Orbitofrontal and hippocampal contributions to memory for face-name associations: the rewarding power of a smile

Memory processes can be enhanced by reward, and social signals such a smiling face can be rewarding to humans. Using event-related functional MRI (fMRI), we investigated the rewarding effect of a simple smile during the encoding and retrieval of face-name associations. During encoding, participants viewed smiling or neutral faces, each paired with a name, and during retrieval, only names were presented, and participants retrieved the associated facial expressions. Successful memory activity of face-name associations was identified by comparing remembered vs. forgotten trials during both encoding and retrieval, and the effect of a smile was identified by comparing successful memory trials for smiling vs. neutral faces. The study yielded three main findings. First, behavioral results showed that the retrieval of face-name associations was more accurate and faster for smiling than neutral faces. Second, the orbitofrontal cortex and the hippocampus showed successful encoding and retrieval activations, which were greater for smiling than neutral faces. Third, functional connectivity between the orbitofrontal cortex and the hippocampus during successful encoding and retrieval was stronger for smiling than neutral faces. As a part of the reward system, the orbitofrontal cortex may modulate memory processes of face-name associations mediated by the hippocampus. Interestingly, the effect of a smile during retrieval was found even though only names were presented as retrieval cues, suggesting that the effect was mediated by face imagery. Taken together, the results demonstrate how rewarding social signals from a smiling face can enhance relational memory for face-name associations.     

Learning to associate names and faces. Impaired acquisition on an ecologically relevant memory task by male alcoholics

The performance of a group of detoxified male chronic alcoholics was compared with that of age-matched nonalcoholic controls on a memory task which at face value seemed relevant to daily life--i.e., learning to associate people's names with their faces. The alcoholics not only made more errors while learning the face-name associations than did the controls, but fewer of them were able to reach the learning criterion. However, 1 hour later, the alcoholics were nevertheless able to recognize all of the faces and names used during acquisition. The savings scores for the alcoholics, an index of the relative number of face-name associations retained during the 1-hour interval, did not differ significantly from those of the controls. These results demonstrate that the alcoholics' paired-associate learning deficit on this ecologically relevant task is related to their failure to form associations rather than to deficiencies in recognition memory or perceptual processes.     

Medial temporal contributions to successful face-name learning

The brain mechanisms that enable us to form durable associations between different types of information are not completely understood. Although the hippocampus is widely thought to play a substantial role in forming associations, the role of surrounding cortical regions in the medial temporal lobe, including perirhinal and parahippocampal cortex, is controversial. Using anatomically constrained functional magnetic resonance imaging, we assessed medial temporal contributions to learning arbitrary associations between faces and names. By sorting learning trials based on subsequent performance in associative and item-specific memory tests, we characterized brain activity associated with successful face-name associative learning. We found that right hippocampal activity was greater when corresponding face-name associations were subsequently remembered than when only a face or a name, but not both, were remembered, or when single-item information or associative information was not remembered. Neither perirhinal nor parahippocampal cortex encoding activity differed across these same conditions. Furthermore, right hippocampal activity during successful face-name association learning was strongly correlated with activity in cortical regions involved in multimodal integration, supporting the idea that interactions between the hippocampus and neocortex contribute to associative memory. These results specifically implicate the hippocampus in associative memory formation, in keeping with theoretical formulations in which contributions to across-domain binding differ among brain structures in the medial temporal region.     

Are faces special in Alzheimer's disease? Cognitive conceptualisation, neural correlates, and diagnostic relevance of impaired memory for faces and names

Memory for faces and names has increasingly become a focus of cognitive assessment and research in Alzheimer's disease (AD). This paper reviews evidence from cognitive and clinical neuroscience regarding the question of whether AD is associated with a specific deficit in face recognition, face-name association, and retrieval of semantic information and names. Cognitive approaches conceptualizing face recognition and face-name association have revealed that, compared to other types of visual stimuli, faces are "special" because of their complexity and high intraclass similarity, and because their association with proper names is arbitrary and unique. Neuroimaging has revealed that due to this particular status, face perception requires a complex interplay of highly specialized secondary visual areas located in the occipitotemporal cortex with a widely distributed system of cortical areas subserving further task-dependent processing. Our review of clinical research suggests that AD-related deficits in face recognition are primarily due to mnestic rather than perceptual deficits. Memory for previously studied or famous faces is closely related to mediotemporal and temporocortical brain regions subserving episodic and semantic memory in general, suggesting that AD-related impairments in this domain are due to neural degeneration in these areas. Despite limited specificity due to the apparent absence of a "genuine" domain-specific deficit of face memory in AD, testing memory for faces and names is useful in clinical contexts, as it provides highly sensitive indices of episodic and semantic memory performance. Therefore, clinical assessment of face memory can usefully contribute to early detection of memory deficits in prodromal and initial stages of AD, and represents a basis for further attempts at rehabilitation. Further advantages, such as ecological validity, high task comprehensibility and, in the case of novel face learning, independence from premorbid intelligence level, render measures of face recognition valuable for clinical assessment in early AD.     

