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Dissociable neural correlates for familiarity and recollection during the encoding and retrieval of pictures.

Results from behavioral studies have supported the idea that recognition memory can be supported by at least two different processes, recollection and familiarity. However, it remains unclear whether these two forms of memory reflect neurally distinct processes. Furthermore, it is unclear whether recollection and familiarity can be best conceived as differing primarily in terms of retrieval processing, or whether they additionally differ at encoding. To address these issues, we used event-related brain potentials (ERPs) to monitor neural correlates of familiarity and recollection at both encoding and retrieval. Participants studied pictures of objects in two types of study blocks and subsequently made remember-know and source memory judgments during retrieval. Results showed that, during encoding, neural correlates of subsequent familiarity and recollection onsetted in parallel, but exhibited differences in scalp topography and time course. Subsequent familiarity-based recognition was associated with a left-lateralized enhanced positivity and observed at anterior scalp sites from 300 to 450 ms, whereas subsequent recollection was associated with a topographically distinct right-lateralized positivity at anterior scalp sites from 300 to 450 ms and bilateral activity from 450 to 600 ms. During retrieval, neural correlates of familiarity emerged earlier than correlates of recollection. Familiarity was associated with an enhanced positivity at frontopolar scalp sites from 150 to 450 ms, whereas recollection was associated with positive ERP modulations over bilateral frontal (300-600 ms) and parietal (450-800 ms) sites. These results demonstrate that familiarity and recollection reflect the outcome of neurally distinct memory processes at both encoding and retrieval.

Adolescent↗

Familiarity enhances invariance of face representations in human ventral visual cortex: fMRI evidence.

Face recognition across different viewing conditions is strongly improved by familiarity. In the present study, we tested the hypothesis that the neural basis of this effect is a less view-dependent representation of familiar faces in ventral visual cortex by assessing priming-related fMRI repetition effects. 15 healthy volunteers made male/female judgements on familiar (famous) and unfamiliar (novel) faces preceded by the same image, a different image of the same face, or another (unprimed) face. Reaction times revealed priming by same and different images independent of familiarity and more pronounced for same than different images. In the imaging data, a main effect of prime condition was found in bilateral fusiform and orbitofrontal regions. A right anterior fusiform region expressed stronger response decreases to repetition of familiar than unfamiliar faces. Bilateral mid-fusiform areas showed stronger response decreases to repetition of same than different images. A regions-of-interest analysis focussing specifically on face responsive regions suggested differences in the degree of image dependency across fusiform cortex. Collapsing across familiarity, there was greater image dependency of repetition effects in right than left anterior fusiform, replicating previous imaging findings obtained with common objects. For familiar faces alone, there was greater generalisation of repetition effects over different images in anterior than middle fusiform. This suggests a role of anterior fusiform cortex in coding image-independent representations of familiar faces.

Adult↗

Impaired discrimination of familiar from unfamiliar faces.

We report investigations of the face processing abilities of J.T., a man who had suffered a right hemisphere stroke. J.T. showed a marked problem in discriminating between familiar and unfamiliar faces, with no corresponding problem in discriminating familiar from unfamiliar names. The problem with faces was still found 2 years after the stroke, but had resolved at long-term follow-up (9 years post stroke). When given unlimited time to respond, J.T. did not show any problem in recognising familiar faces, but tended to think that he recognised unfamiliar faces. When under time pressure, however, J.T. also failed to recognise a number of familiar faces which he could readily identify when the time pressure was removed. J.T.'s ability to remember a face and to think of other people who might be similar in appearance was affected by whether or not the face seemed familiar or unfamiliar to him. Hence, whatever underlay the spurious sense of familiarity was sufficient to produce real differences between the way in which genuinely unfamiliar and spuriously familiar faces were seen, leading us to suggest that his impaired discrimination of unfamiliar from familiar faces reflected a malfunction of face recognition units.

