assess this difference further, the amplitudes at these lateral fronto-temporal sites Ži.e., F8, Fc6, T8. in the 1200–1600ms interval were quantified for the Episodic-Easy and -Difficult conditions. This interval begins immediately af-

Fig. 4. Across-subject isopotential Žtop row. and CSD maps Žbottom row. for the post-response interval based on the ERPs elicited at all 32 channels in the three cued recall conditions ŽSemantic, CRS; Episodic-Easy, CRH; Episodic-Difficult, CRL.. Unshaded and unshaded regions indicate positive and negative current densities, respectively. The difference between contour lines corresponds to a density increment of 4 mVrcm2 . In all other respects, these maps are the same as those in Fig. 3.


ter the mean retrieval time in the Easy condition and ends after mean retrieval time in the Difficult condition. Since the ANOVA on these areas only approached significance w F Ž1,11. s 3.6, p s 0.08x, the data only suggest that this positivity is related to retrieval duration. 3.2.2. Post-response interÕal actiÕity After successfully recalling a word, subjects were instructed to keep the retrieved word in memory until they could report it when the word stem reappeared approximately 4.5 s after its initial presentation. During the postretrieval interval, there was a small negative slow wave present over left frontal scalp Ži.e., F7, F3, Fc5, T7. that continued to the end of the recording epoch. At the same time, there was a positive slow wave present over the frontal poles Ži.e., Fp1, Fp2.. To determine more about this post-response activity, CSD maps were calculated for a 500-ms interval Ž250 ms for the Episodic-Difficult condition. beginning at the mean RT plus one S.D. ŽFig. 4.. Compared with the CSD maps of the pre-response recall-

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related activity ŽFig. 3., the focus of this negative current density shifted medially Žtoward F3. and somewhat more posteriorly Žtoward Fc5., indicating that different areas of left frontal cortex were active before and after retrieval. To determine if the pattern of brain activity changed between the pre- and post-response time windows, topographic profile comparisons were done on the data from left central–frontal sites Ži.e., F7, Fc5, T7, C3.. After scaling the waveform areas between 300–600 ms and 1500–2000 ms, the topographic difference observed in the semantic recall condition only approached significance w F Ž1,18. s 3.9, p s 0.06x. However, in the Episodic-Easy condition, there was a significant topographic difference between the early and late intervals Ži.e., 1800–2200 ms was used due to the longer mean RT. w F Ž1,20. s 5.4, p s 0.03x, indicating that there was a significant change in the pattern of brain activation between the pre- and post-retrieval intervals. Note also that the CSD maps indicate that a second focus of negative current density appeared in an homologous area of the right frontal scalp.

Fig. 5. Across-subject ERP averages at 23 electrode sites elicited on the trials when the subjects failed to complete the word stems in the Episodic-Easy Ždashed lines. and Episodic-Difficult Ždotted lines. conditions. The waveforms for the completed stems in the Episodic-Difficult condition Žsolid lines. are included for comparison.


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Table 3 Summary of topographic profile comparison results for completed and non-completed episodic recall trials Latency interval Žms. 400–490 Episodic-Difficult F 2.4 df 2,26 p 0.11 Episodic-Easy a F -1 df p 0.42

500–590

600–690

700–790

800–890

900–990

1000–1090

1100–1190

1200–1290

3.9 2,29 0.032

6.8 2,28 0.004

7.1 2,31 0.003

5.4 3,33 0.004

5.9 3,33 0.002

4.6 3,34 0.009

4.0 3,36 0.014

2.8 3,38 0.050

2.8 2,28 0.07

3.4 2,27 0.046

4.9 2,28 0.015

5.8 2,31 0.007

4.6 2,30 0.018

4.0 3,33 0.016

3.5 3,34 0.026

4.0 3,35 0.015

a

a Comparisons calculated using all 31 electrodes. All df ’s Greehouse–Geisser corrected and rounded down to the nearest whole number.

3.2.3. Uncompleted stem trials To determine if there were differences in brain activity as a function of whether subjects were successful at completing the word stems, averages were calculated for trials when subjects did not respond, indicating that they could not recall the appropriate word. Due to the high completion rates in the semantic condition Ži.e., 95%., averages could be calculated only for the two episodic conditions. The resulting waveforms are superimposed in Fig. 5, along with those elicited by the completed stems in the Episodic-Difficult condition. As was the case for the ERP activity associated with successful recall, there were few differences between the ERPs elicited by the uncompleted stem trials from the two episodic recall conditions, despite the fact that there were twice as many uncompleted stems in the Episodic-Difficult condition. 1 Moreover, during the first 400 ms, ERP activity for uncompleted stem trials in both conditions was largely the same as that for the completed stem trials. After 400 ms, the uncompleted trials elicited more negative ERPs at midline frontal, central, parietal and inferior posterior scalp. In addition, uncompleted stems elicited significantly less LPC activity between 500 and 900 ms over parietal scalp Ži.e., P3, Pz, P4. than completed stems in both the Episodic-Easy w F Ž1,11. s 22.8, p - 0.0006x and Episodic-Difficult w F Ž1,11. s 18.6, p - 0.002x conditions. Note that, despite these clear differences, the ERPs for completed and uncompleted words stems were remarkably similar to one another over the frontal poles and bilaterally over inferior frontal scalp Ži.e., F7, Fp1, Fp2, F8.. The absence of differences at the Fp1 and Fp2 sites as a function of whether the stems were completed, despite differences at the three immediately posterior sites Ži.e., F3, Fz, F4., raises the possibility that, in all recall conditions, the ERPs elicited at these central–

