Do I know you? Insights into memory for faces from brain potentials.

The recognition of faces is central to human social interaction. Recordings of event-related potentials (ERPs) from the brain can shed light on the various processes that occur when a face is recognized and when knowledge related to a specific person is retrieved. ERP contrasts between processing familiar and processing novel faces offer a gateway into investigations of semantic memory for familiar persons. In particular, activity of face recognition units and semantic information units--memory representations of faces and person-related knowledge, respectively--can be indexed by specific ERPs. These potentials thus provide valuable tools for studying the cognitive and neurobiological architecture of person recognition. ERPs have also been found useful for investigating other types of memory for faces. Specifically, important insights have been derived from the study of a category of memory phenomena known as priming. Priming can be revealed in special tests when face recognition is facilitated based on prior experience. Describing the neural processes associated with memory for faces is an exciting focus of research, and future results from this line of inquiry promise to provide further knowledge about face recognition and the various types of memory that can be provoked by a human face.

Neural events that underlie remembering something that never happened.

We induced people to experience a false-memory illusion by first asking them to visualize common objects when cued with the corresponding word; on some trials, a photograph of the object was presented 1800 ms after the cue word. We then tested their memory for the photographs. Posterior brain potentials in response to words at encoding were more positive if the corresponding object was later falsely remembered as a photograph. Similar brain potentials during the memory test were more positive for true than for false memories. These results implicate visual imagery in the generation of false memories and provide neural correlates of processing differences between true and false memories.

Word repetition in amnesia. Electrophysiological measures of impaired and spared memory.

Amnesic patients often show improved performance when stimuli are repeated, even in the absence of conscious memory for those stimuli. Although these performance changes are typically attributed to perceptual or motor systems, in some cases they may be related to basic language processing. We examined two neurophysiological measures that vary with word repetition in 12 amnesic patients and 12 control subjects: (i) a late positive component of the event-related potential (ERP) linked to conscious memory and (ii) the N400 component that varies with language comprehension. In each trial, the subject heard a category name, then viewed a word, and then decided whether the word was semantically congruous or incongruous (e.g. 'yes' for 'baby animal: cub'; 'no' for 'water sport: kitchen'). Recall and recognition testing at the end of the experiment showed that control subjects had better memory for congruous than for incongruous words, as did the amnesic patients, who performed less well overall. In contrast, amnesic patients were unimpaired on the category decisions required in each trial and, like the control subjects, showed a large N400 for incongruous relative to congruous words. Similarly, when incongruous trials were repeated after 0-13 intervening trials, N400s were reduced in both groups. When congruous trials were repeated, a late positive repetition effect was observed, but only in the control group. Furthermore, the amplitude of the late positive repetition effect was highly correlated with later word recall in both patients and controls. In the patients, the correlation was also observed with memory scores from standardized neuropsychological tests. These data are consistent with a proposed link between the late positive repetition effect and conscious memory. On the other hand, the N400 repetition effect was not correlated with episodic memory abilities, but instead indexed an aspect of memory that was intact in the amnesic patients. The preserved N400 repetition effect is an example of preserved memory in amnesia that does not easily fit into the categories of low-level perceptual processing or of motor learning. Instead, the sensitivity of the N400 to both semantic context and repetition may reflect a short-term memory process that serves language comprehension in realtime.

Brain potentials associated with recollective processing of spoken words.

The neurocognitive foundations of recollection can be explored by recording event-related potentials (ERPs) from the human brain. In the present study, we monitored brain activity while participants heard a series of words, first in a study phase and again, 1-2 min later, in a test phase, when both priming and recognition were measured. Level of processing at study was manipulated within-subjects via instructions either to visualize the referent of each word (the image task) or to detect the presence of target letters (the letter task). Priming of lexical decision response time was observed but did not differ across study task, whereas recognition was better for image- than for letter-task words. Brain potentials recorded at test revealed a task effect, wherein ERPs were more positive for image- than for letter-task words approximately 600-900 msec after word onset. The task effect was restricted to posterior scalp locations and was interpreted as an indication of visual imagery triggered by spoken words. Given that similar potentials were also elicited at study, we speculate that accurate recognition of words from the image task involved the recapitulation of the visual imagery that was initially engaged during the study phase.

Neural correlates of memory retrieval and evaluation.