Aged↗

Self-organization of an artificial neural network subjected to attention shift impairments and familiarity preference, characteristics studied in autism.

Autism is a developmental disorder with possibly multiple pathophysiologies. It has been theorized that cortical feature maps in individuals with autism are inadequate for forming abstract codes and representations. Cortical feature maps make it possible to classify stimuli, such as phonemes of speech, disregarding incidental detail. Hierarchies of such maps are instrumental in creating abstract codes and representations of objects and events. Self-Organizing Maps (SOMs) are artificial neural networks that offer insights into the development of cortical feature maps. Attentional impairment is prevalent in autism, but whether it is caused by attention-shift impairment or strong familiarity preference or negative response to novelty is a matter of debate. We model attention shift during self-organization by presenting a SOM with stimuli from two sources in four different modes, namely, novelty seeking (regarded as normal learning), attention-shift impairment (shifts are made with a low probability), familiarity preference (shifts made with a lower probability to the source that is the less familiar to the SOM of the two sources), and familiarity preference in conjunction with attention-shift impairment. The resulting feature maps from learning with novelty seeking and with attention-shift impairment are much the same except that learning with attention-shift impairment often yields maps with a somewhat better discrimination capacity than learning with novelty seeking. In contrast, the resulting maps from learning with strong familiarity preference are adapted to one of the sources at the expense of the other, and if one of the sources has a set of stimuli with smaller variability, the resulting maps are adapted to stimuli from that source. When familiarity preference is less pronounced, the resulting maps may become normal or fully restricted to one of the sources, and in that case, always the source with smaller variability if such a source is present. Such learning, in a system with many different maps, will result in very uneven capacities. Learning with familiarity preference in conjunction with attention-shift impairment surprisingly has higher probability for the development of normal maps than learning with familiarity preference alone.

Attention↗

Orthography and familiarity effects in word processing.

Both orthographic regularity and visual familiarity have been implicated as contributors to the efficiency of processing visually presented words. Our studies sought to determine which of the internal codes representing words in the nervous system are facilitated by these two variables. To do this, sets of letter strings in which orthography and familiarity were factorially combined were used as the basis for physical, phonetic, semantic, and lexical judgments. The data indicated consistent effects of orthography on the activation of all codes. These effects were seen in same-different matching and in judgments of stimulus orientation, which are based on visual codes; in judgments of pronounceability based on phonetic codes; in judgments of meaningfulness based on semantic codes; and in lexical decisions, which are based on phonetic and semantic codes together. Familiarity, on the other hand, had a clear influence on the activation of semantic codes and to a lesser extent affected phonetic codes. Despite previous positive results found in matching letter strings, however, no influence of familiarity occurred in judgments based on visual codes once evidence for criterion shifting was eliminated. Our negative results included direct tests of facilitation in matching acronyms (e.g., FBI) and in matching both regular and irregular strings familiarized by specific training. It now appears that earlier findings of visual familiarity effects may be attributed to response biases resulting from the activation of higher level codes sensitive to familiarity, and to the use of small sets of training stimuli that allowed subjects to induce orthographic-like rules. The results obtained so far with our methods seem to reconcile an inconsistent literature by showing that speeded decisions based on visual codes are most strongly influenced by rule-governed processing mechanisms sensitive to orthographic structure, whereas decisions based on phonetic and semantic codes are affected about equally by rule-governed mechanisms and by stimulus-specific mechanisms sensitive to familiarity. This conclusion may lead to changes in notions of how effective various kinds of visual training are likely to be at different stages in the acquisition of reading skill.

Discrimination Learning↗

Effect of referent object familiarity on verbal learning in the sighted and the blind.