1 Note that some differences between these two averages may be due to the fact that there was a mean of only 18 trials in the averages for the Easy condition compared to a mean of 35 trials in the averages for the Difficult condition.

frontal sites may reflect activity in brain areas different from those generating the ERPs at the frontal poles. As was the case for completed word stems, there were relatively few aspects of the ERPs elicited by uncompleted stems that could be ascribed to differences in task difficulty. Although subjects were presumably trying to retrieve the appropriate word for most or all of this initial 2 s of the recall epoch, the few differences that appeared over central and parietal scalp did not seem to be related to task difficulty. That is, there was slightly more, rather than less, amplitude in the Episodic-Easy condition, as occurred for the completed stem trials ŽFig. 5.. The isopotential maps for the ERPs elicited by the uncompleted word stems in the Episodic-Difficult condition are shown in Fig. 2 Žbottom row.. These maps indicate that, beginning around 700 ms, the distribution of frontal negative potentials shifted medially and posteriorly, a trend that continued into the 900–1190-ms interval. To determine the presence and temporal extent of scalp topographic differences between the ERPs elicited by the completed and uncompleted word stems, comparisons were made in successive 100-ms intervals, separately for each episodic recall condition. The results of these profile comparisons, calculated on the basis of the areas obtained from all 31 electrode sites, are shown in Table 3. These analyses indicate that significantly different patterns of generator activity were apparent beginning at 500 ms post-stimulus in the Episodic-Easy condition and at 600 ms in the Episodic-Difficult condition. These results strongly suggest that different patterns of neural activity were apparent relatively soon after stimulus onset as a function of whether subjects would ultimately be able to recall the correct word from episodic memory. To determine more precisely the nature of the distributional differences in ERP activity between the completed and uncompleted stem trials, difference waveforms were calculated by subtracting the ERPs elicited by uncompleted stems from those elicited by completed word stems. CSD maps based on these difference waveforms reveal that a complex pattern of additional brain activity was


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Fig. 6. Across-subject isopotential Žtop row. and CSD maps Žbottom row. for the difference waveforms Žfrom all 32 channels. calculated by subtracting the averages for the uncompleted stem trials from those for the correctly completed stem trials in the Episodic-Difficult condition. Unshaded and shaded regions indicate positive and negative current densities, respectively. The difference between contour lines corresponds to an increment of 0.5 mV in the isopotential maps and 3.5 mVrcm2 in the CSD maps. In all other respects, these maps are the same as those in previous figures.

Fig. 7. Across-subject ERP averages at 23 electrode sites elicited by old, Lab list, words during recognition test 1 Žsolid lines.. The oldrnew difference waveforms, obtained by subtracting the waveforms elicited by new words in test 1 from those elicited by old words are also shown Ždotted lines.. These waveforms are superimposed on those elicited when subjects recalled the same Lab list words ŽEpisodic-Difficult; dashed lines..

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Fig. 8. Across-subject isopotential maps Žbased on the waveforms from all 32 channels. showing the distribution of positive Žunshaded. and negative Žshaded. voltages elicited when Lab list Žold. words were correctly recognized Žold; top row.. Maps based on the oldrnew difference ERPs are presented in the bottom row ŽOrN.. The difference between contour lines is 1.0 mV Ž0.5 mV for the oldrnew difference.. In all other respects, these maps are the same as previous figures.

elicited on trials when subjects were unable to retrieve the appropriate word from the Lab list ŽFig. 6, bottom row.. These maps indicate that, beginning around 500 ms, two foci of negative current density appeared over left Ži.e., F3. and right Ži.e., F4. medial frontal scalp, with two others posteriorly over left medial parietal Ži.e., P3. and right lateral parietal Ži.e., P8. scalp. This activity increased subsequently Ži.e., 700–890 ms. and continued at about the same amplitude until it disappeared between 1200 and 1400 ms. 3.2.4. Recognition-related ERP actiÕity In Fig. 7, the ERPs elicited by old, Lab list, words during recognition are shown along with oldrnew difference waveforms, in comparison with the ERPs elicited when the same words were successfully recalled Ži.e., Episodic-Difficult condition.. 2 These waveforms, and the isopotential maps based on them ŽFig. 8., reveal that, after 300 ms, large differences in neural activity occurred as a function retrieval mode. That is, unlike the recall-related ERP activity, ERPs elicited during recognition were dominated by a large LPC in the 400–800-ms interval that, although maximal over posterior scalp, was present to some degree over much of the scalp with the exception of

2 The recognition data here are analyzed in full in Johnson et al. w20x and are represented here only to permit comparisons between the two retrieval modes. These comparisons are based on the recognition data from the first recognition test on the Lab list words since most studies generally use only a single study-test combination. In addition, this comparison eliminates the introduction of temporally and spatially overlapping ERP activity on both the LPC and oldrnew effect resulting from the effects of test repetition Žsee Ref. w20x..

