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How does the brain discriminate familiar and unfamiliar faces?: a PET study of face categorical perception.

Where and how does the brain discriminate familiar and unfamiliar faces? This question has not been answered yet by neuroimaging studies partly because different tasks were performed on familiar and unfamiliar faces, or because familiar faces were associated with semantic and lexical information. Here eight subjects were trained during 3 days with a set of 30 faces. The familiarized faces were morphed with unfamiliar faces. Presented with continua of unfamiliar and familiar faces in a pilot experiment, a group of eight subjects presented a categorical perception of face familiarity: there was a sharp boundary in percentage of familiarity decisions between 40% and 60% faces. In the main experiment, subjects were scanned (PET) on the fourth day (after 3 days of training) in six conditions, all requiring a sex classification task. Completely novel faces (0%) were presented in Condition 1 and familiar faces (100%) in Condition 6, while faces of steps of 20% in the continuum of familiarity were presented in Conditions 2 to 5 (20% to 80%). A principal component analysis (PCA) indicated that most variations in neural responses were related to the dissociation between faces perceived as familiar (60% to 100%) and faces perceived as unfamiliar (0 to 40%). Subtraction analyses did not disclose any increase of activation for faces perceived as familiar while there were large relative increases for faces perceived as unfamiliar in several regions of the right occipito-temporal visual pathway. These changes were all categorical and were observed mainly in the right middle occipital gyrus, the right posterior fusiform gyrus, and the right inferotemporal cortex. These results show that (1) the discrimination between familiar and unfamiliar faces is related to relative increases in the right ventral pathway to unfamiliar/novel faces; (2) familiar and unfamiliar faces are discriminated in an all-or-none fashion rather than proportionally to their resemblance to stored representations; and (3) categorical perception of faces is associated with abrupt changes of brain activity in the regions that discriminate the two extremes of the multidimensional continuum.

Adult↗

Neural substrates for functionally discriminating self-face from personally familiar faces.

Understanding the neurobiological substrates of self-recognition yields important insight into socially and clinically critical cognitive functions such as theory of mind. Experimental evidence suggests that right frontal and parietal lobes preferentially process self-referent information. Recognition of one's own face is an important parameter of self-recognition, but well-controlled experimental data on the brain substrates of self-face recognition is limited. The goal of this study was to characterize the activation specific to self-face in comparison with control conditions of two levels of familiarity: unknown unfamiliar face and the more stringent control of a personally familiar face. We studied 12 healthy volunteers who made "unknown," "familiar," and "self" judgments about photographs of three types of faces: six different novel faces, a personally familiar face (participant's fraternity brother), and their own face during an event-related functional MRI (fMRI) experiment. Contrasting unknown faces with baseline showed activation of the inferior occipital lobe, which supports previous findings suggesting the presence of a generalized face-processing area within the inferior occipital-temporal region. Activation in response to a familiar face, when contrasted with an unknown face, invoked insula, middle temporal, inferior parietal, and medial frontal lobe activation, which is consistent with an existing hypothesis suggesting familiar face recognition taps neural substrates that are different from those involved in general facial processing. Brain response to self-face, when contrasted with familiar face, revealed activation in the right superior frontal gyrus, medial frontal and inferior parietal lobes, and left middle temporal gyrus. The contrast familiar vs. self produced activation only in the anterior cingulate gyrus. Our results support the existence of a bilateral network for both perceptual and executive aspects of self-face processing that cannot be accounted for by a simple hemispheric dominance model. This network is similar to those implicated in social cognition, mirror neuron matching, and face-name matching. Our findings also show that some regions of the medial frontal and parietal lobes are specifically activated by familiar faces but not unknown or self-faces, indicating that these regions may serve as markers of face familiarity and that the differences between activation associated with self-face recognition and familiar face recognition are subtle and appear to be localized to lateral frontal, parietal, and temporal regions.

Brain↗

The neural basis of the butcher-on-the-bus phenomenon: when a face seems familiar but is not remembered.