In a series of paired-associate tasks we investigate why some highly concrete nouns are easier to remember than other highly concrete nouns, even when such word attributes as imagery value are held constant. In Experiment 1 both the congenitally blind and the sighted remembered nouns with referents highly familiar to the blind better than nouns with referents of low familiarity to the blind. Although this effect was anticipated for the blind, it was unexpected for the sighted because the referents of low familiarity to the blind have been visually experienced by the sighted and are as easy for the sighted to image as the referents highly familiar to the blind. Experiments 2 through 5 explore why the extent to which the blind are familiar with an object should predict verbal learning for the sighted. As it turned out, referents that were familiar to the blind were also familiar to the sighted. After ruling out various alternative explanations we were able to conclude that it is the extent of perceptual experience with a noun's referent, irrespective of the modality through which the experience is acquired, that determines ease of verbal learning. Any theory that accounts for the concrete-noun effect must also be able to account for the effect of referent familiarity, and our results are discussed within this context.

Adult↗

The warm glow heuristic: when liking leads to familiarity.

Five studies demonstrate that the positive valence of a stimulus increases its perceived familiarity, even in the absence of prior exposure. For example, beautiful faces feel familiar. Two explanations for this effect stand out: (a). Stimulus prototypicality leads both to positivity and familiarity, and (b). positive affect is used to infer familiarity in a heuristic fashion. Studies 1 and 2 show that attractive faces feel more familiar than average ones and that prototypicality accounts for only part of this effect. In Study 3, the rated attractiveness of average faces was manipulated by contrast, and their perceived familiarity changed accordingly, although their inherent prototypicaliry remained the same. In Study 4, positive words felt more familiar to participants than neutral and negative words. Study 5 shows that the effect is strongest when recognition is difficult. The author concludes that both prototypicality and a warm glow heuristic are responsible for the "good-is-familiar" phenomenon.

Adolescent↗

A spondee list for determining speech reception threshold without prior familiarization.

The purpose of this investigation was to select a list of spondees from the CID W-1 spondee word list that eliminates the need for familiarization but produces spondee thresholds equivalent to those obtained with familiarization. Forty-eight subjects with normal hearing responded to familiarized and unfamiliarized spondee words at their familiarized spondee threshold levels. Spondee words that were correctly identified most often without prior familiarization or whose correct response rates were least altered by familiarization were selected for the final list. Seventeen words were selected from the criteria of the present study; two of these words were excluded from the final list since they did not fall within the recommended 4-dB range. The 15 remaining spondee words without familiarization produced spondee thresholds equivalent to the entire CID W-1 list with familiarization in a direct comparison of the two lists in 20 subjects with normal hearing.

Adolescent↗

Exploring levels of face familiarity by using an indirect face-matching measure.

An experiment is reported in which participants matched complete images of unfamiliar, moderately familiar, and highly familiar faces with simultaneously presented images of internal and external features. Participants had to decide if the two images depicted same or different individuals. Matches to internal features were made faster to highly familiar faces than both to moderately familiar and to unfamiliar faces, and matches to moderately familiar faces were made faster than to unfamiliar faces. For external feature matches, this advantage was only found for "different" decision matches to highly familiar faces compared to unfamiliar faces. The results indicate that the differences in familiar and unfamiliar face processing are not the result of all-or-none effects, but seem to have a graded impact on matching performance. These findings extend the earlier work of Young et al (1985 Perception 14 737-746), and we discuss the possibility of using the matching task as an indirect measure of face familiarity.

Adolescent↗

The importance of stable schooling: do familiar sticklebacks stick together?

Preferences for rejoining shoals composed of familiar individuals have recently been documented in a variety of small, shallow-water fish species. Such preferences are assumed to be adaptive, since familiar groups have improved anti-predator defences and more stable dominance hierarchies. However, the design of these studies may have created conditions that elevate preferences for familiar individuals. Furthermore, in natural habitats, where significant opportunities for inter-shoal transfer may exist, it is unclear whether shoals stay together long enough for such preferences to develop. Here we present the results of a laboratory study examining whether prior familiarity influences the subsequent shoal composition of sticklebacks (Gasterosteus aculeatus) allowed to re-assort freely in a large arena tank. We show that fish from different familiarity groups associate with familiar conspecifics significantly more than predicted by a model of random assortment, suggesting that even when there is ample opportunity for inter-group transfer, shoal composition can remain stable. We discuss the phenomena that may lead to the formation of familiar groups in natural habitats. In addition, we suggest that familiarity benefits may reduce the relative value of transferring to otherwise more attractive (e.g. larger or more phenotypically matched) groups, and thereby stabilize shoal structure.

