Research report
The late negative episodic memory effect: the effect of recapitulating study details at test

https://doi.org/10.1016/j.cogbrainres.2004.10.005Get rights and content

Abstract

An hypothesis concerning mnemonic function suggests that perceptual details of previously experienced episodes are retrieved from the cortices that initially processed that information during the encoding phase. Cycowicz et al. [Cycowicz, Y.M., Friedman, D. and Snodgrass, J.G., Remembering the color of objects: an ERP investigation of source memory, Cereb Cortex, 11 (2001) 322–334.] have interpreted the presence of a late negative episodic memory (EM) effect, maximal over parieto-occipital scalp, as a brain signature of the search for and/or retrieval/evaluation of the specific perceptual source-specifying attributes (i.e., color) of pictures in the visual cortical regions that were recruited during the encoding of that information. The present study assessed the validity of this hypothesis. Twelve participants studied pictures outlined in red or green and were subsequently tested with inclusion (i.e., item; old or new regardless of color) and exclusion (i.e., source; same color, different color/new judgments) tasks. In both, old pictures were presented either in the same color as at study or in the alternate color. A late negative, parieto-occipital EM effect was of much larger amplitude in the source compared to the item task. It was of similar magnitude to correctly recognized pictures whose colors were identical at study and test relative to those whose colors changed, and was not modulated by the success or failure of the source retrieval. These data run counter to the initial hypothesis that the late negative EM effect reflects the search for and/or retrieval of specific perceptual attributes such as color. Rather, the late negative EM effect may reflect the search for and/or retrieval/evaluation of more general source-specifying information in the cortical regions that initially processed the stimuli.

Introduction

Investigators of memory function have often contrasted two processes, familiarity and recollection, which are thought to underlie recognition memory performance [18]. Whereas familiarity is relatively automatic and is hypothesized to underlie the retrieval of item or content information without the details, or context within which the event was embedded, recollection is effortful and is required when retrieving contextual information, such as the spatio- (where) temporal (when) attributes within which the initial episode was encountered. The retrieval of contextual attributes is labeled source memory.

Compared to simple, old/new recognition memory paradigms, source memory paradigms, in addition to requiring old/new memory judgments, also solicit judgments concerning the context within which the original episode was experienced. For example, during a study phase participants might hear words presented in either a male or female voice. During the subsequent test phase, subjects would be asked to make old/new judgments to visually presented words. Then, for any word judged old, they would be asked to provide a source judgment concerning the original presentation, was it presented in either the male or female voice? [35]. In this type of memory experiment, simply judging whether the item is old or new can be accomplished without reference to contextual details, i.e., this judgment can be based solely on whether the item seems familiar or not.

However, remembering whether the item was presented, for example, by a male or female voice, requires active recollection of such contextual information. In these kinds of designs, a recollection-based response has been operationalized as a correctly recognized old item (i.e., a hit) whose source has also been correctly retrieved. A familiarity-based recognition response has been operationalized as a correctly recognized old item whose source has been incorrectly attributed. Presumably, this indicates that this latter type of recognition judgment was not accompanied by contextual detail. That is, an item correctly recognized as old, but receiving an incorrect source judgment is assumed to be based only on familiarity; an item correctly recognized as old attracting a correct source judgment is assumed to be based on familiarity as well as recollection.

This source memory paradigm has been very often employed in event-related brain potential (ERP) studies of recognition memory. The aim of these investigations has been to obtain brain activity signatures corresponding to familiarity and recollection hypothesized to operate in two-process theories of recognition memory [18]. Investigators using this type of paradigm have uncovered a series of old/new or episodic memory (EM) effects that appear to reflect unique mnemonic functions [7], [13], [24], [25]. Typically, correctly recognized old items elicit greater positivity than correctly rejected new items. The EM effect is then defined as the ERP difference between correctly recognized old and correctly rejected new items. The most consistently reported EM effects have been labeled the medial prefrontal EM effect (active between about 300 and 500 ms), the left parietal EM effect (500–900 ms), and the right prefrontal EM effect (800–2000 ms). Some consensus as to the functional roles of each of these EM effects exists. The medial prefrontal EM effect has been associated with the familiarity component of recognition memory [2], [14], [19] (but see [37] and [29]). This conclusion is based on the findings that the medial prefrontal EM effect is of equivalent magnitude in the ERPs associated with previously studied, correctly recognized old items whether those items were given a “remember” (retrieval of context based on recollection) or “know” (retrieval of content based on familiarity) judgment [28], according to the paradigm originally described by Tulving [30]. In the same vein, the medial prefrontal EM effect is generally of equivalent magnitude in the ERPs associated with old items and unstudied lures that are highly similar to one another and thus generate a large familiarity signal [2], [22]. The subsequent parietal EM effect has been associated with recollection, based on a large number of findings indicating that this EM effect is larger in association with items whose sources are correctly attributed compared to those that are not [28], [34], [35]. The functional role of the right prefrontal EM effect is currently controversial, although some investigators have advanced the hypothesis that it reflects some kind of executive control function, such as monitoring the products of retrieval in the service of modifying ongoing memory performance (e.g., Refs. [25], [36]).