A common distinction in contemporary research on episodic memory is between familiarity, an unsubstantiated impression that an event was experienced previously, and recollection, remembering some information plus the spatiotemporal context of the episode in which it was acquired. The epitome of pure familiarity--the butcher-on-the-bus phenomenon--occurs when one believes that a person is familiar (often upon seeing their face in an atypical context) while failing to recall any information about that person whatsoever. Prior research on familiarity and recollection has relied on verbal material. Whereas word meanings and pronunciations are well learned in advance, here we produced pure familiarity and recollection using photographs of faces never seen before the experiment. When participants recognized a face, recollection was inferred if they also remembered either the occupation associated with that face earlier in the experiment or any other episodic detail. Pure familiarity was inferred when recognition occurred in the absence of any such contextual retrieval. Analyses of brain potentials recorded during initial encoding showed that right-sided neural activity predicted subsequent face familiarity, whereas bilateral potentials predicted subsequent face recollection. Results during memory testing were inconsistent with the popular idea that familiarity is generically indexed by reduced frontal N400-like potentials. Instead, both memory experiences were associated with bilateral, parietal-maximum brain potentials, although with smaller amplitudes and for a shorter duration for familiarity. These similarities between electrophysiological correlates of pure familiarity and recollection suggest that familiarity with faces may arise by virtue of a subset of the neural processing responsible for recollection.

Adolescent↗

Odor discrimination and recognition memory as a function of familiarization.

The role of olfactory familiarization in short-term recognition of odors was investigated. Subjects were asked to make qualitative similarity judgments regarding either identical or dissimilar odors delivered in pairs. Except for control groups, subjects got familiarized with either the first (target) or the second (distractor) or both odors from a pair. Groups also differed according to the number of familiarization sessions--one, two, or three--taking place prior to the discrimination judgments. There was no significant influence of familiarization on correct recognition scores for pairs of identical odors. The most salient finding was a marked decrease of false alarms as a function of the number of familiarization sessions, which evidenced a positive effect of familiarization on discrimination for pairs of dissimilar odors. These judgments were not dependent on an intensity criterion. False alarms did not vary according to whether subjects had been familiarized with the target or the distractor or both odors from a pair. A positive correlation found between discrimination performances and the number of odors correctly remembered as being presented during familiarization suggested that familiarization resulted in long-term storing of memory traces for familiarized odors. Since familiarization was effective despite conditions unfavorable to the use of semantic encoding, the results argue in favor of a predominantly perceptual encoding of odors in the investigated task.

Adult↗

Neural response to the visual familiarity of faces.

Recognizing personally familiar faces is the result of a spatially distributed process that involves visual perceptual areas and areas that play a role in other cognitive and social functions, such as the anterior paracingulate cortex, the precuneus and the amygdala [M.I. Gobbini, E. Leibenluft, N. Santiago, J.V. Haxby, Social and emotional attachment in the neural representation of faces, Neuroimage 22 (2004) 1628-1635; M.I. Gobbini, J.V. Haxby, Neural systems for recognition of familiar faces, Neuropsychologia, in press; E. Leibenluft, M.I. Gobbini, T. Harrison, J.V. Haxby, Mothers' neural activation in response to pictures of their, and other, children, Biol. Psychiatry 56 (2004) 225-232]. In order to isolate the role of visual familiarity in face recognition, we used fMRI to measure the response to faces characterized by experimentally induced visual familiarity that carried no biographical information or emotional content. The fMRI results showed a stronger response in the precuneus to the visually familiar faces consistent with studies that implicate this region in the retrieval of information from long-term memory and imagery. Moreover, this finding supports the hypothesis of a key role for the precuneus in the acquisition of familiarity with faces [H. Kosaka, M. Omori, T. Iidaka, T. Murata, T. Shimoyama, T. Okada, N. Sadato, Y. Yonekura, Y. Wada, Neural substrates participating in acquisition of facial familiarity: an fMRI study, Neuroimage 20 (2003) 1734-1742]. By contrast, the visually familiar faces evoked a weaker response in the fusiform gyrus, which may reflect the development of a sparser encoding or a reduced attentional load when processing stimuli that are familiar. The visually familiar faces also evoked a weaker response in the amygdala, supporting the proposed role of this structure in mediating the guarded attitude when meeting someone new.