Animals↗

Cross-species familiarity in shoaling fishes.

Preferential association with familiar shoal mates confers a number of potentially important benefits to individuals, including improved anti-predator effects and the reduction of aggression in competitive interactions. Until now, however, familiarity has been demonstrated purely between conspecifics. Here, we present evidence that familiarity preferences can override natural preferences for conspecifics. Individual focal fishes (chub, Leuciscus cephalus) were given a choice of two stimulus shoals of the same size composed of conspecifics or of heterospecifics (minnows, Phoxinus phoxinus) in a flow tank. A series of four treatments was carried out to investigate the effects of familiarity, induced by a 15 day association between the focal fish and the stimulus fishes, on the choices made by the focal fish. Focal fishes showed a significant preference for conspecifics over heterospecifics when both stimulus shoals were composed of non-familiar individuals. Focal fishes also showed a significant preference for stimulus shoals composed of familiar fishes over stimulus shoals composed of non-familiar fishes when both shoals were conspecific and when both shoals were heterospecific. Finally, the preference of focal fishes for conspecifics disappeared when the alternative, a shoal of heterospecifics, was composed of familiar individuals. The importance of this work is discussed in the context of species interactions in free-ranging shoals.

Animals↗

The effects of familiarization on intelligibility and lexical segmentation in hypokinetic and ataxic dysarthria.

This study is the third in a series that has explored the source of intelligibility decrement in dysarthria by jointly considering signal characteristics and the cognitive-perceptual processes employed by listeners. A paradigm of lexical boundary error analysis was used to examine this interface by manipulating listener constraints with a brief familiarization procedure. If familiarization allows listeners to extract relevant segmental and suprasegmental information from dysarthric speech, they should obtain higher intelligibility scores than nonfamiliarized listeners, and their lexical boundary error patterns should approximate those obtained in misperceptions of normal speech. Listeners transcribed phrases produced by speakers with either hypokinetic or ataxic dysarthria after being familiarized with other phrases produced by these speakers. Data were compared to those of nonfamiliarized listeners [Liss et al., J. Acoust. Soc. Am. 107, 3415-3424 (2000)]. The familiarized groups obtained higher intelligibility scores than nonfamiliarized groups, and the effects were greater when the dysarthria type of the familiarization procedure matched the dysarthria type of the transcription task. Remarkably, no differences in lexical boundary error patterns were discovered between the familiarized and nonfamiliarized groups. Transcribers of the ataxic speech appeared to have difficulty distinguishing strong and weak syllables in spite of the familiarization. Results suggest that intelligibility decrements arise from the perceptual challenges posed by the degraded segmental and suprasegmental aspects of the signal, but that this type of familiarization process may differentially facilitate mapping segmental information onto existing phonological categories.

Adult↗

Cortical representations of personally familiar objects and places: functional organization of the human posterior cingulate cortex.