Evidence for a specific role of the anterior hippocampal region in successful associative encoding

It has been well established that the hippocampal formation plays a critical role in the formation of memories. However, functional specialization within the hippocampus remains controversial. Using functional magnetic resonance imaging (fMRI) during a face-name associative encoding task, followed by a postscan recognition test for face memory and face-name pair memory, we investigated the roles of anterior and posterior hippocampal regions in successful encoding of associations and items. Whole-brain and region of interest (ROI) analyses revealed that the anterior hippocampal formation showed increased activation for subsequently remembered face-name associations compared with pairs that were forgotten. In contrast, the posterior hippocampal formation showed activation above baseline during attempted encoding of face-name pairs, but no evidence of differential activation based on subsequent memory. Furthermore, exploratory whole-brain analyses revealed that a parahippocampal region, most likely corresponding to perirhinal cortex, showed subsequent memory effects for faces. These data provide evidence for functional specialization within the hippocampal formation based on the associative nature of the stimuli and subsequent memory.     

Human brain potential correlates of repetition priming in face and name recognition

We investigated repetition priming in the recognition of famous people by recording event-related brain potentials (ERPs) and reaction times (RTs). Participants performed speeded two-choice responses depending on whether or not a stimulus showed a famous person. In Experiment 1, a facilitation was found in RTs to famous (but not to unfamiliar) faces when primed by the same face shown in an earlier priming phase of the experiment. In ERPs, an influence of repetition priming was observed neither for the N170 nor for a temporal N250 component which in previous studies had been shown to be sensitive to immediate face repetitions. ERPs to primed unfamiliar faces were more negative over right occipitotemporal areas than those to unprimed faces, but this effect was specific for repetitions of the same image, consistent with recent findings. In contrast, ERPs to primed familiar faces were more positive than those to unprimed faces at parietal sites from 500-600 ms after face onset, and these priming effects were comparable regardless of whether the same or a different image of the celebrity had served as prime. In Experiment 2, similar results were found for name recognition-a facilitation in RTs to primed familiar but not unfamiliar names, and a parietal positivity to primed names around 500-600 ms. ERP repetition effects showed comparable topographies for faces and names, consistent with the idea of a common underlying source. With reference to current models of face recognition, we suggest that these ERP repetition effects for familiar stimuli reflect a change in post-perceptual representations for people, rather than a neural correlate of recognition at a perceptual level.     

“What do you know about Ho Chi Minh?” Italian norms of proper name comprehension

Ninety-eight healthy participants were examined with a new test of Famous Name Comprehension which, in the framework of a serial model of person processing, sequentially assessed Name Recognition (i.e., the ability to classify items as familiar or unfamiliar) and Person Identification (i.e., the ability to provide biographical knowledge of recognised items). Names were presented in a written format. A perfectly equivalent face version of the test allowed a comparison of familiarity and identification of people from name and from face input. Furthermore, the effect of the "age" of the items, i.e. the time elapsed from the presumed first exposure to the stimulus to the time of testing, was also investigated. Normative data are provided. Education was the only significant variable for recognition, while education, age and gender turned out to be significant for identification. Recognition was significantly better with name than with face input, while on identification names and faces did not differ significantly. "Oldest" items were both recognised and identified significantly worse than recent ones. The results of face-name comparison are interpreted in terms of the different opportunities to be exposed to names and faces, the relevance of visuoperceptual attributes linked to faces and the evidence of shared knowledge from different inputs. The relative advantage of recent celebrities supports the semantic characterisation of knowledge of famous people.     

