Event-related potentials during a short-term memory task: The role of stimulus-type

Dual-process theorists posit that two components of the event-related potential (ERP), the N400 and the P300, index the processes of familiarity and recollection, respectively. We recorded EEG while subjects performed a Sternberg (1966) memory task using verbal stimuli (letters, words, and objects) and non-verbal stimuli (spatial locations and sinusoidal gratings). We found that verbal and non-verbal stimuli elicit qualitatively different ERPs during encoding and retrieval. The N400 differentiates old and new verbal stimuli, but does not differentiate old and new non-verbal stimuli. However, the P300 differentiates old and new stimuli of both types. We conclude that familiarity requires a semantic label, but recollection does not. According to dual-process theorists, dissociations observed in recognition memory tasks can be explained by two separable memory processes: recollection and familiarity (for review, see Yonelinas, 2002). Dual process theorists generally describe recollection as a process involving the recognition of specific details, including episodic information, while they describe familiarity as a feeling of knowing in the absence of source information. The classic illustration of this dissociation is the experience of being “familiar” with a person’s face without being able to “recollect” the person’s name (Mandler, 1991). Despite years of research, dual-process theorists still lack a full understanding of how familiarity and recollection operate, and in what ways these processes differ from each other. In the following study, we explore the differences in the event-related potentials (ERPs) during verbal and visual Sternberg (1966, 1975) memory tasks. We are interested in seeing how established effects from ERP studies of verbal memory generalized to visual memory, and most importantly, what this means for the current dual-process accounts of these effects. The sizeable literature on the effect of stimulus repetition on the ERP has found that ERPs evoked by previously experienced stimuli are more positive-going than ERPs evoked by new stimuli (for review, see Johnson, 1995; Rugg, 1995). This effect, variably referred to as the “ERP repetition effect” or the “ERP old/new effect,” has been divided into early and late factors corresponding to the N400 and P300 components of the ERP. This division is justified by evidence demonstrating that these two components are sensitive to different experimental manipulations (Smith, 1993; Curran, 2000) and arise from distinct neural sources (Smith & Halgren, 1989; Guillem, N’Kaoua, Rougier, & Claverie, 1995). While initial attempts to interpret these two components within a dual-process framework ERPS AND MEMORY FOR DIFFERENT STIMULUS-TYPES 2 yielded a hodgepodge of relatively unsupported claims (Potter, Pickles, Roberts, & Rugg, 1992; Wilding, Doyle, & Rugg, 1995; Wilding & Rugg, 1996, 1997; Rugg, Schloerschedit, & Mark, 1998), recent studies using novel experimental paradigms, including the remember/know procedure (Tulving, 1985), have led to a more lucid picture in which the N400 indexes familiarity and the P300 indexes a recollective process (Duzel, Yonelinas, Mangun, Heinze, & Tulving, 1997; Curran, 2000; Curran, Tanaka, & Weiskopf, 2002; Curran & Cleary, 2003; Curran, 2004). When interpreted within a dual-process framework, the remember/know procedure generates responses corresponding to both recollection (“remember”) and familiarity (“know”). Several studies have found that the P300 component of the ERP old/new effect is associated with “remember” responses, while the N400 component is associated with “know” responses (Smith, 1993; Curran, 2004; Duzel et al., 1997). Curran and colleagues (2000, 2003) have corroborated these finding in a series of experiments using a variation on the study-test procedure in which subjects are expected to differentiate between studied stimuli and new stimuli that are sometimes very similar to the studied stimuli. They found that stimuli similar to those on the study list led to flunctuations in the N400 consistent with a feeling of familiarity, while only items identical to those on the study list caused flunctuations in the P300. This is consistent with the P300 being an index of recollection, a process that involves the recognition of details. An alternative to dual-process perspectives of the ERP old/new effect is the “context integration hypothesis” (Rugg & Doyle, 1994; Mecklinger, 1998). Rugg and Doyle (1994) argued that the N400 component represents the degree to which a word can be integrated with its context. According to the context integration hypothesis, contextual integration is facilitated when a word re-occurs one or more times in the same context. Furthermore, Rugg and Doyle (1994) claimed that context integration is dependent on certain stimulus properties, particularly the ability of the stimulus to be represented as a semantic construct that they refer to as a “unitary code. ” Because of this restraint, the context integration hypothesis predicts that non-verbal stimuli should not elicit the N400 component of the ERP old/new effect. Consistent with the predictions of the context integration hypothesis, a series of studies have shown that a robust ERP old/new effect is elicited by words (Rugg, 1985), nonwords (Rugg, 1987; Rugg & Nagy, 1987), and meaningful pictures (Zhang, Begleiter, Porjesz, & Litke, 1997; Rugg & Doyle, 1994), but no effect is evoked by various non-verbal stimuli, including orthographically illegal nonwords (Rugg & Nagy, 1987), meaningless pictures (Rugg & Doyle, 1994; Thomas, 1992; Zhang et al., 1997; Crites, Delgado, Devine, & Lozano, 2000), novel objects (Rugg, 1995; Beisteiner et al., 1996), and spatial locations (Bosch, Mecklinger, & Friederici, 2001; Mecklinger & Muller, 1996; Mecklinger, 1998; Mecklinger & Bosch, 1999; Mecklinger & Meinshausen, 1998). While two studies have found ERP old/new effects using seemingly non-verbal stimuli (Curran et al., 2002; Penney, Mecklinger, Hilton, & Cooper, 2000), both of these studies involved substantial training that may have allowed the subjects to categorize and semantically encode the stimuli. Electrophysiological studies of recognition memory find that repeated words elicit more positive-going ERPs when compared to new words. The effect encompasses both the N400 and P300 components of the ERP and is often absent when non-verbal stimuli are used, but most investigations of this effect using non-verbal stimuli have not looked at the N400 and P300 components of the ERP separately. It is important to analyze these ERPS AND MEMORY FOR DIFFERENT STIMULUS-TYPES 3 components separately given evidence that they arise from different sources (Guillem et al., 1995) and represent distinct processes (Curran, 2000). In the following study, five different stimulus-types are used in a Sternberg (1966) short-term scanning memory paradigm in an attempt to better understand the effect of stimulus rehearsability on the ERP and the ERP old/new effect in particular. Stimulus-types include letters, words, objects, spatial dot locations (Jonides et al., 1993), and sinusoidal gratings (Kahana & Sekuler, 2002; Zhou, Kahana, & Sekuler, 2004). It is our hope that by using a range of stimuli varying in several stimulus properties, including verbal rehearsability, we will acquire a better understanding of the early and late components of the ERP old/new effect, and whether or not they depend on a semantic code. Furthermore, better understanding the role that the N400 and P300 components play in visual and verbal recognition memory may in turn shed some light on the processes familiarity and recollection that have been associated with these components.1