The recognition of both personally familiar objects and places involves nonspatial memory retrieval processes, but only personally familiar places are represented as space. Although the posterior cingulate cortex (PCC) is considered to process both types of such memories, its functional organization is poorly understood. In this event-related fMRI study, normal subjects judged familiar/unfamiliar pictures in four categories: familiar places (FP), familiar objects (FO), unfamiliar places (UP), and unfamiliar objects (UO), thus constituting a two-factorial design. A significant main effect of stimuli with greater activation in the place (FP and UP) than object (FO and UO) trials was observed bilaterally in several medial temporo-occipito-parietal regions, including the caudal PCC (cPCC) and parahippocampal gyrus. The reverse comparison revealed greater activation in the lateral inferior occipito-temporal junctions and intraparietal sulci bilaterally. A significant main effect of familiarity with greater activation in the familiar (FP and FO) than unfamiliar (UP and UO) trials was observed in the mid-dorsal PCC (mPCC), retrosplenial cortex, posterior precuneus, and the left intraparietal sulcus. Activation specific to the FP trials (as assessed by the interaction) was observed in the right posterodorsal PCC (pPCC) only. Together with data from previous functional imaging studies, the results suggest a functional segregation of human PCC with differential involvement of pPCC in spatial representations of personally familiar places and of the mPCC and retrosplenial cortex in episodic retrieval of personally familiar places and objects. Activation of the left intraparietal sulcus may reflect retrieval of memories related to object manipulation.

Adolescent↗

Separating the brain regions involved in recollection and familiarity in recognition memory.

The neural substrates of recognition memory retrieval were examined in a functional magnetic resonance imaging study designed to separate activity related to recollection from that related to continuous variations in familiarity. Across a variety of brain regions, the neural signature of recollection was found to be distinct from familiarity, demonstrating that recollection cannot be attributed to familiarity strength. In the prefrontal cortex, an anterior medial region was related to recollection, but lateral regions, including the anterior and dorsolateral prefrontal cortex, were related to familiarity. Along the lateral parietal cortex, two functionally distinct regions were also observed: a lateral parietal/temporal region related to recollection and a more superior parietal region involved in familiarity. Similarly, in medial parietal regions, the posterior cingulate was related to recollection, whereas the precuneus was related to familiarity. The hippocampus was related to recollection, but also exhibited an inverse relationship to familiarity-driven recognition confidence. The results indicate that recollection and familiarity rely on different networks of brain regions and provide insights into the functional roles of different regions involved in episodic recognition memory.

Adult↗

Combined pharmacological and electrophysiological dissociation of familiarity and recollection.

Dual-process theories of recognition memory hypothesize separate underlying familiarity and recollection processes, but the necessity of multiple processes is debated. Previous research has suggested that scalp-recorded event-related brain potentials (ERPs) may index the activity of separate familiarity and recollection processes. Other research indicates that the amnestic drug midazolam impairs recollection more than familiarity. Here, we used a convergent pharmacological and electrophysiological approach to manipulate and monitor human brain activity and provide evidence for separate processes. Midazolam selectively influenced the putative ERP-correlate of recollection but not the putative ERP-correlate of familiarity. Under control conditions (saline), subjects' accuracy correlated with the recollection-related but not the familiarity-related ERP component, suggesting that recollection was dominant in driving memory. The opposite pattern was observed under midazolam administration, suggesting that when recollection fails, subjects may leverage familiarity to compensate. Thus, in contrast to perspectives holding that familiarity represents the default process, these results suggest that recollection was dominant until its impairment unveiled the influence of familiarity.

Adult↗

Central forebrain Fos responses to familiar male odours are attenuated in recently mated female mice.