Adult↗

Evidence for several components of word familiarity.

Familiarity with a word can be divided into two main components: familiarity with the form of the word (due to both its lexicality and its specific form) and familiarity with its meaning. In this study, ratings of familiarity were compared for words whose meaning was unknown to participants (UM words), for words of known meaning (KM words), and for unknown words (U words). Linguistic and experiential frequencies were equivalent. Rated familiarity was lower for UM than KM words and even lower for U words. Next, we built pseudowords from these stimuli by changing one letter and submitted them to two familiarity rating tasks that differed in the nature of the additional stimuli: either only nonwords or nonwords plus words. It was assumed that familiarity ratings would be lower for pseudowords built from UM words than for pseudowords built from KM words. The data were consistent with this assumption, and ratings depended on the initial categories of stimuli. These results support the view that usual word familiarity has two components, familiarity with form and familiarity with meaning, and a double source, processing of word form and processing of word meaning. The full set of these materials and norms may be downloaded from www.psychonomic.org/archive.

Cognition↗

Familiarity Bias and Belief Reversal in Relative Likelihood Judgment.

People are often called on to make an assessment of the relative likelihood of events (e.g., which of two investments is more likely to outperform the market?) and their complements (which of the two investments is more likely to perform no better than the market?). Probability theory assumes that belief orderings over events and their complements should mirror each other (i.e., P(A) >/= P(B) iff P (not-A) </= P(not-B)). This principle is violated in several surveys in which we asked people to assess the relative likelihood of familiar versus unfamiliar events. In particular, respondents are biased to view more familiar events (and their complements) as more likely than less familiar events (and their complements). Similarly, we observe that subjects are biased to view less familiar events (and their complements) as less likely than more familiar events (and their complements). Further studies demonstrate that the familiarity bias is less pronounced among subjects who are asked to judge the probability of each event rather than which event is more likely. Moreover, a greater proportion of subjects rate the more familiar event as more likely than assign a higher probability to that event. These patterns can be construed as belief reversals, analogous to the preference reversal phenomenon in decision making. The data are consistent with a contingent weighting model in which the process of judging relative likelihood biases attention toward evidence supporting the target hypothesis (and away from evidence supporting its complement). Because it is easier to recruit evidence supporting familiar events than unfamiliar events, this skewed attention causes both familiar events and their complements to be judged more likely, on average, than unfamiliar events and their complements. Copyright 2000 Academic Press.

Journal Article↗

Cue familiarity is represented in monkey medial prefrontal cortex during visuomotor association learning.

To examine functional roles of the medial prefrontal cortex (mPFC) in visuomotor association learning, neuronal activity in the mPFC of a behaving monkey was recorded during this learning. The monkey was presented a cueing visual stimulus, and required to push, pull or turn a manipulator according to the cue following a delay period. Under the control condition, three cues (circle, triangle and square) instructed the monkey to the three responses in a block of trials. After 2 months of training the animal was familiar with these cue-response associations. Under the learning condition, two of the three familiar cues and one novel cue were presented in a block. The monkey initially did not know what the novel cue instructed at first and learned a new cue-response association by trial and error. Neurons in the mPFC showed marked responses to cue presentation, and cue responses changed depending on whether cues were familiar or novel. A group of mPFC neurons responded to novel cues, but not to familiar cues. Another group of neurons responded to familiar cues, but not to novel cues. In a subgroup of these familiar cue-selective neurons, cue response was increased under the learning condition compared to the control condition. These results suggest that mPFC neurons differentiate between familiar and novel instructions, and that the neurons responsive to familiar stimuli enhance their modulations when both familiar and novel instructions have to be processed during task performance.

Action Potentials↗

Electrophysiological dissociation of the neural correlates of recollection and familiarity.

