Context effects on the neural correlates of recognition memory: an electrophysiological study.

Event-related potentials (ERPs) were recorded during a recognition memory test for previously studied visual objects. Some studied objects were paired with the same context (landscape scenes) as at study, some were superimposed on a different studied context, and some were paired with new contexts. Unstudied objects were paired with either a studied or a new context. Three ERP memory effects were observed: an early effect elicited by all stimuli containing at least one studied component; a second effect elicited only by stimuli in which both object and context had been studied; and a third effect elicited by stimuli containing a studied object. Thus, test stimuli engaged three distinct kinds of memory-related neural activity which differed in their specificity for task-relevant features.

When more means less: neural activity related to unsuccessful memory encoding.

The neural correlates of memory encoding have been studied by contrasting neural activity elicited by items at the time of learning according to whether they were later remembered or forgotten [1]. Previous studies have focused on regions where neural activity is greater for subsequently remembered items [2-8]. Here, we describe regions where activity is greater for subsequently forgotten items. In two experiments that employed the same incidental learning task, activity in an overlapping set of cortical regions (posterior cingulate, inferior and medial parietal, and dorsolateral prefrontal) was associated with failure on a subsequent memory test.

The functional neuroanatomy of episodic memory.

Functional neuroimaging studies have revealed that effective encoding in episodic memory is associated with enhanced activity in left prefrontal cortex, whereas retrieval is accompanied by the enhancement of predominantly right-sided prefrontal activity. The extent of the contribution of prefrontal cortex to episodic memory, and the fact that the encoding and retrieval operations it supports are differentially lateralized, were unexpected on the basis of evidence from lesion studies. Such studies have highlighted the crucial role in episodic memory played by the hippocampus and related medial temporal lobe structures. Neuroimaging studies, however, have had only limited success in elucidating the role of the hippocampus in episodic memory. Refinements in experimental design and improved spatial resolution should promote rapid future progress with respect to this issue.

Dissociable human perirhinal, hippocampal, and parahippocampal roles during verbal encoding.

The precise contribution of perirhinal cortex to human episodic memory is uncertain. Human intracranial recordings highlight a role in successful episodic memory encoding, but encoding-related perirhinal activation has not been observed with functional imaging. By adapting functional magnetic resonance imaging scanning parameters to maximize sensitivity to medial temporal lobe activity, we demonstrate that left perirhinal and hippocampal responses during word list encoding are greater for subsequently recalled than forgotten words. Although perirhinal responses predict memory for all words, successful encoding of initial words in a list, demonstrating a primacy effect, is associated with parahippocampal and anterior hippocampal activation. We conclude that perirhinal cortex and hippocampus participate in successful memory encoding. Encoding-related parahippocampal and anterior hippocampal responses for initial, remembered words most likely reflects enhanced attentional orienting to these positionally distinctive items.

Recollection and familiarity in recognition memory: an event-related functional magnetic resonance imaging study.

The question of whether recognition memory judgments with and without recollection reflect dissociable patterns of brain activity is unresolved. We used event-related, functional magnetic resonance imaging (fMRI) of 12 healthy volunteers to measure hemodynamic responses associated with both studying and recognizing words. Volunteers made one of three judgments to each word during recognition: whether they recollected seeing it during study (R judgments), whether they experienced a feeling of familiarity in the absence of recollection (K judgments), or whether they did not remember seeing it during study (N judgments). Both R and K judgments for studied words were associated with enhanced responses in left prefrontal and left parietal cortices relative to N judgments for unstudied words. The opposite pattern was observed in bilateral temporoccipital regions and amygdalae. R judgments for studied words were associated with enhanced responses in anterior left prefrontal, left parietal, and posterior cingulate regions relative to K judgments. At study, a posterior left prefrontal region exhibited an enhanced response to words subsequently given R versus K judgments, but the response of this region during recognition did not differentiate R and K judgments. K judgments for studied words were associated with enhanced responses in right lateral and medial prefrontal cortex relative to both R judgments for studied words and N judgments for unstudied words, a difference we attribute to greater monitoring demands when memory judgments are less certain. These results suggest that the responses of different brain regions do dissociate according to the phenomenology associated with memory retrieval.

Event-related potentials and the phonological processing of words and non-words.