far frontal Ži.e., Fp1, Fp2., lateral frontal Ži.e., F7, F8. and cerebellar sites Ži.e, Cb1, Cb2.. In contrast, during recall, a much smaller LPC, with a much more restricted topography, was present primarily at three parietal sites Ži.e., P3, Pz, P4.. However, during recognition, the phasic negativity, present over central scalp Ži.e., Cz, C3. between 250 and 450 ms, appeared to be smaller and briefer than that elicited at the same location during recall, although the onset of this activity appeared to be the same for both retrieval modes. ANOVAs on areas at sites where this negativity was greatest Ži.e., Cz, C3. revealed that significantly greater amounts of negativity were elicited during recall in the 400–600-ms interval w F Ž1,11. s 6.6, p 0.05x. Another difference between the ERP activity elicited by the Lab list words during the two types of retrieval was apparent over inferior posterior scalp. The negative slow wave, beginning around 400 ms and maximal over inferior posterior scalp Ži.e., Cb1, Cb2., was significantly larger during recall compared to recognition in the 400–1000-ms interval w F Ž1,11. s 8.1, p - .02x. Finally, during recognition, the Lab words elicited a late positive wave, maximal over right frontal–central scalp Ži.e., Cz, C4, Fz, F4., that began between 800 and 1200 ms and continued to the end of the 2-s recording epoch. Note that, although there are some similarities in the recall and recognition potential maps for the 900–1190-ms interval, this epoch begins 200 ms after the recognition RT but almost 600 ms prior to the recall RTs. Therefore, it would seem unlikely that this activity represents the same process in both retrieval modes. One similarity in ERP activity across retrieval modes occurred in the negative slow wave activity elicited over the frontal poles Ži.e., Fp1, Fp2.. Activity there was similar


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Fig. 9. Across-subject CSD maps Žbased on the waveforms from all 32 channels. showing the distribution of positive Žunshaded. and negative Žshaded. current densities elicited when Lab list Žold. words were correctly recognized Žold; top row.. CSD maps based on the oldrnew difference ERPs are shown in the bottom row ŽOrN.. The difference between contour lines is 7 mVrcm2 Ž3.5 mVrcm2 for the oldrnew difference.. In all other respects, these maps are the same as previous figures.

in amplitude and timing in both conditions, although this negativity began somewhat later Ži.e., approximately 350 ms vs. 500 ms. and lasted somewhat longer during recognition compared to during recall. An ANOVA comparing the waveform areas at these two sites between 400 and 1000 ms during recall and recognition conditions confirmed the visual impression that there was little difference as a function of retrieval mode w F - 1x. Note that potential maps indicate that the focus of this negativity was somewhat more anterior and medial during recognition compared to recall. CSD maps based on the ERPs elicited by Lab words during recognition ŽFig. 9. reveal that, between 200 and 490 ms, there was a positive current density at Pz and negative current density at Cz that were both similar to those elicited during cued recall of these same words ŽFig. 3.. While ERP activity over posterior scalp remained much the same in the 500–690-ms interval for both retrieval modes, the focus over far-frontal scalp was slightly more medial during recognition and activity diminished rapidly after 700 ms, by which time subjects had, on average, made their oldrnew recognition decision. In accord with past studies, oldrnew difference waveforms were derived by subtracting the ERPs elicited by new words from those elicited by old words ŽFig. 7.. The isopotential and CSD maps based on these waveforms are presented in Figs. 8 and 9, respectively. The oldrnew difference ERPs and isopotential maps were characterized primarily by a widespread positive peak that was maximal between 500 and 600 ms over left parieto-occipital scalp. After the posterior positivity disappeared, another focus of positive potential appeared over medial right frontal scalp in the 900–1190-ms interval. Note that there was little

evidence in the difference waveforms of either the early negative slow wave over the frontal poles ŽFp1, Fp2. or the late positive slow wave Ži.e., after 1200 ms. activity over right frontal–central scalp, indicating that the amplitudes of these potentials were about the same for old and new words during recognition. The CSD maps reveal further that, in the 300–490-ms interval, there were positive current densities over left frontal scalp Ži.e., F3. and bilaterally over parietal–occipital scalp. This posterior activity then consolidated into a left hemisphere positive current density as another positive current density appeared over right frontal–central scalp Ži.e., centered at Fc2.. By 900 ms, the posterior activity faded leaving only the right frontal–central current density.

4. Discussion The data revealed both within- and between-task behavioral differences in retrieval accuracy and speed during recall of semantic and episodic information in a word-stem cued recall paradigm. Overall, as measured by both percent completed stems and RT, semantic recall was significantly more accurate and faster than episodic recall. Further, episodic recall difficulty was successfully manipulated with the two word lists since subjects were able to recall significantly more Home list words in significantly less time compared to recall of Lab list words. Finally, episodic recall of Lab list words was only marginally less accurate, albeit twice as slow, as when subject had to recognize the same words. Given that we used blocked conditions, the question arises as to whether the results might be affected by state