Examining the neural basis of episodic memory: ERP evidence that faces are recollected differently from names

Episodic memory is supported by recollection, the conscious retrieval of contextual information associated with the encoding of a stimulus. Event-Related Potential (ERP) studies of episodic memory have identified a robust neural correlate of recollection—the left parietal old/new effect—that has been widely observed during recognition memory tests. This left parietal old/new effect is believed to provide an index of generic cognitive operations related to recollection; however, it has recently been suggested that the neural correlate of recollection observed when faces are used as retrieval cues has an anterior scalp distribution, raising the possibility that faces are recollected differently from other types of information. To investigate this possibility, we directly compared neural activity associated with remember responses for correctly recognized face and name retrieval cues. Compound face–name stimuli were studied, and at test either a face or a name was presented alone. Participants discriminated studied from unstudied stimuli, and made a remember/familiar decision for stimuli judged ‘old’. Remembering faces was associated with anterior (500–700 ms) and late right frontal old/new effects (700–900 ms), whereas remembering names elicited mid frontal (300–500 ms) and left parietal (500–700 ms) effects. These findings demonstrate that when directly compared, with reference to common episodes, distinct cognitive operations are associated with remembering faces and names. We discuss whether faces can be remembered in the absence of recollection, or whether there may be more than one way of retrieving episodic context.     

Encoding novel face-name associations: a functional MRI study

The process of forming new associations between previously unrelated items of information, such as a name and a face, likely requires the integration of activity within multiple brain regions. The hippocampus and related structures in the medial temporal lobe are thought to be particularly critical in binding together items of information. We studied eight healthy young subjects with functional magnetic resonance imaging (fMRI) during the encoding of novel face-name associations compared to viewing repeated face-name pairs. A consistent pattern of activation was observed in the hippocampus, pulvinar nucleus of the thalamus, fusiform and dorsolateral prefrontal cortices across individual subjects. The location of the activation within the hippocampus was more anterior than previously reported in studies using similar novel vs. repeated paradigms with stimuli that did not specifically require relational processing among unrelated items. These data suggest that the process of forming new face-name associations is supported by a distributed network of brain regions, and provide additional evidence for the essential role of the hippocampus in associative memory processes.     

The modulatory effect of semantic familiarity on the audiovisual integration of face‐name pairs

To recognize individuals, the brain often integrates audiovisual information from familiar or unfamiliar faces, voices, and auditory names. To date, the effects of the semantic familiarity of stimuli on audiovisual integration remain unknown. In this functional magnetic resonance imaging (fMRI) study, we used familiar/unfamiliar facial images, auditory names, and audiovisual face‐name pairs as stimuli to determine the influence of semantic familiarity on audiovisual integration. First, we performed a general linear model analysis using fMRI data and found that audiovisual integration occurred for familiar congruent and unfamiliar face‐name pairs but not for familiar incongruent pairs. Second, we decoded the familiarity categories of the stimuli (familiar vs. unfamiliar) from the fMRI data and calculated the reproducibility indices of the brain patterns that corresponded to familiar and unfamiliar stimuli. The decoding accuracy rate was significantly higher for familiar congruent versus unfamiliar face‐name pairs (83.2%) than for familiar versus unfamiliar faces (63.9%) and for familiar versus unfamiliar names (60.4%). This increase in decoding accuracy was not observed for familiar incongruent versus unfamiliar pairs. Furthermore, compared with the brain patterns associated with facial images or auditory names, the reproducibility index was significantly improved for the brain patterns of familiar congruent face‐name pairs but not those of familiar incongruent or unfamiliar pairs. Our results indicate the modulatory effect that semantic familiarity has on audiovisual integration. Specifically, neural representations were enhanced for familiar congruent face‐name pairs compared with visual‐only faces and auditory‐only names, whereas this enhancement effect was not observed for familiar incongruent or unfamiliar pairs. Hum Brain Mapp 37:4333–4348, 2016. © 2016 Wiley Periodicals, Inc.     

The Pre-exposure Technique: A Novel Method for Enhancing the Effects of Imagery in Face-name Association Learning

We report the effects of stimulus pre-exposure in combination with either non-specific or imagery instructions on face-name learning in 15 memory-impaired subjects. Pre-exposure involved viewing the face alone (for 6 seconds) and making various judgements about the person depicted (e.g. honesty), prior to being shown the face-name pair for learning (for 4 seconds). When the face-name pairs were shown for 4 seconds accompanied by non-specific instructions, pre-exposure to the faces alone led to performance levels as good as when face-name pairs were shown for 10 seconds, and significantly greater performance than when the face-name pairs were shown for just 4 seconds. In line with the results of previous studies, imagery was found significantly to enhance face-name association learning, compared to non-specific instructions. However, performance was increased still further by combining imagery with pre-exposure: Under these conditions, subjects were able to remember almostdouble the number of names on the firstrecall trial than under imagery alone instructions.     