Event-related potentials (ERPs) were employed to investigate electrophysiological correlates of recognition memory in a task that allowed segregation of test items according to whether they were recollected (operationalized by introspective report) or, if recollection failed, their level of familiarity (operationalized by recognition confidence). The amplitude of a negative-going ERP deflection that onsets around 300 ms post-stimulus varied inversely with familiarity strength. This effect was maximal over the left frontal scalp. It did not differ between the ERPs elicited by highly familiar versus recollected items, indicating that the recollection is not merely a consequence of strong familiarity. By contrast, a later positive deflection (onset ca. 500 ms post-stimulus) was enhanced in ERPs elicited by recollected relative to highly familiar items. This effect was maximal over the left posterior scalp and was insensitive to familiarity, as indicated by its absence in the contrast between items judged highly familiar versus highly unfamiliar. The findings constitute a double dissociation between the neural correlates of recollection and familiarity. Together with the results of a parallel functional magnetic resonance imaging study (A.P. Yonelinas et al., J. Neurosci. (2005), 25, 3002-3008), they indicate that recollection and familiarity rely on qualitatively distinct neural systems and strongly support dual-process models of recognition memory.

Adolescent↗

The effects of inversion and eye displacements of familiar and unknown faces on early and late-stage ERPs.

OBJECTIVES: The objective of this study is to examine whether configural alterations of faces affect early or late processing stages as a function of their familiarity and their level of representation in memory. We then sought to verify whether the structural encoding stage is susceptible to top-down influences. METHODS: Electrophysiologic and behavioral studies were undertaken, during which unknown and familiar faces were presented upright or upside-down with or without feature alterations. The subjects were asked to determine whether the faces were familiar or not. RESULTS: N170 and N360 amplitudes were larger for familiar faces as well as altered ones. A higher degree of familiarity decreased reaction times (RTs) and N360 latencies, but increased N170 latencies, whereas face alterations increased RTs and latencies of both components examined. However, familiarity interacted with altered face configurations only for RTs and the N170. SIGNIFICANCE: In the perceptual stage, familiar faces seem to develop a more elaborate type of processing because of top-down influences linked to the robust nature of their representations in memory. The more elaborate type of processing for familiar faces has advantageous consequences for the following steps of information processing, by facilitating access to structural representations in memory (N360) as well as the final step reflected by RTs. The fact that configural alterations cause different effects for familiar as opposed to unfamiliar faces indicate that these stimuli are processed in a qualitatively different manner and solicit different representations in memory.

Adult↗

Effects of visual familiarity for words on interhemispheric cooperation for lexical processing.

The purpose of this study was to examine the effects of visual familiarity of words on interhemispheric lexical processing. Words and pseudowords were tachistoscopically presented in a left, a right, or bilateral visual fields. Two types of words, Katakana-familiar-type and Hiragana-familiar-type, were used as the word stimuli. The former refers to the words which are more frequently written with Katakana script, and the latter refers to the words which are written predominantly in Hiragana script. Two conditions for the words were set up in terms of visual familiarity for a word. In visually familiar condition, words were presented in familiar script form and in visually unfamiliar condition, words were presented in less familiar script form. The 32 right-handed Japanese students were asked to make a lexical decision. Results showed that a bilateral gain, which indicated that the performance in the bilateral visual fields was superior to that in the unilateral visual field, was obtained only in the visually familiar condition, not in the visually unfamiliar condition. These results suggested that the visual familiarity for a word had an influence on the interhemispheric lexical processing.

Adult↗

Selection of odorants for memory tests on the basis of familiarity, perceived complexity, pleasantness, similarity and identification.

In a procedure for the selection of two equivalent sets of familiar and two equivalent sets of unfamiliar odours for use in odour memory studies, 24 naïve subjects were first asked to rate the familiarity, perceived complexity and pleasantness of 54 a priori unfamiliar odours and 57 a priori familiar odours and to identify the latter. After selection of the 40 most familiar and the 40 least familiar odours, the subjects sorted each of these two sets into groups of similar odours. Their results were analysed by multidimensional scaling and cluster analysis and each set was divided into two recognition sets that had the same degree of similarity between target and distractor odours and that had similar values of familiarity, pleasantness, perceived complexity (familiar and unfamiliar sets) and identifiability (familiar sets). Finally, recognition tasks were performed in order to check the equivalence in memory performance of both the two familiar and the two unfamiliar recognition sets.