Results from recent neuroimaging studies have led to a controversy as to whether right or left prefrontal regions are relatively more important for episodic retrieval. To address this issue, we recorded event-related brain potentials during two recognition tests with identical stimuli but differing retrieval demands. In both tests, participants viewed a sequence of object drawings, half of which were identical to ones viewed earlier except for a change in size and half of which were new. Instructions were to discriminate between old and new objects (general test) or to additionally decide whether old objects were larger or smaller at study (specific test). Frontal brain potentials that were more positive during the specific than during the general test for both old and new objects were interpreted as neural correlates of the process by which specific attributes of test cues are compared with information retrieved from memory. Another ERP difference between the specific and general tests, which was observed for old objects only, had a left posterior scalp topography and was interpreted to reflect the reactivation of memories for studied objects. Frontal and posterior potentials thus reflected two memory processes important for accurate episodic retrieval. Furthermore, our findings suggest that both left and right prefrontal regions were engaged when demands to retrieve and evaluate perceptual information increased.

Electrophysiological correlates of recollecting faces of known and unknown individuals.

We recorded brain potentials from healthy human subjects during a recognition test in order to monitor neural processing associated with face recollection. Subjects first attempted to memorize 40 faces; half were accompanied by a voice simulating that person speaking (e.g., "I'm Jimmy and I was a roadie for the Grateful Dead") and half were presented in silence. In the test phase, subjects attempted to discriminate both types of old faces (i.e., "named" and "unnamed" faces) from new faces. Recognition averaged 87% correct for named faces, 74% correct for unnamed faces, and 91% correct for new faces. Potentials to old faces were more positive than those to new faces from 300 to 600 ms after face onset. For named faces, the old-new ERP difference was observed at anterior and posterior scalp locations. For unnamed faces, the old-new ERP difference was observed only at posterior scalp locations. Results from a prior experiment suggest that these effects do not reflect perceptual priming of faces. The posterior portion of the old-new ERP difference was thus interpreted as a neural correlate of retrieval of visual face information and the anterior portion as an indication of retrieval of person-specific semantic information.

Neural measures of conscious and unconscious memory.

Neuropsychological studies of memory disorders have played a prominent role in the development of theories of memory. To test and refine such theories in future, it will be advantageous to include research that utilizes physiological measures of the neural events responsible for memory. Measures of the electrical activity of the brain in the form of event-related potentials (ERPs) provide one source of such information. Recent results suggest that these real-time measures reflect relevant encoding and retrieval operations. In particular, distinct electrical responses have been associated with recollective processing of words and with priming of visual word-form. This source of evidence can thus enrich our understanding of both the cognitive structure and neural substrates of human memory.

Frontal brain activity during episodic and semantic retrieval: insights from event-related potentials.

Previous neuropsychological and neuroimaging results have implicated the prefrontal cortex in memory retrieval, although its precise role is unclear. In the present study, we examined patterns of brain electrical activity during retrieval of episodic and semantic memories. In the episodic retrieval task, participants retrieved autobiographical memories in response to event cues. In the semantic retrieval task, participants generated exemplars in response to category cues. Novel sounds presented intermittently during memory retrieval elicited a series of brain potentials including one identifiable as the P3a potential. Based on prior research linking P3a with novelty detection and with the frontal lobes, we predicted that P3a would be reduced to the extent that novelty detection and memory retrieval interfere with each other. Results during episodic and semantic retrieval tasks were compared to results during a task in which subjects attended to the auditory stimuli. P3a amplitudes were reduced during episodic retrieval, particularly at right lateral frontal scalp locations. A similar but less lateralized pattern of frontal P3a reduction was observed during semantic retrieval. These findings support the notion that the right prefrontal cortex is engaged in the service of memory retrieval, particularly for episodic memories.

An electrophysiological analysis of modality-specific aspects of word repetition.

Priming effects to words are reduced when modality changes from study to test. This change was examined here using behavioral and electrophysiological measures of priming. During the study, half of the words were presented visually and half auditorally; during a subsequent lexical decision test, all words were presented visually. Lexical decisions were faster for within- than cross-modality repetitions. In contrast, modality influenced recognition only for low-frequency words. During lexical decision, event-related brain potentials were more positive to studied than unstudied words (200-500 ms). A larger and shorter duration effect was observed for within- than cross-modality repetitions (300-400 ms). This later effect is viewed as an electrophysiological index of modality-specific processing associated with priming. Results suggest that multiple events--both modality-specific and modality-nonspecific--underlie perceptual priming phenomena.

Frontal brain potentials during recognition are modulated by requirements to retrieve perceptual detail.