Biographical knowledge: modality-specific or modality-neutral?

A number of patients have been reported who produce more semantic information in response to faces than to names, and vice versa (e.g., Eslinger et al., 1996). It has sometimes been claimed that these patterns are consistent with the hypothesis that faces and names gain access to separate, modality-specific, biographic knowledge systems. Resolving this debate has proved somewhat difficult, however, given limitations of existing data. Not only are there relatively few patients showing these particular patterns of differentiation, but also testing has often not been sufficiently thorough to rule out alternative accounts. In this paper, we present results of two studies investigating biographical knowledge differences in neurological patients and healthy adult controls. The first study focused on two patients who appeared to access more information about famous people in response to their names than to their faces. On superficial analysis, this pattern could be seen to support the notion of modality-specific biographical knowledge systems. However, closer examination revealed that, for both cases, the findings could be explained by a difficulty in face recognition, rather than by assuming separate semantic representations for faces and names. The second study investigated the role of face and name cues in accessing biographical information in younger and older healthy adults. We found that accuracy in retrieval of biographical information was significantly better with name cues for both groups. Results from these studies not only highlight the processes that must be examined in order to demonstrate modality-specific differences conclusively, but also reveal a fundamental bias in retrieval of biographical knowledge that has not been addressed in research of this nature.     

Errorless learning and spaced retrieval: how do these methods fare in healthy and clinical populations?

While errorless learning and spaced retrieval have both proved effective in helping many patients with acquired brain injury (ABI) and dementia learn novel information, it is not clear which of these principles we should apply to target treatment most effectively. To address this issue we conducted a systematic comparison of these principles in three experiments, comparing their effectiveness in healthy controls (N = 60), patients with ABI (N = 30), and patients with dementia (N = 15). Participants were asked to learn face-name associations, and the relative effectiveness of the principles over and above trial-and-error learning was investigated. The results were remarkably consistent across experiments: Both errorless learning and spaced retrieval produced greater accuracy in name recall than did trial-and-error learning, but recall under conditions of spaced retrieval was significantly better than that under errorless learning. We discuss the implications of these findings and suggest that spaced retrieval may be the stronger memory rehabilitation principle when it comes to learning face-name associations in people with mild to moderate memory impairment.     

Differential localization of brain systems subserving memory for names and faces in normal subjects with event-related potentials

Evidence from brain-damaged patients suggests different memory systems for verbal and nonverbal stimuli which also have different neuroanatomical substrates. We explored whether the scalp topographies of event-related potentials (ERPs) might confirm the dissociability of these systems. Unfamiliar faces and names were presented in separate conditions, study blocks alternating with recognition blocks. During recognition the familiarity of each stimulus was rated on a 4-point scale. The amplitudes of the ERPs to the study items were monotonically related in size to the mean subsequent familiarity ratins. Memory-related ERP differences (Dm) were calculated by subtracting ERPs recorded during the study phase to items with low subsequent familiarity ratings from items with high familiarity ratings. The Dm for faces and names showed stimulus-specific scalp topographies between 400 and 800 ms. These findings confirm that memory for names and faces is mediated by at least partially different brain systems.     

Alzheimer's patients engage an alternative network during a memory task

We conducted an event-related functional magnetic resonance imaging experiment to better understand the potentially compensatory alternative brain networks activated by a clinically relevant face-name association task in Alzheimer's disease (AD) patients and matched control subjects. We recruited 17 healthy subjects and 12 AD patients at an early stage of the disease. They underwent functional magnetic resonance imaging scanning in four sessions. Each of the sessions combined a "study" phase and a "test" phase. Face/name pairs were presented in each study phase, and subjects were asked to associate faces with names. In the test phase, a recognition task, faces seen in the study phase were presented each with four different names. The task required selection of appropriate previously associated names from the study phase. Responses were recorded for post hoc classification into those successfully or unsuccessfully encoded. There were significant differences between the groups in accuracy and reaction time. Comparison of correctly versus incorrectly encoded and recognized pairs in the two groups indicated bilateral hippocampal hypoactivation both when encoding and recognizing in the AD group. Moreover, patients showed bilateral hyperactivation of parts of the parietal and frontal lobes. We discuss whether hyperactivation of a frontoparietal network reflects compensatory strategies for failing associative memory in AD patients.     

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.     