Event-related potentials (ERPs) were recorded during a task which required subjects to discriminate between rhyming and non-rhyming visually presented pairs of letter strings, consisting of equal proportions of word-word and word-non-word combinations. Pair members were presented sequentially with an interstimulus interval of 1.56 sec. As in a previous study [Rugg, M. D., Brain Lang. In press], ERPs elicited by rhyming and non-rhyming words were differentiated by a late negative component (N450) in waveforms following the non-rhyming words. This effect was greatest over the midline and the right hemisphere. The same rhyme/non-rhyme difference was also observed, to an equal extent, in ERPs elicited by non-words. It is concluded that N450, presumed to be related to the "N400" component observed under conditions of semantic incongruity [Kutas, M. and Hillyard, S.A., Science 207, 203-205, 1980] does not seem to depend on linguistic processing at the semantic level for its modulation.

The effects of handedness on event-related potentials in a rhyme-matching task.

Event-related potentials (ERPs) were recorded from one midline and three pairs of homotopic lateral sites while subjects determined whether or not sequentially presented words rhymed. ERPs from 11 left-handed males with a family history of sinistrality were compared with those from 12 right-handers, none of whom had such a family history. As in previous work (e.g. Rugg, M. D. Neuropsychologia 22, 435-443, 1984) the slow negative wave developing during the interval in which subjects waited for the final word was more negative from left-hemisphere electrodes, and the rhyme/non-rhyme differences in the ERPs following this word were greater over the right hemisphere. Neither of these asymmetries differed between the left and right-handers. Possible reasons for the occurrence of these ERP asymmetries during rhyme-matching are discussed, and it is suggested that the aspect(s) of linguistic processing tapped by this task, and influencing concurrently recorded ERPs, may be similarly lateralised in the brains of left- and right-handers.

Memory and consciousness: a selective review of issues and data.

Methods for dissociating and independently studying conscious (explicit) and unconscious (implicit) memory are discussed. Recent work in the field of amnesia is then briefly reviewed, focusing on the question of how clearly the disorder fractionates according to the implicit-explicit distinction. Finally, evidence supporting dual-process models of recognition memory is reviewed, and data suggesting that amnesic patients have relatively spared familiarity-based recognition memory are critically assessed.

Event-related potentials and the recognition memory exclusion task.

Subjects heard words that were presented in either a male or a female voice, and were required to perform one of two encoding tasks according to the gender of the voice. At test studied words were presented visually, along with a set of words new to the experiment. Subjects were required to respond on one key to words belonging to one of the two classes of studied word (targets), and to respond on a different key both to words belonging to the other study class (non-targets), and to words new to the experiment. In comparison to the event-related potentials (ERPs) elicited by new words, the ERPs elicited by correctly detected targets exhibited two temporally and topographically distinct positive going effects: one of these was phasic, showed a parietal maximum, and was larger over the left than the right hemisphere. The second effect was more sustained in time, frontally distributed, and was larger over the right hemisphere. The ERPs elicited by correctly classified non-targets contained the parietal effect only. These findings confirm that retrieval of contextual information in tests of recognition memory (recollection) is associated with two distinct ERP modulations. While one of these may be closely tied to process necessary for recollection, the other may reflect less obligatory processes which operate on the products of successful retrieval.

An event-related potential study of memory for words spoken aloud or heard.

Subjects made old/new recognition judgements to visually presented words, half of which had been encountered in a prior study phase. For each word judged old, subjects made a subsequent source judgement, indicating whether they had pronounced the word aloud at study (spoken words), or whether they had heard the word spoken to them (heard words). Event-related potentials (ERPs) were compared for three classes of test item; words correctly judged to be new (correct rejections), and spoken and heard words that were correctly assigned to source (spoken hit/hit and heard hit/hit response categories). Consistent with previous findings (Wilding, E. L. and Rugg, M. D., Brain, 1996, 119, 889-905), two temporally and topographically dissociable components, with parietal and frontal maxima respectively, differentiated the ERPs to the hit/hit and correct rejection response categories. In addition, there was some evidence that the frontally distributed component could be decomposed into two distinct components, only one of which differentiated the two classes of hit/hit ERPs. The findings suggest that at least three functionally and neurologically dissociable processes can contribute to successful recovery of source information.

An event-related potential study of explicit memory on tests of cued recall and recognition.