To assess the role of prefrontal cortex in retrieval and address the controversy about whether prefrontal retrieval operations are engaged only following successful retrieval, we recorded event-related brain potentials during two recognition tests with differing demands on retrieval effort. Both tests included object drawings that were (1) identical to those studied, (2) the same but with altered aspect ratios, and (3) previously unseen. Instructions were to respond "old" only if drawings were not modified (specific test) or regardless of modifications (general test). Frontal potentials were enhanced during the specific relative to the general test for all three types of drawings. We conclude that these potentials reflected differential engagement of strategic retrieval, that this function relied on left prefrontal cortex, and that it was not contingent on successful retrieval.

Brain waves following remembered faces index conscious recollection.

At a glance, one can often determine whether a face belongs to a known individual. To investigate brain mechanisms underlying this memory feat, we recorded EEG signals time-locked to face presentations. In the study phase, 40 unknown faces were presented, 20 of which were accompanied by a voice simulating that person speaking. Instructions were to remember the faces with spoken biographical information (R-faces) and to forget the others (F-faces). In the test phase, famous and non-famous faces were presented in a visually degraded manner. Subjects made two-choice fame judgments and priming was observed in the form of faster and more accurate responses for old than for new non-famous faces. Priming did not differ between R-faces and F-faces. In a second experiment, faces were not degraded at test and behavioral responses were made only when faces were presented twice in immediate succession. Brain potentials elicited 300 to 900 ms after stimulus onset from frontal and parieto-occipital scalp regions were larger for R-faces than for F-faces. Recognition tested later was more accurate for R-faces than for F-faces. Because the study-phase manipulation influenced recognition but not priming, we conclude that this procedure succeeded in isolating neural correlates of recollective processing from more automatic uses of face memory as indexed by priming.

Memory changes with normal aging: behavioral and electrophysiological measures.

We examined performance in young and elderly on an implicit (lexical decision) and an explicit (recognition) memory test. The difference in lexical decision times between old and new words was equivalent in the two groups, although the elderly were slower. In both groups, recognition accuracy (lower in the elderly) was higher following semantic than nonsemantic encoding, whereas lexical decision times were unaffected. Divergent brain potentials for old and new words during lexical decisions constituted a repetition effect, which reflected greater positivity (200-800 ms) for old words, particularly over the left hemisphere; this effect was smaller and later in the elderly. An electrophysiological marker of enhanced recollection for words from the semantic encoding task took the form of a left-sided positivity (500-800 ms). The effect was smaller in the elderly than the young, providing an additional index of their impaired recognition processes.

Brain potentials associated with perceptual priming vs explicit remembering during the repetition of visual word-form.

Priming of visual word-form was studied using a reading manipulation in which some words appeared in a backward format (e.g., d-r-o-w) instead of the usual forward format. In Experiment 1, subjects discriminated occasional targets (common first names) from other words with a speeded response. Reaction time was faster for words that had also appeared earlier in the forward format compared to the backward format. Event-related potentials (ERPs) recorded in response to word presentations showed a corresponding difference, a positive offset present during the time interval beginning about 300 ms after word onset from electrodes over occipital and parietal cortex. In Experiment 2, the task was changed to a recognition test, and a later and more widespread ERP response was observed, thus confirming the association between the ERP difference in Experiment 1 and priming rather than explicit remembering. ERP measures were presumably sensitive to neural events underlying the specific influence of recent reading experiences on the processing of visual word-form, thus providing real-time evidence on the neural mechanisms of priming.

An electrophysiological measure of priming of visual word-form.

Priming and recollection are expressions of human memory mediated by different brain events. These brain events were monitored while people discriminated words from nonwords. Mean response latencies were shorter for words that appeared in an earlier study phase than for new words. This priming effect was reduced when the letters of words in study-phase presentations were presented individually in succession as opposed to together as complete words. Based on this outcome, visual word-form priming was linked to a brain potential recorded from the scalp over the occipital lobe about 450 ms after word onset. This potential differed from another potential previously associated with recollection, suggesting that distinct operations associated with these two types of memory can be monitored at the precise time that they occur in the human brain.

Impaired acquisition and rapid forgetting of patterned visual stimuli in Alzheimer's disease.

Whether or not rate of forgetting is accelerated in Alzheimer's disease (AD) is controversial. This study examined recognition of visual patterns in patients with AD and in controls at 10 min relative to a learning baseline measured after a 10-s delay (delayed recognition ratio, DRR). Comparable baseline performances were attained in the two groups by manipulating stimulus exposure times. Comparisons between 25 AD and 48 age-matched controls demonstrated lower DRR in AD when initial recognition, which was statistically worse in AD, was covariated. DRR was also lower in an analysis of subgroups closely matched on initial performance. The findings suggest that forgetting is accelerated in AD because multiple aspects of memory processing, including storage, are impaired.