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effects. While this possibility cannot be ruled out, it appears unlikely since the waveforms obtained here under blocked conditions have substantially the same componential structure as those obtained by Allan et al. w1x ŽFig. 1. in a condition requiring random recall of semantic and episodic information. For example, both past and present results show a frontal negative peak at 200 ms followed by a positive component beginning around 300 ms, along with the predominantly negative activity over lateral posterior scalp. For reasons that are not clear, our data and those of Allan et al. w1x, although similar to each other, do not resemble as closely the cued recall ERP data reported by Allan and Rugg w2x. 4.1. Semantic Õs. episodic cued recall Recall of semantic and episodic information elicited different but overlapping patterns of ERP activity. All three recall conditions were characterized primarily by: Ž1. an early onset negative wave, maximal over central scalp, lasting from 200 to 690 ms; Ž2. a negative wave, maximal over left inferior frontal scalp Ži.e., F7., lasting from 300 ms until 300–400 ms after the RT response; Ž3. a positive wave, present bilaterally but earlier and larger over right temporal scalp, lasting from about 300 ms until 300–400 ms after the RT response; Ž4. a long-lasting negativity, maximal over inferior posterior scalp, between 400 ms and the end of the recording epoch; Ž5. a small positivity, maximal over parietal scalp, between 400 and 1000 ms; and Ž6. a slow positivity, maximal over right lateral frontal scalp, which peaked 100–200 ms prior to the mean RT in each condition. There were two primary differences in the ERP activity elicited during semantic and episodic recall. The first involved the negative wave that was maximal over anterior frontal scalp Ži.e., Fp1, Fp2.. While the onset Ž300 ms. and initial peak latency Ž500 ms. of this activity was the same across conditions, its duration varied as a function of the type of information being retrieved. That is, while this negativity rapidly diminished after peaking during semantic recall, it continued at peak levels for an another 300 ms in both episodic recall conditions. Thus, while there were no significant topographic differences over frontal scalp between 300 and 600 ms as a function of which type of information was accessed, there were significant differences between semantic and episodic recall at the same sites in the 600–900-ms interval. The second difference was that significantly more negativity was elicited over cerebellar–occipital scalp between 700 and 1000 ms during semantic retrieval than in the episodic conditions, although the onset and peak timing of this activity was the same in all three recall series. Similar results were found by Allan et al. w1x over occipital scalp. This activity does not appear to reflect differences in task difficulty, however, since it was largest in the semantic condition, the easiest task and essentially the same in both episodic recall

conditions, despite substantial differences in retrieval difficulty. Each of these patterns of ERP activity is discussed in more detail below. A key finding of both previous ERP studies of cued recall was the presence of a positive slow wave late in the recording epoch, maximal over anterior scalp, that was larger for stems completed episodically w1,2x. A similar result is evident in our data ŽFig. 1. since we also found increased positivities, maximal over right frontal scalp, when stems were completed using episodic memory Ži.e., the difficult condition, which is most comparable to the conditions in 1, 2. compared to when there were completed on the basis of semantic memory. Thus, it appears that the ERP activity elicited during cued stem recall tasks is largely, if not entirely, independent of whether episodic or semantic memories are retrieved under blocked or random conditions. 4.2. Early central negatiÕity (250–600 ms) A phasic negative potential with an early onset was elicited over central scalp and its presence in the CSD maps indicates that its’ neural generator is located relatively close to the Cz electrode site. Across the three recall conditions, the amplitude and onset and offset latencies Ž250–600 ms. of this potential were approximately the same, suggesting that activity here was not influenced by differences in either task difficulty or type of retrieval. Consistent with this, a negative potential with a similar scalp distribution, onset latency and amplitude was elicited during recognition, although its duration was about 100 ms less. Thus, across the three recall conditions and recognition, the main difference in this negativity was that its duration was shorter during recognition compared to recall. Given the scalp distribution of this potential, it is possible that it represents activity in the anterior cingulate cortex, an area that PET studies have found to be active during semantic and episodic recall and episodic recognition. For example, the present results are consistent with those of Cabeza et al. w9x who found that recall was associated with greater activity in the anterior cingulate cortex than was recognition. 4.3. Left inferior frontal negatiÕity (300-mean RT) The ERPs revealed that a negative component appeared around 300 ms over left inferior frontal scalp Ži.e., F7. during all three cued recall conditions. While not discussed or quantified, a similar negativity is present in the waveforms reported by Allan et al. w1x. The presence of a negative current density in the CSD maps, focussed over left inferior frontal scalp, indicates that this activity was generated in the underlying tissue from about 300 ms after onset of the word stem until the shortly after subjects signalled their retrieval with the button press. This ERP activity may correspond to the increased blood flow ob-


served in a roughly analogous area Ži.e., Brodmann’s Area 45, 46. in PET studies of semantic memory cued recall w7,8,10,13,30,44x, an area thought to be part of a ‘semantic executive system’ that is essential for retrieving semantic information w12x. The present ERP data indicate that the same region is active during both semantic and episodic cued recall, suggesting that subjects may perform the episodic recall task, at least in part, by using semantic memory to generate possible completions for the stem. While such processing is all that is required in the semantic task, additional processes would be necessary during episodic recall to select the correct response from generated items. These processes may be indexed by the ERP activity generated in right lateral frontal areas, since its duration appears to be most closely related to retrieval time. Contrasting with the present results, PET studies of episodic recall found increased blood flow more frequently in right dorsolateral frontal cortex w5,6,9x than in bilateral frontal cortex w38x. One reason why the ERP technique indicates greater involvement of left frontal areas than the PET technique could be the use and choice of baseline tasks in PET experiments. That is, if stem completion w5,6,38x, or another task drawing on semantic memory processes w9,13,30x, is used as the reference task, subtraction of this ‘baseline’ activity from the episodic recall task activity would remove the semantic memory contribution to episodic recall from the scans. Nevertheless, like the PET results, the ERP data show that the right frontal areas play a larger role in episodic retrieval than in semantic retrieval. 4.4. Far-frontal negatiÕe slow waÕe (300–1000 ms) Between 300–400 and 1000 ms, there was a negative slow wave present bilaterally over the frontal poles Ži.e., Fp1, Fp2.. While this activity appeared to be slightly larger over the left hemisphere, this may have resulted from overlap with the right frontal positivity that followed. The timing and extent of this negativity appeared to be about the same during both episodic recall conditions, despite significant differences in retrieval speed and success, strongly suggesting that neither the amplitude nor duration of this negativity was influenced by retrieval effort or success. This conclusion is supported further by the fact that the timing and magnitude of this activity was the same even when subjects were unable to retrieve the appropriate word from episodic memory. Thus, although the duration of this negativity was significantly less during semantic recall, the episodic recall data, taken as a whole, argue against its briefness during semantic recall was due to the relative ease of that task. Rather, the data are more consistent with the idea that the later part of this negativity is specific to episodic retrieval. Additional support for the idea that the longer duration of this component is a specific reflection of an episodic memory process is the finding that the onset latency,