The event-related potential (ERP) correlates of performance on test of word-stem cued recall and recognition memory were contrasted. ERPs elicited by stems attracting successful recall exhibited a sustained positive-going shift relative to ERPs elicited by stems completed with unstudied items. This positive shift was maximal at electrode sites on and adjacent to the midline. An equally sustained positive-going ERP modulation was observed for the recognition memory task in ERPs elicited by recognised 'old' items relative to ERPs elicited by correctly rejected 'new' items. The scalp topography of this effect shifted from a parietally distributed asymmetry favouring left hemisphere sites, to a frontally distributed effect maximal over midline and right hemisphere sites. The findings indicate that ERP correlates of explicit memory are task-dependent. The disparate ERP effects are interpreted as reflecting a common explicit retrieval mechanism which is sensitive to the nature of retrieval cues provided at test.

Word repetition within- and across-visual fields: an event-related potential study.

A divided visual field (DVF) procedure was used to investigate the scalp distribution of the event-related potential (ERP) repetition effect. ERPs were recorded from 27 scalp sites whilst subjects (n = 20) discriminated between words and non-words presented to either the left (LVF) or the right (RVF) visual field. A proportion of the words were repeated on the trial immediately following their first presentation. In two within-field repetition conditions the two encounters with a word occurred in the same visual field (LVF or RVF). In two across-field repetition conditions, the two encounters with a word occurred in different visual fields. For both words and non-words, task performance was better for RVF presentations than for LVF presentations. In each repetition condition there was a positive-going shift in the ERP elicited by repeated words compared to that elicited by words on their first presentation. This ERP repetition effect was equivalent in magnitude and lateralised to the right hemisphere to an equivalent degree in all four repetition conditions. It is suggested that the ERP effects largely reflect the processing of visual form thought to occur predominately in the right hemisphere.

Asymmetries in event-related potentials during rhyme-matching: confirmation of the null effects of handedness.

Event-related potentials (ERPs) were recorded from 16 right- and 16 left-handed subjects during two variants of a sequential rhyme-judgement task. These variants manipulated the demands placed on short-term memory, by requiring subjects to match a word either with one or with three previously presented words. In both tasks, ERPs exhibited two lateral asymmetries: (i) during the interval prior to the final word, the CNV was more negative over the left hemisphere, and (ii) rhyme/non-rhyme differences in the amplitude of the N450 component of the ERPs to the final word were larger over the right than the left hemisphere. Neither of these asymmetries was smaller or more variable in left- than in right-handed subjects. It is suggested that these data may indicate that some aspects of language processing are, irrespective of handedness, relatively invariant in the direction and degree of their cerebral lateralization.

Event-related potentials and the semantic matching of faces.

Event-related brain potentials (ERPs) were recorded while subjects determined whether two sequentially presented famous faces depicted individuals belonging to the same or to different occupational categories. During the 1.56 sec interval between the onset of the faces, ERPs recorded from right hemisphere electrodes were more negative-going than those from electrodes over the left hemisphere. The ERPs evoked by the second face on each trial differed as a consequence of whether or not the person depicted belonged to the occupational category specified by the first face. This difference took the form of a bilaterally-distributed negative-going shift in the ERPs evoked by non-matching as opposed to matching faces. This negativity was maximal around 450 msec post-stimulus. The ERP asymmetries during the inter-stimulus interval are interpreted as evidence for the engagement of cognitive processes lateralized to the right hemisphere. The match/non-match differences are considered to reflect the modulation of an "N400" component similar to that evoked by words, and thus suggest that such components can be modulated by associative priming between non-linguistic stimuli.

Recognition memory for new associations: electrophysiological evidence for the role of recollection.

The electrophysiological correlates of recognition memory for new associations were investigated in two experiments. In both experiments subjects first studied unrelated word pairs. At test, they were presented with old words in the same pairing as at study (same pairs), old words in a different pairing from study (rearranged pairs), and pairs of new words. In Experiment 1 the test requirement was to discriminate between old and new pairs and, for any pair judged old, to then judge whether the pair was the same or rearranged. In Experiment 2 the requirement was merely to discriminate between old and new pairs. Event-related potentials (ERPs) were recorded for correctly classified same, rearranged and new pairs. The ERPs elicited by same pairs exhibited a similar pattern of effects in both experiments. Relative to the ERPs to new pairs, these effects took the form of sustained positive shifts with two distinct scalp maxima, over the left temporo-parietal and right frontal scalp respectively. ERPs to rearranged pairs showed effects which were similar in scalp topography, but markedly smaller in magnitude. This pattern of ERP effects closely resembles that found previously for test items defined as recollected on the basis of their attracting a successful source judgement. The findings therefore suggest that associative recognition memory shares some of the recollective processes that are engaged by the requirement to retrieve contextual information about a study episode. The findings from Experiment 2 indicate that the processes associated with the recollection of associated pairs are engaged regardless of whether the retrieval of associative information is an explicit task requirement.