Consolidating dispersed neocortical memories: the missing link in amnesia.

Consolidation is often conceptualised as a general process by which memory traces can be strengthened in the brain. An alternative idea, developed here, is that a particular sort of consolidation is required for establishing memories belonging to a neurobiologically defined category-memories dispersed across multiple distinct neocortical zones. These memories are consolidated via the formation of a neocortical cell assembly that confers coherence to the set of scattered neocortical memory traces. A set of memory traces linked in this manner can subsequently serve as the basis for conscious recollection. A disruption of this neocortical consolidation process is held to be responsible for the patterns of preserved and impaired memory observed in amnesic patients. A suitable strategy for empirically testing this sort of theory requires an examination of evidence from neuropsychological studies of amnesia and from studies of the neural substrates of memory functions in normal subjects.

Functional Neuroimaging of Cortical Dysfunction in Alcoholic Korsakoff's Syndrome.

Many neuropsychological investigations of human memory have focused on the amnesic deficits of alcoholic Korsakoff's syndrome. Structural neuroimaging suggests that the syndrome results from midline diencephalic damage, but functional neuroimaging has the potential to reveal additional neuropathology that may be responsible for cognitive dysfunction. Accordingly, high-resolution positron emission tomography (PET) was used to measure regional cerebral metabolic rates for glucose utilization in five alcoholic Korsakoff patients and nine alcoholic control subjects. Results from a continuous recognition test administered during the radiotracer uptake period indicated that all subjects performed normally with respect to immediate memory, whereas Korsakoff patients demonstrated a marked memory impairment in delayed recognition. PET results from the Korsakoff group showed a widespread decline in glucose metabolism in frontal, parietal, and cingulate regions, suggesting that these functional abnormalities in the cerebral cortex contribute to the memory impairment. Hippocampal glucose metabolism did not differ between the groups. Thus, the evidence did not support the hypothesis that parallel brain dysfunctions are responsible for the similar amnesic symptomatology after hippocampal and diencephalic damage. We hypothesize that the amnesic dysfunction of Korsakoff's syndrome depends on a disruption of thalamocortical interactions that mediate a function critical for normal memory storage.

New-association priming of word identification in normal and amnesic subjects.

Subjects took an implicit memory test in which pairs of unrelated words were flashed briefly and the ability to identify the second word of each pair was measured as a function of prior study. In young subjects, identification was better when the second word had been studied compared to when it had not been studied (word-specific priming). Identification was also better when the two words had been paired at study compared to when they had been studied separately (association-specific priming). In amnesic patients, word-specific priming was normal compared to that in age- and IQ-matched control subjects. Association-specific priming was observed, but it was below normal levels. This outcome suggests that the amnesic dysfunction can encompass priming of new verbal associations but spare priming of existing verbal information.

Potentials evoked in human and monkey medial temporal lobe during auditory and visual oddball paradigms.

Event-related potentials (ERPs) were recorded from epileptic patients with electrodes chronically implanted in the medial temporal lobe (MTL) and other intracranial locations, and from monkeys with epidural, transcortical, and MTL electrodes. For both humans and monkeys, the eliciting events consisted of trains of auditory or visual stimuli in which a random 10-20% deviated in pitch or pattern from the remaining stimuli. The distribution of ERPs elicited by the rare (oddball) stimuli in both species was similar, consisting of a P3 recorded from the scalp or cortical surface and a slightly later, but temporally overlapping, focal negativity in the hippocampus and nearby MTL structures. The similarity between the patterns of ERPs in humans and monkeys establishes the feasibility of studying the electrogenesis of P3-like activity with detailed intracranial recordings in an animal model. The data also establish that the MTL ERPs in human patients represent a normal neurophysiological process unrelated to epilepsy.

Event-related potentials elicited by deviant endings to melodies.

Event-related potentials were recorded from scalp electrodes while subjects listened to well-known melodies. The melodies ended either with the expected note or with a different note. This design was a nonlinguistic analogue of the design used by Kutas and Hillyard (1980b), who first reported that anomalous terminal words in sentences elicited N400 potentials. However, Besson and Macar (1987) reported that deviant terminal notes in melodies did not elicit N400 potentials. In the present study, additional time was allowed for expectations to develop for the terminal note. Deviant terminal notes did not elicit N400s. In both studies, however, the deviant notes elicited P300-like waves. This outcome raised the possibility that N400 might have been masked by the positive potential. In a second condition in which P300 amplitude was minimized, N400s were again not evident. These results thus illustrate two additional situations in which nonlinguistic stimuli that deviated from a sequential pattern failed to elicit N400 potentials.