Adult↗

Crew familiarity: operational experience, non-technical performance, and error management.

INTRODUCTION: Crew familiarity, in terms of having recent operational experience together as a crew, is seen as an important safety-related variable. However, little evidence exists to unpack the underlying processes with respect to familiarity. This study investigated the relationships between crew familiarity, non-technical performance, and error management. METHOD: Data were collected during normal line operations at a commercial airline by observers using a methodology based on the Line Operations Safety Audit (LOSA). A total of 154 flights were analyzed, 31% of which were operated by an unfamiliar crew, with 69% operated by a familiar crew. RESULTS: The rate of error occurrence was found to be higher for unfamiliar crews, and these crews were found to make different types of errors when compared with familiar crews. However, with respect to the management of error events, no significant difference was found between unfamiliar and familiar crews. No significant effect of crew familiarity was found with respect to crews' non-technical performance. However, strong correlations were found between crews' non-technical performance and the management of errors. DISCUSSION: The findings indicate that crew familiarity, in terms of whether a crew has flown together recently or not, has little operational significance with respect to the management of error events during normal line operations. Accordingly, the suggestion that unfamiliar crews operate at a higher level of safety-related risk was not supported. Non-technical performance appears to be a stronger driver of effective error management than crew familiarity, and is highlighted as a focus for further investigation and intervention.

Accidents, Aviation↗

Positron-emission tomography of brain regions activated by recognition of familiar music.

BACKGROUND AND PURPOSE: We can easily recognize familiar music by listening to only one or 2 of its opening bars, but the brain regions that participate in this cognitive processing remain undetermined. We used positron-emission tomography (PET) to study changes in regional cerebral blood flow (rCBF) that occur during listening to familiar music. METHODS: We used a PET subtraction technique to elucidate the brain regions associated with the recognition of familiar melodies such as well-known nursery tunes. Nonmusicians performed 2 kinds of musical tasks: judging the familiarity of musical pieces (familiarity task) and detecting deliberately altered notes in the pieces (alteration-detecting task). RESULTS: During the familiarity task, bilateral anterior portions of bilateral temporal lobes, superior temporal regions, and parahippocampal gyri were activated. The alteration-detecting task bilaterally activated regions in the precunei, superior/inferior parietal lobules, and lateral surface of frontal lobes, which seemed to show a correlation with the analysis of music. CONCLUSION: We hypothesize that during the familiarity task, activated brain regions participate in retrieval from long-term memory and verbal and emotional processing of familiar melodies. Our results reinforced the hypothesis reported in the literature as a result of group and case studies, that temporal lobe regions participate in the recognition of familiar melodies.

Adult↗

Medial temporal and prefrontal contributions to working memory tasks with novel and familiar stimuli.

Lesions of parahippocampal structures impair performance of delayed matching tasks in nonhuman primates, suggesting a role for these structures in the maintenance of items in working memory and short-term stimulus matching. However, most human functional imaging studies have not shown medial temporal activation during working memory tasks and have primarily focused on functional magnetic resonance imaging (fMRI) signal intensity changes in the prefrontal and posterior parietal cortex. The goal of this study was to test the hypothesis that the difference between the human and nonhuman primate data results from the use of highly familiar stimuli in human working memory studies and trial-unique stimuli in nonhuman primate studies. We used fMRI to examine prefrontal and temporal lobe activation during performance of a working memory (two-back) task, using blocks of novel and highly familiar complex pictures. Performance of the working memory task with novel complex pictures resulted in greater signal change within medial temporal lobe structures than performance of the task with familiar complex pictures. In contrast, the working memory task with highly familiar stimuli resulted in greater prefrontal activation. These results are consistent without hypothesis that the medial temporal lobe is recruited for the short-term maintenance of information that has no prior representation in the brain, whereas the prefrontal cortex is important for monitoring familiar stimuli that have a high degree of interference. A second set of tasks examined stimulus matching. Subjects performed a target-matching task, during which they identified a single target presented in blocks of novel or familiar stimuli. The results provide evidence of hippocampal and parahippocampal recruitment in the target-matching task with familiar stimuli. These results are consistent with prior animal studies and suggest that prefrontal regions may be important for the monitoring and matching of familiar stimuli which have a high potential for interference, whereas medial temporal regions may become proportionally more important for matching and maintenance of novel stimuli.