Electrophysiological dissociation of recency and recognition memory.

Event-related brain potentials (ERPs) were recorded during the test phases of two experiments. In experiment 1, subjects first studied two consecutively presented word lists. At test, they were presented with pairs of words, and were required to judge which word had been presented most recently. The test pairs were composed of two previously studied words, one drawn from each list, (Old+Old pairs), one previously studied and one new word (Old+New pairs), or two unstudied words (New+New pairs). At temporo-parietal electrodes, ERPs to Old+Old and Old+New pairs were both reliably more positive-going than those to New+New pairs. At electrode sites overlying prefrontal cortex, ERPs to Old+Old pairs attracting correct recency judgements were more positive, from around 300 ms onwards, than those elicited by the other classes of item, which did not differ from one another. In experiment 2, the test task was changed to one that required discrimination between Old+New items on the one hand, and Old+Old and New+New pairs on the other. ERPs to Old+Old and Old+New pairs once again differed from those to New+New pairs at temporo-parietal sites, but no differences were evident between the ERPs from frontal electrode sites. In line with the evidence from lesion studies, these findings suggest that judgements of relative recency depend upon processes, supported by the prefrontal cortex, additional to those that are necessary for recognition memory. They further suggest that these processes are activated rapidly and selectively in response to pairs of studied items when these must be discriminated on the basis of their relative recency of occurrence.

The effect of encoding manipulations on neural correlates of episodic retrieval.

The present experiments investigated whether the neural correlates of explicit (conscious) retrieval from episodic memory vary qualitatively according to conditions at encoding, as is predicted by current views of the neural basis of memory retrieval. Event-related potential (ERP) correlates of word stem (e.g. MOT_) cued recall were compared for items studied under different encoding conditions. In Experiment 1, encoding was either 'shallow' or 'deep' whereas in Experiment 2 the presentation modality of the study items was either visual or auditory. In both experiments robust ERP memory effects were observed for stems completed with explicitly retrieved items from each encoding condition. The effects varied in their magnitude, such that they were largest when elicited by the more memorable class of item in each experiment. The scalp distributions of the effects did not differ according to encoding condition, a finding which offers no support for the view that retrieval involves the literal reinstatement of neural activity engaged at the time of encoding. The findings instead point to the existence of a set of retrieval operations that are engaged regardless of the conditions under which retrieved information is encoded.

Recognition memory for emotionally negative and neutral words: an ERP study.

Scalp recorded event-related potentials were used to investigate the neural activity elicited by emotionally negative and emotionally neutral words during the performance of a recognition memory task. Behaviourally, the principal difference between the two word classes was that the false alarm rate for negative items was approximately double that for the neutral words. Correct recognition of neutral words was associated with three topographically distinct ERP memory 'old/new' effects: an early, bilateral, frontal effect which is hypothesised to reflect familiarity-driven recognition memory; a subsequent left parietally distributed effect thought to reflect recollection of the prior study episode; and a late onsetting, right-frontally distributed effect held to be a reflection of post-retrieval monitoring. The old/new effects elicited by negative words were qualitatively indistinguishable from those elicited by neutral items and, in the case of the early frontal effect, of equivalent magnitude also. However, the left parietal effect for negative words was smaller in magnitude and shorter in duration than that elicited by neutral words, whereas the right frontal effect was not evident in the ERPs to negative items. These differences between neutral and negative words in the magnitude of the left parietal and right frontal effects were largely attributable to the increased positivity of the ERPs elicited by new negative items relative to the new neutral items. Together, the behavioural and ERP findings add weight to the view that emotionally valenced words influence recognition memory primarily by virtue of their high levels of 'semantic cohesion', which leads to a tendency for 'false recollection' of unstudied items.

Neural response suppression, haemodynamic repetition effects, and behavioural priming.

Repeated stimulus processing is often associated with a reduction in neural activity, as measured by single-cell recording or by haemodynamic imaging techniques like PET and fMRI. These reductions are sometimes linked to the behavioural phenomenon of priming. In this article, we discuss issues relevant to theories that attempt to relate these phenomena, concentrating in particular on the interpretative limitations of current imaging techniques.