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amplitude and duration of this negativity was not significantly different across retrieval modes Ži.e., recognition vs. recall.. Also, during recognition, the magnitude of this far-frontal negativity was about equal following both old and new words, a result consistent with an episodic memory process since subjects would have to initiate a memory search for both old and new words during recognition. This negativity did, however, appear to be somewhat more spatially widespread, extending more posteriorly, during recall compared to recognition. Another aspect of this component which is inconsistent with its being related to retrieval success is the finding that this negativity always lasted until about 1000 ms, whether mean retrieval time was 701 ms for old words during recognition or 1452 ms in the Episodic-Difficult condition. Taken together, the evidence supports an interpretation in which this far-frontal negativity reflects a process common to all attempts to access episodic memory, possibly reflecting processes associated with the initiation of strategic search. This would be consistent with suggestions that the frontal lobes are part of a system that modulates intentional, effortful and strategic search of memory w15,16,24x. 4.5. Inferior posterior negatiÕe slow waÕe (400–2000 ms) Another difference between semantic and episodic recall and between episodic recall and recognition was that, in both these comparisons, there was relatively more negative slow wave activity over cerebellar scalp between 400 ms and the end of the 2-s recording epoch. Note that, while largest over cerebellar scalp, these potentials extended to occipital ŽO1, O2. and posterior lateral parietal ŽP7, P8. scalp. In spite of its proximity to the occipital lobe, the late onset and prolonged duration of this negative slow wave makes it highly unlikely that it reflects a sensory process. Similar late negativities are apparent over occipital scalp in previous reports of recall-related ERP activity Žw1,2x, and see w4,29x for related PET results.. 4.6. Posterior positiÕity (400–1000 ms) During recall, there was a positive potential, not unlike the LPC, that was maximal over midline parietal scalp between 400 and 1000 ms. However, the lack of any amplitude variation across the three recall conditions is contrary to the rather large body of evidence showing that LPC Ži.e., P300. amplitude is inversely related to task difficulty under a wide variety of task conditions w18x, including recognition memory tasks w20,21x. In those paradigms, however, the LPC occurred roughly coincident with the mean RT, a situation that did not obtain here since, across recall conditions, the LPC peaked 200–900 ms before the subjects’ mean RT signalling successful recall. It is notable that peak latency of this activity during recall was the same as that of the parietal maximal LPC

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elicited during recognition, when LPC latency was about 100 ms less than mean RT.

The CSD maps revealed the presence of locally-generated ERP activity in temporal regions when subjects retrieved both semantic and episodic information. This activity appeared first over right hemisphere when a positive current density appeared around 340 ms. Moreover, the CSD maps suggest that this activity extended to the anterior temporal or right inferior frontal scalp, although it will require more electrodes to determine more about the spatial characteristics of this activity. Activity in the left hemisphere appeared to lag activity in the right hemisphere by about 100 ms, and it did not appear to reach the same magnitude or extend as far anterior as it did on the right. In all conditions, this temporal activity ended shortly after retrieval was completed, as indicated by the RT.

memory while subjects waited for the reappearance of the stimulus prompting their verbal response. That is, the task shifted from retrieval to maintenance once the subject successfully retrieved the appropriate word. Negative slow waves with a similar left frontal maximum have been reported in a series of studies by Ruchkin et al. w32–35x when subjects must retain verbal, but not visuo-spatial, material in working memory. Moreover, a bilateral pattern of asymmetric negative current densities, similar to that found here, was reported by Ruchkin et al. w35x ŽFig. 5. in a working memory task involving rehearsal of verbal material. The asymmetrical nature of this bilateral ERP activity also accords well with the results of PET studies of verbal working memory showing increased blood flow bilaterally in inferior ŽBA 44. and posterior ŽBA 6. frontal cortex w27,31x. Together, the present data and those of Ruchkin et al. indicate that the same general brain areas are active regardless of whether the information being maintained comes from external or internal sources.