Seeing sounds and hearing sights: the influence of prior learning on current perception

It is well known that previous perceptual experiences alter subsequent perception, but the details of the neural underpinnings of this general phenomenon are still sketchy. Here, we ask whether previous experiences with an item (such as seeing a person's face) leads to the alteration of the neural correlates related to processing of the item as such, or whether it creates additional associative connections between such substrates and those activated during prior experience. To address this question, we used magnetoencephalography (MEG) to identify neural changes accompanying subjects' viewing of unfamiliar versus famous faces and hearing the names of unfamiliar versus famous names. We were interested in the nature of the involvement of auditory brain regions in the viewing of faces, and in the involvement of visual regions in the hearing of names. Evoked responses from MEG recordings for the names and faces conditions were localized to auditory and visual cortices, respectively. Unsurprisingly, peak activation strength of evoked responses was larger for famous versus nonfamous names within the superior temporal gyrus (STG), and was similar for famous and nonfamous faces in the occipital cortex. More relevant to the issue of experience on perception, peak activation strength in the STG was larger for viewed famous versus nonfamous faces, and peak activation within the occipital cortex was larger for heard famous versus nonfamous names. Critically, these experience-related responses were present within 150-250 msec of stimulus onset. These findings support the hypothesis that prior experiences may influence processing of faces and names such that perception encompasses more than what is imparted on the senses.     

Neural correlates of reactivation and retrieval-induced distortion

Reactivation of recently acquired information can strengthen memory storage and likely contributes to memory consolidation. Retrieval (generating information about prior events) may improve memory storage because it entails reactivation. Alternatively, retrieval may promote storage of retrieved information, and, if retrieval is inaccurate, subsequent recall could be distorted by the retrieved information. If retrieval modifies memory storage, as hypothesized, neural signals associated with accurate retrieval at that time may be distinct from neural signals associated with the degree of repeated retrieval error evident at some later time. We tested this prediction using a 3-session protocol. During session 1, people learned object-location associations to criterion and completed a cued-recall test in which locations were recalled upon viewing objects. During session 2, an electroencephalogram (EEG) was recorded during cued recall for a subset of the associations. During session 3, cued recall was tested for all associations. Retrieval improved storage, in that recall at session 3 was superior for objects tested in session 2 compared with those not tested. Retrieval-induced distortion was revealed in session 3 for those objects tested in session 2, in that those objects were generally placed closer to locations retrieved at session 2 relative to original study locations. EEG analyses revealed positive potentials (400-700 ms) associated with relatively accurate recall at session 2. Memory updating was reflected in positive potentials after 700 ms that differentially predicted the degree to which recall promoted storage of the session-2-retrieved location. These findings demonstrate unique neurocognitive processing whereby memories are updated with information produced during retrieval.     

Early and late event-related potentials are modulated by infant and adult faces of high and low attractiveness

The processing of infant faces may be somewhat distinct from that of adult faces. Indeed, recent neuroimaging studies have provided evidence of an early, “baby-specific” neural response whereby infant faces are perceived more rapidly than adult faces. Using event-related potentials, the present study aimed to determine whether the preferential response to infant faces is present at both early and late stages of face processing, and to investigate the effects of esthetic appearance on the processing of adult and infant faces by directly manipulating the perceived attractiveness or cuteness within a given face identity. Here, we find evidence for enhanced processing of infant faces, relative to adult faces, at both early (N170, P2) and late (LPC) stages of face processing. We also find that the esthetic appearance of both infant and adult faces modulates early neural responses, with enhanced responses to less attractive/cute faces as compared to more attractive/cute faces. Overall, our results provide additional evidence for a preferential response to infant faces at early stages of processing, and provide new evidence that this preferential response occurs at later stages of face processing as well, independent of the esthetic quality of the face or observer sex.     

Famous people recognition through personal name: a normative study

In this normative study, we investigated famous people recognition through personal name, using as stimuli the names of the same 40 Italian famous persons whose faces and voices had been utilized for the normative study of the Famous People Recognition Battery. For each famous people, we assessed name familiarity, person identification (when the name had been considered as familiar), and false alarms. The investigation was carried out on 143 normal subjects who varied in age and education. Name familiarity and semantic scores were affected by educational level, whereas age influenced false alarms. A comparison between results obtained with names in this research and with faces and voices of the same famous people in our previous study showed that familiarity scores were higher for personal names than those for faces and voices, which obtained the worst scores. Person identification scores were not significantly different from names and from faces, but both these scores were significantly higher than the semantic scores obtained by voices. Taken together, these results are inconsistent with the influential interactive activation and competition model of person recognition.