Relatively few types of contexts or sources have been used in these investigations, which have included gender of voice, spatial location and list membership (i.e., temporal context). Despite the obvious differences, these source types have yielded fairly similar EM effects. By contrast with these types of source information, Cycowicz et al. [5] used line drawings of common objects that were painted in either red or green during the study phase. During two ensuing test phases, pictures were outlined in black and, in the inclusion or item test, subjects had to judge simply whether the picture was old or new, regardless of its outline color in the study phase; during the exclusion or source test, subjects had to judge whether the item was initially painted in a target color (for example, red) during study (hereafter referred to as Targets), or was painted in the alternate color (green in this example) or was new (these latter responses were assigned to the same response hand). Previously studied pictures painted in the alternate color are hereafter designated as Nontargets to distinguish them from new pictures.

Unlike previous investigations of source memory, Cycowicz et al. recorded a large-amplitude negative EM effect, maximal over parieto-occipital scalp, which was markedly larger in the source than the item task. Due to three factors, (1) the source in this paradigm was color, (2) the negative EM was coincident with mean reaction time (RT), and (3) the negative EM effect showed a topographic focus over parieto-occipital scalp, Cycowicz and co-workers suggested that the late negative EM effect could have reflected the search for and/or retrieval of the color in which the picture was painted during the study phase in the cortical regions that originally processed color information.

As mentioned, the peak latency of the negative EM effect (between ∼800 and 1000 ms) occurred at about the same time as mean reaction time. The negative activity onset as the preceding parietal EM effect was returning to baseline. On this basis, Cycowicz et al. [5] advanced the hypothesis that sufficient time would have elapsed for the late negative EM effect to have reflected brain activity related to an attempt to reinstate the initial image along with its associated color during the source retrieval task [6]. Further, in the original Cycowicz et al. study [5], the negative EM effect was as large during successful as it was during unsuccessful source retrieval. Hence, the “reinstatement” interpretation offered by Cycowicz and co-workers is consistent with the presence of negative-going activity in the ERPs associated with trials on which an incorrect source decision had been made, as subjects would have had to attempt to retrieve the conjunction of attributes (the picture and its color) regardless of the success of the retrieval attempt.

Although other investigators had also observed similar negative-going EM effects (review by Ref. [11]), Cycowicz et al. [5] were, to our knowledge, the first to compare directly this activity between item and source retrieval tasks. Subsequent investigations have also assessed the difference between item and source tasks. For example, in a study by Johansson et al. [12], subjects viewed words which were followed by the presentation of a rectangular outline. In half the trials, a picture was presented within the rectangle. In the remainder, a picture was not presented and subjects were asked to imagine the object named by the label and project it into the rectangular outline. For both types of trials, subjects were asked to determine how well the pictured (or imagined) object fit the verbal label. At test, subjects performed two tasks, in which only the verbal labels of previously studied and new items were intermixed. One task was a simple, old/new recognition paradigm, the other a source monitoring procedure. In the latter, participants had to retrieve the action they performed during study (either viewing the object or imagining it) in association with the verbal label. By contrast with the old/new recognition task, a late-onset, negative EM effect was of much larger amplitude in the source task. It peaked between 1000 and 1200 ms and was maximal over parieto-occipital scalp, highly similar to the negative EM effect recorded by Cycowicz et al. [5] (the scalp topography of the Johansson et al. [12] negative EM effect can be seen in Fig. 2 of Johansson and Mecklinger [11]). Johansson et al. [12] raised the possibility, consistent with the interpretation offered by Cycowicz et al. [5], that the negativity reflected the reinstatement of the original object (or imaged object) along with the action that was performed (perceiving or imagining).