4.8. Inferior right frontal positiÕity (600-2000 ms)

4.10. Episodic recall Õs. recognition

Despite large behavioral differences in the speed and number of stem completions, the ERP activity elicited in the two episodic recall conditions was very similar, with the amplitude, onset and peak latencies of most components being the same in both conditions. The most apparent difference was that the late right dorsolateral frontal positivity was larger and later in the Episodic-Difficult condition. The finding that the ERPs in the Episodic-Difficult condition remained positive while those in the Episodic-Easy condition returned to baseline, coupled with the fact that this positivity peaked 100–200 ms before the mean RT in both conditions, suggests a possible link between this inferior right frontal activity and episodic retrieval. Additional evidence that right frontal activity is related merely to the attempt to retrieve episodic memories, rather than to successful retrieval is provided by the data showing that this positivity was present to an equal extent in the waveforms elicited by the uncompleted word stems Žsee also w22,25x..

By comparing recognition data obtained early in the learning process with recall data obtained at the end of the process, only a marginal difference in accuracy remained between percent of the Lab list words correctly recognized Žcorrected for guessing. and recalled, although substantial differences in retrieval time remained. Therefore, it is reasonable to suggest that the differences in ERP activity elicited in these two conditions are more likely to be due to differences in processing related to retrieval mode than to processing related to differences in retrieval difficulty. Overall, there were a number of similarities between the ERP activity elicited during recognition and recall, including the similar negativities found at the frontal poles and the early negativity at central sites Ži.e., C3, Cz., although this latter activity was significantly briefer during recognition. Unlike recall, recognition was characterized by a widespread LPC component and no negativity over left inferior frontal scalp. Moreover, consistent with the uncompleted stem trial data, during recognition, the frontal Ži.e., F3, Fz, F4. and far-frontal Ži.e., Fp1, Fp2. sites showed distinct patterns of activity, adding to the argument that the ERP activity recorded at far-frontal and more posterior frontal areas reflect, at least to some extent, the activity in different frontal areas. Perhaps the most surprising difference between the two retrieval modes was the complete absence of any ERP activity during recall corresponding to any of the three subcomponents of the old–new difference w20,41,45,46x. That is, if the old–new effect represented a process invoked whenever episodic memory is accessed successfully, it should be elicited during both recognition and recall. This result did not obtain in the present study and, although direct comparisons across studies are difficult, Allen et al. w1x and Allen and Rugg w2x also failed to find

4.7. Temporal positiÕities (300-post RT)

4.9. Post-response left dorsolateral frontal negatiÕity After subjects signalled the completion of retrieval, the left inferior frontal negativity was replaced by another negative slow wave. The locus of this post-response negativity was more medial and posterior than the pre-response negativity, a shift in scalp distribution that was significant in the Episodic-Easy condition and borderline significant in the Semantic condition. The CSD maps revealed bilateral foci that were spatially symmetrical, but with greater activity over left dorsolateral cortex, a strong indication that this activity was locally generated. Given its location and timing, it is reasonable to suggest that this negativity reflects the maintenance of the retrieved word in working


evidence of the old–new effect in their cued recall paradigm. Together, the data from these two studies suggest that the old–new effect reflects an episodic memory process that is specifically related to recognition, and not to other types of episodic retrieval. 4.11. Successful Õs. unsuccessful episodic retrieÕal In addition to providing information on brain activity during retrieval failure, the ERPs elicited by uncompleted word stems provide information relevant to distinguishing between those brain processes invoked as part of a general retrieval attempt from those related to successful retrieval. Moreover, they address the issue of which ERP effects are related to task difficulty, independent of the retrieval process. The uncompleted stem data suggest that the ERP activity recorded at left inferior frontal and far-frontal sites reflects retrieval processes that are independent of retrieval success since activity in these areas was the same for both completed and uncompleted trials and they were unaffected by task difficulty, either across or within tasks. Instead, the main ERP differences between completed and uncompleted stem trials were found over a widespread area centered along the midline of the scalp. CSD maps calculated on difference waveforms designed to isolate brain activity elicited during retrieval failure produced the unexpected result that the pattern of additional generator activity somewhat resembled that associated with the old– new difference found during recognition. While they do not overlap perfectly, the current densities apparent in the old–new effect in the 500–690-ms interval Ži.e, F3, F4-Fc2, P3-O1, Cp6. were similar to those foci active in the uncompleted stem trials in the 500–1190-ms interval. Note that, since there were few if any latency differences between the ERPs associated with successful and unsuccessful retrieval, these differences are not likely to be artifactually created by the subtraction. However, the idea that the generators responsible for the old–new effect in recognition would be active when retrieval is unsuccessful is inconsistent with the fact that the old–new effect is found only in cases where subjects had correct knowledge that the item was previously encountered. Thus, although all stems referred to words that were old, and the subjects were fully cognizant of that fact, it is not clear why such activity should be elicited given that there apparently was no conscious retrieval.

5. Conclusion The present study revealed that the patterns of ERP activity elicited when subjects accessed long-term memory depended both on the type of information being recalled, semantic or episodic, and on retrieval mode, recall or recognition. Temporal and topographic analyses of the ERP indicated that a temporally and spatially distributed

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neural network is activated during semantic and episodic recall, with both characterized by activity in left inferior frontal cortex, central scalp, temporal lobes and inferior posterior Ži.e, cerebellar. scalp. Episodic recall was distinguished from semantic recall, as has been found in PET studies, by greater activity over the frontal poles and right frontal areas. In addition, episodic recall and recognition showed similar activity over the frontal poles and central scalp, but the left frontal activity elicited during recall was entirely absent during recognition. Also, a characteristic aspect of the ERP activity elicited during episodic recognition, the oldrnew effect, was absent during episodic recall. These differences in brain activity both within and across tasks appear to be related more to differences in retrieval processes than to differences in task difficulty since manipulation of recall difficulty and analysis of trials when recall failed indicated that most of the ERP activity elicited here was unaffected by task difficulty.