Adult↗

Environmental familiarization in rats: differential effects of acute and chronic nicotine.

If an environment is familiar, rats will interact more with a novel object than if the environment is unfamiliar. In two experiments we used this behavioral tendency to assess the effects of nicotine on environmental familiarization (i.e., an elevated platform). As expected, rats given 2 min of exposure to the platform on 2 consecutive days (familiarization phase) interacted more with a novel object in a subsequent test than rats that had not experienced the platform until the test day. During the familiarization phase acute pretreatment with nicotine (0.6 and 1.8 mg/kg, subcutaneous) 10 min before platform exposure interfered with familiarization processes, as measured by object interaction on the drug-free test day. Behavioral measures of activity (e.g., turning and midline crosses) eliminated an account based on nicotine-induced motor impairment. Furthermore, this effect of acute nicotine on familiarization was not due to nonspecific effects of nicotine. Controls that received equivalent nicotine exposure temporally separated from platform exposure interacted more with the novel object than similarly treated controls that were unfamiliar with the platform on the test day. Interestingly, rats treated once daily with 0.6 mg/kg nicotine for 14 days before the familiarization phase (chronic condition) did not show a decrease in environmental familiarity. This dissociation extends a growing literature finding that the behavioral and neurobiological effects of nicotine differ, in part, after acute and chronic exposure. Indeed, acute nicotine (0. 2, 0.6, and 1.2 mg/kg) in the present report consistently decreased the amount of time spent with one paw on the edge of the platform; chronic nicotine did not affect this behavior.

Acetylcholine↗

The influence of topic and listener familiarity on aphasic discourse.

This study investigated the effects of listener and topic familiarity on verbal output. A total of 32 subjects were included: 5 Broca's, 7 conduction, and 10 anomic aphasics; and 10 normal controls. Subjects performed story retell and procedural discourse tasks containing familiar and unfamiliar topics. Tasks were completed with a familiar listener (spouse) and an unfamiliar listener (examiner). Results indicated that topic familiarity significantly influenced verbal output, however specific findings were dependent on task. In procedural discourse, the amount of verbal output (number of T-units) was significantly greater on familiar topics. In contrast, the complexity (number of words and clauses per T-unit) was significantly greater on unfamiliar topics. On story retell, verbal output (number of T-units) was also greater on familiar topics. However, grammatic complexity did not increase with unfamiliar topics. Words per T-unit remained higher on familiar topics. The variable of listener familiarity was not found to be significant.

Aged↗

Ethanol familiarity and naltrexone treatment affect ethanol responses in rats.

In the present study, the effects of ethanol familiarity on the ability of naltrexone to alter ethanol palatability and consumption were examined. One group of rats was allowed continuous access to 10% vol/vol ethanol and water for 3 weeks. A second group received only water. At the end of this time, the groups were further subdivided and injected with either 3mg/kg naltrexone or saline (total of four groups; n=11-13 per group) before ethanol taste reactivity tests with 10% vol/vol ethanol and ethanol consumption tests. Results showed that naltrexone effectively decreased ingestive responding and increased aversive responding. Further, rats familiar with alcohol made more ingestive responses to 10% vol/vol ethanol. A significant interaction of drug treatment and familiarity was found in the data for aversive responses: naltrexone treatment produced more aversive responses in ethanol-familiar rats, whereas saline treatment resulted in fewer aversive responses in rats familiar with ethanol. Naltrexone treatment clearly reduced consumption of 10% vol/vol ethanol, although its effects were attenuated somewhat by ethanol familiarity. The present data indicate that both alcohol familiarity and naltrexone treatment affect ethanol reactivity and ethanol consumption in outbred rats. The interaction of naltrexone treatment and ethanol familiarity only for aversive reactivity and the lack of such an interaction for the consumption measures suggests that the mechanisms underlying ethanol reactivity and ethanol consumption may be dissociable at the neural level.

Alcohol Deterrents↗