Exposure of recently mated female mice to the urinary odours of an unfamiliar male blocks pregnancy (the Bruce effect). The absence of a pregnancy block in response to the stud male's familiar odours depends on an olfactory memory that is formed in the accessory olfactory bulb (AOB) in response to vomeronasal organ (VNO) inputs during mating. Sexually naive Balb/c female mice in pro-oestrus/oestrus were either placed onto soiled bedding ('bedding-only' females) from, or allowed to mate with, a Balb/c male ('recently mated' females). After 42 h, females were placed for 90 min onto clean bedding (controls) or onto soiled bedding from either a C57BL/6 male (unfamiliar bedding) or a Balb/c male (familiar bedding). Significant increases in Fos-immunoreactivity (Fos-IR, a marker of neuronal activation) occurred in the medial amygdala and the medial preoptic area (MPA) of 'bedding only' females exposed to either unfamiliar or familiar bedding and in 'recently mated' females exposed to unfamiliar bedding but not to familiar bedding. This suggests that a mating-induced memory prevents the later activation by the familiar stud male's odours of neurons in forebrain regions that receive inputs from the VNO--AOB. 'Bedding-only' females later exposed to either familiar or unfamiliar bedding had increased Fos-IR in the G alpha(o) protein-expressing basal zone of the VNO whereas no such effect occurred in 'recently mated' females. Familiar, as well as unfamiliar, male odours augmented Fos-IR in significantly more rostral than caudal AOB granule cells in all groups, with the effect being strongest in 'recently mated' females exposed to familiar male bedding. This outcome is consistent with the absence of odour-induced Fos-IR in forebrain regions of these females and, presumably, the absence of a pregnancy block.

Animals↗

Comparison of computational models of familiarity discrimination in the perirhinal cortex.

This study compares the efficiency and plausibility of published computational models of familiarity discrimination in the perirhinal cortex. Substantial evidence indicates that the perirhinal cortex is involved in both the familiarity discrimination aspect of recognition memory and in perceptual functions involved with representations of complete stimuli (i.e., object identification). Published models of how the perirhinal cortex may perform familiarity discrimination can be divided into two groups. The first group assumes that a proportion of perirhinal neurons form a network specialised just for familiarity discrimination (these models may be based on Hebbian or anti-Hebbian synaptic plasticity). In contrast, the second group assumes that both familiarity discrimination and learning representations of complete stimuli are performed within a single combined network. This study establishes that when the responses of neurons that provide input to the familiarity discrimination network are correlated (as indicated by experimental data), specialised networks based on anti-Hebbian learning may recognise the previous occurrence of many more stimuli (i.e., have a capacity up to thousands of times larger) than specialised networks based on Hebbian learning. The currently published combined models do not learn an optimal stimulus representation (they do not fully extract statistically independent features), and hence their capacities are even lower than those of the specialised models based on Hebbian learning. Hence, the combined models published thus far are critically less efficient than the specialised models based on anti-Hebbian learning. This study also compares the consistency of the models with experimental observations concerning what is known of synaptic plasticity in the perirhinal cortex and the responses of its neurons. Many theoretically important parameters remain undetermined, and experiments are suggested to provide information critical for refining and distinguishing between the various models. However, the above theoretical arguments and currently published data favour the existence of a separate network specialised for familiarity discrimination.

Animals↗

Altered odor-induced expression of c-fos and arg 3.1 immediate early genes in the olfactory system after familiarization with an odor.

In adult rats, repeated exposure to an odorant, in absence of any experimentally delivered reinforcement, leads to a drastic decrease in mitral/tufted (M/T) cell responsiveness, not only for the familiar odor but also for other novel odors. In the present study, using two different and complementary in situ hybridization methods, we analyzed the effect of familiarization with an odorant on c-fos and arg 3.1 mRNA expression levels, and we examined the odor specificity of this effect. Odor exposure induces a specific increase in c-fos and arg 3.1 expression in some particular olfactory bulb quadrants. Previous familiarization with the test odor results in a decreased expression of both IEGs in these quadrants, leading to the alteration of the odor-specific pattern of c-fos and arg 3.1 expression. In contrast, this odor-specific pattern is not affected when different odors are used for familiarization and test. Similarly, an odor-specific familiarization effect leading to a reduced c-fos and arg 3.1 expression was also detected in the cingulate cortex and in the anterior piriform cortex. These results support our hypothesis that the decrease in M/T cell responsiveness following a preceding familiarization with an odorant may be related to a particular form of synaptic plasticity involving changes at the genomic level, and reveals further insight in olfactory information processing and the cellular mechanisms underlying familiarization in the olfactory system.

Animals↗