Although lacking a comparison of item and source tasks, Leynes et al. [16] also assessed source monitoring by asking their subjects during study to perform an action or to plan to perform the action in response to the presentation of an action phrase. During test, the action phrases (planned and performed) were re-presented intermixed with new action phrases. Participants were required to identify the phrase as performed, planned or new. Leynes et al. recorded a large-amplitude, negative EM effect that peaked between 1200 and 1800 ms and displayed a parieto-occipital topography. Because both planning to perform an action and actual performance of an action phrase involve a high degree of visual processing, the Leynes et al. data may also be interpreted as consistent with the reinstatement of the representation of the action and its contextual attribute, i.e., whether it was planned or performed. In both the Johansson et al. [12] and Leynes et al. [16] investigations, the parieto-occipital topography of the negative EM effects is consistent with these computations involving visual cortical processing regions.

Johansson and Mecklinger [11] have reviewed these and other studies in which late, negative EM effects have been observed. The main conclusions from the review are that (1) this negative activity can be recorded in old/new recognition memory paradigms, provided “action monitoring” is required—typically engendered by difficult response demands, as in false memory paradigms. In these tasks the negativity is observed with a posterior scalp topography, but only in reaction time (RT)-locked averages; (2) the late negative EM effect occurs whether retrieval is successful or not and (3) when attribute conjunctions may have to be retrieved (as in source memory paradigms), the negativity is observed in stimulus-locked averages. Johansson and Mecklinger [11] proposed that, in source memory tasks, the stimulus-locked, late negative EM effect could reflect “… processes related to forming and holding a representation of a conjunction of attributes that specify the prior episode” (p. 23), for example, the pictorial object and its color as in previous investigations from this laboratory [3]. As stated earlier, both the original object and its associated color might be reinstated for evaluation.

Based on the fact that the late negative EM effect is not associated with successful retrieval, it is possible that, similar to the functional role proposed for the right prefrontal EM effect, the late negative EM effect might reflect monitoring and/or evaluative operations that, due to the perceptual nature of the source (e.g., color; visualizing whether an object was imagined or viewed), take place in posterior cortical regions associated with visual processing. In previous investigations from this laboratory, pictures were presented in red or green outline during the study phase, but were presented in black outline during the test phases. In the current investigation, by contrast, pictorial objects were presented in red or green outline during the encoding phases and then, during two test phases, were re-presented either in the same color as during study or the alternate color. During the item test, subjects were required to judge the items as old or new regardless of the color in which they were outlined during study and test. On the other hand, during the source test subjects had to make Same (old object, same color) or Different (old object, different color)/New judgments, labeled, respectively, target old, nontarget old and new items.

It was predicted, based on previous work from this [3], [5] and other [11] laboratories, that the amplitude of the negative EM effect would not be modulated by whether or not retrieval of source attributes was successful. Johansson and Mecklinger [11] postulate that the late negative EM effect is generated when attributes of the previously studied item are not easily recovered upon presentation of the test probe. In the current experimental design, this might occur when the object presented at test is painted in a different color than its studied counterpart, because the color cue does not match the stored representation. On this view, one would predict larger negative activity when the test cue and the stored representation differ. Johansson and Mecklinger [11] have also suggested that the magnitude of the posterior negative EM effect increases when response demands are complex or difficult. On this basis, one could predict that this negative EM effect would be larger to nontargets in the exclusion or source task, as these items require a complex hand to response mapping, i.e., nontarget old and new items are both assigned to the same response hand, whereas target old items require a different response hand.

Section snippets

Materials and methods

For ease of exposition, the inclusion or old/new recognition task will be referred to as the “item” task, because the retrieval of contextual information is not explicitly required. By contrast, the exclusion task, which requires retrieval of context, will be referred to as the “source” task. We use these terms as convenient labels, even though on a proportion of “item task” trials recollection may have been involved and on a proportion of “source task” trials a familiarity process was

Behavioral data

Table 1 presents the behavioral data from the item (A) and source (B) tasks.

Discussion

The results of the current study replicate well two previous findings: (1) greater magnitude late negative activity in the source compared to the item task; and (2) very little difference between tasks in the magnitude of the parietal EM effect. The current data suggest that the negative EM effect reflects the search for and/or retrieval/evaluation of source-specifying information, although what is searched for, retrieved and/or evaluated does not necessarily have to be specific, color features

Acknowledgments

The authors thank Mr. Charles L. Brown, III for computer programming and technical assistance, Ms. Letecia Latif for subject recruitment, and the volunteers for generously giving their time. This study was supported in part by grant HD14959 from NICHD, and by the New York State Department of Mental Hygiene.

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