Acknowledgements This research was supported by the Research Foundation of the City University of New York ŽPSCrCUNY Awards 664499 and 666243.. We would also like to acknowledge the assistance of Olga Fridman for her generous help with electrode placement, and Toni Bellusci, Hannah Hoch, Eliesa Feit, and Chloe Shest who also helped during stimulus preparation and data collection. We also wish to thank David Friedman for the software used to calculate the isopotential and CSD maps.

References w1x K. Allan, M.C. Doyle, M.D. Rugg, An event-related potential study of word-stem cued recall, Cogn. Brain Res. 4 Ž1996. 251–262. w2x K. Allan, M.D. Rugg, An event-related potential study of explicit memory on tests of cued recall and recognition, Neuropsychologia 35 Ž1997. 387–397. w3x American Electroencephalographic Society guidelines for standard electrode position nomenclature, J. Clin. Neurophysiol. 8 Ž1991. 200–202. w4x I.M. Appollonio, J. Grafman, V. Schwartz, S. Massaquoi, M. Hallett, Memory in patients with cerebellar degeneration, Neurology 43 Ž1993. 1536–1544. w5x L. Backman, O. Almkvist, J. Andersson, A. Nordberg, B. Winblad, R. Reineck, B. Langstrom, Brain activation in young and older adults during implicit and explicit retrieval, J. Cogn. Neurosci. 9 Ž1997. 378–391. w6x R.L. Buckner, S.E. Petersen, J.G. Ojemann, F.M. Miezin, L.R. Squire, M.E. Raichle, Functional anatomical studies of explicit and implicit memory retrieval tasks, J. Neurosci. 15 Ž1995. 12–29. w7x R.L. Buckner, M.E. Raichle, S.E. Petersen, Dissociation of human prefrontal cortical areas across different speech production tasks and gender groups, J. Neurophysiol. 74 Ž1995. 2163–2173. w8x R.L. Buchner, E. Tulving, Neuroimaging studies of memory: theory and recent PET results, in: F. Boller, J. Grafman ŽEds.., Handbook

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w27x

w28x

R. Johnson Jr. et al.r CognitiÕe Brain Research 7 (1998) 119–136 of Neuropsychology, Vol. 10, Elsevier, Amsterdam, 1995, pp. 439– 466. R. Cabeza, S. Kapur, F.I.M. Craik, A.R. McIntosh, S. Houle, E. Tulving, Functional neuroanatomy of recall and recognition: a PET study of episodic memory, J. Cogn. Neurosci. 9 Ž1997. 254–265. R. Cabeza, L. Nyberg, Imaging cognition: an empirical review of PET studies with normal subjects, J. Cogn. Neurosci. 9 Ž1997. 1–26. N.J. Cohen, L.R. Squire, Preserved learning and retention of pattern analyzing skill in amnesia: dissociation of knowing how and knowing that, Science 210 Ž1980. 207–209. J.B. Demb, J.E. Desmond, A.D. Wagner, C.J. Vaidya, G.H. Glover, J.D.E. Gabrielli, Semantic encoding and retrieval in the left inferior prefrontal cortex: a functional MRI study of task difficulty and process specificity, J. Neurosci. 15 Ž1995. 5870–5879. P.C. Fletcher, C.D. Frith, P.M. Grasby, T. Shallice, R.S.J. Frackowiak, R.J. Dolan, Brain systems for encoding and retrieval of auditory-verbal memory: an in vivo study in humans, Brain 118 Ž1995. 401–416. D. Friedman, ERPs during continuous recognition memory for words, Biol. Psychol. 30 Ž1990. 61–87. J.S. Janowsky, A.P. Shimamura, L.R. Squire, Source memory impairment in patients with frontal lobe lesions, Neuropsychologia 27 Ž1989. 1043–1056. W. Jetter, U. Poser, R.B. Freeman Jr., H.J. Markowitsch, A verbal long term memory deficit in frontal lobe damaged patients, Cortex 22 Ž1986. 229–242. R. Johnson Jr., Auditory and visual P300s in temporal lobectomy patients: evidence for modality-dependent generators, Psychophysiology 26 Ž1989. 633–650. R. Johnson Jr., On the neural generators of the P300 component of the event-related potential, Psychophysiology 30 Ž1993. 90–97. R. Johnson Jr., Event-related potential insights into the neurobiology of memory systems, in: F. Boller, J. Grafman ŽEds.., Handbook of Neuropsychology, Vol. 10. Elsevier, Amsterdam, 1995, pp. 135–163. R. Johnson Jr., K. Kreiter, B. Russo, J. Zhu, A spatio-temporal analysis of recognition-related event-related brain potentials. Int. J. Psychophysiol., in press. R. Johnson Jr., A. Pfefferbaum, B.S. Kopell, P300 and long-term memory: latency predicts recognition time, Psychophysiology 22 Ž1985. 497–507. S. Kapur, F.I.M. Craik, C. Jones, G.M. Brown, S. Houle, E. Tulving, Functional role of the prefrontal cortex in memory retrieval: a PET study in humans, NeuroReport 6 Ž1995. 1880–1884. G. McCarthy, C.C. Wood, Scalp distributions of event-related potentials: an ambiguity associated with analysis of variance models, Electroencephalogr. Clin. Neurophysiol. 62 Ž1985. 203–208. M. Moscovitch, Memory and working-with-memory: a component process model based on modules and central systems, J. Cogn. Neurosci. 4 Ž1992. 257–267. L. Nyberg, E. Tulving, R. Habib, L.-G. Nilsson, S. Kapur, S. Houle, R. Cabeza, A.R. McIntosh, Functional brain maps of retrieval mode and recovery of episodic information, NeuroReport 7 Ž1995. 249– 252. K.A. Paller, M. Kutas, Brain potentials during memory retrieval provide neurophysiological support for the distinction between conscious recollection and priming, J. Cogn. Neurosci. 4 Ž1992. 375– 391. E. Paulesu, C.D. Frith, R.S.J. Frackowiak, The neural correlates of the verbal component of working memory, Nature 362 Ž1993. 342–345. F. Perrin, J. Pernier, O. Bertrand, J.F. Echallier, Spherical splines for

w29x

w30x

w31x

w32x

w33x

w34x

w35x

w36x

w37x

w38x

w39x

w40x

w41x

w42x

w43x w44x

w45x

w46x

scalp potential and current source density mapping, Electroencephalogr. Clin. Neurophysiol. 72 Ž1989. 184–187. S.E. Petersen, P.T. Fox, M.I. Posner, M. Mintun, M.E. Raichle, Positron emission tomographic studies of the cortical anatomy of single-word processing, Nature 331 Ž1988. 585–589. M. Petrides, B. Alivisatos, A. Evans, Functional activation of the human ventrolateral frontal cortex during mnemonic retrieval of verbal information, Proc. Natl. Acad. Sci. U.S.A. 92 Ž1995. 5803– 5807. M. Petrides, B. Alivisatos, E. Meyer, A. Evans, Functional activation of the human frontal cortex during the performance of working memory tasks, Proc. Natl. Acad. Sci. U.S.A. 90 Ž1993. 878–882. D.S. Ruchkin, R.S. Berndt, R. Johnson Jr., W. Ritter, J. Grafman, H.L. Canoune, Modality-specific processing streams in verbal working memory: evidence from spatio-temporal patterns of brain activity, Cogn. Brain Res. 6 Ž1997. 95–113. D.S. Ruchkin, R. Johnson Jr., J. Grafman, H.L. Canoune, W. Ritter, Multiple visuo-spatial working memory rehearsal buffers: evidence from spatio-temporal patterns of brain activity, Neuropsychologia 35 Ž1997. 195–209. D.S. Ruchkin, H.L. Canoune, R. Johnson Jr., W. Ritter, Working memory and preparation elicit different patterns of event-related brain potential activity, Psychophysiology 32 Ž1995. 399–410. D.S. Ruchkin, R. Johnson Jr., J. Grafman, H.L. Canoune, W. Ritter, Distinctions and similarities among working memory processes: an event-related potential study, Cogn. Brain Res. 1 Ž1992. 53–66. M.D. Rugg, ERP studies of memory, in: M.D. Rugg, M.G.H. Coles ŽEds.., Electrophysiology of Mind, Event-Related Potentials and Cognition, Oxford Univ. Press, Oxford, 1995. M.D. Rugg, A.M. Schloerscheidt, M.C. Doyle, C.J. Cox, G.R. Patching, Event-related potentials and the recollection of associative information, Cogn. Brain Res. 4 Ž1996. 297–302. D.L. Schacter, N.A. Alpert, C.R. Savage, S.L. Rauch, M.S. Albert, Conscious recollection and the human hippocampal formation: evidence from positron emission tomography, Proc. Natl. Acad. Sci U.S.A. 93 Ž1996. 321–325. M.E. Smith, Neurophysiological manifestations of recollective experience during recognition memory judgments, J. Cogn. Neurosci. 5 Ž1993. 1–13. L.R. Squire, J.G. Ojemann, F.M. Miezin, S.E. Petersen, T.O. Videen, M.E. Raichle, Activation of the hippocampus in normal humans: a functional anatomical study of memory, Proc. Natl. Acad. Sci. U.S.A. 89 Ž1992. 1837–1841. I. Tendolkar, M.C. Doyle, M.D. Rugg, An event-related potential study of retroactive interference in memory, NeuroReport 8 Ž1997. 501–506. C.T. Trott, D. Friedman, W. Ritter, M. Fabiani, Item and source memory: differential age effects revealed by event-related potentials. NeuroReport, in press. E. Tulving, Elements of episodic memory, Behav. Brain Sci. 7 Ž1984. 257–268. E. Tulving, S. Kapur, F.I.M. Craik, M. Moscovitch, S. Houle, Hemispheric encodingrretrieval asymmetry in episodic memory: positron emission tomography findings, Proc. Natl. Acad. Sci. U.S.A. 91 Ž1994. 2016–2020. E.L. Wilding, M.C. Doyle, M.D. Rugg, Recognition memory with and without retrieval of context: an event-related potential study, Neuropsychologia 33 Ž1995. 743–767. E.L. Wilding, M.D. Rugg, An event-related potential study of recognition memory with and without retrieval of source, Brain 119 Ž1996. 889–905.