Famous faces activate contextual associations in the parahippocampal cortex

The parahippocampal cortex (PHC) has been traditionally implicated both in place processing and in episodic memory. How could the same cortical region mediate these cognitive functions that seem quite different? We have recently proposed that the PHC should be seen as more generally mediating contextual associative processing, which is required for both navigation and memory. We therefore predicted that any associative objects should activate the PHC. To test this generalization, we investigated the extent to which common stimuli that are nonspatial by nature, namely faces, activate the PHC, although their perception is typically associated with other cortical structures. Specifically, we compared the activation elicited by famous faces, which are highly associated with rich pictorial and contextual information (e.g., Tom Cruise) and are not associated with a specific place, with activation elicited by unfamiliar faces. Consistent with our prediction, contrasting famous with unfamiliar faces revealed significant activation within the PHC. Taken collectively, these findings indicate that the PHC should be regarded as mediating contextual associations in general and not necessarily spatial or episodic information.     

Spatio temporal dynamics of face recognition

To better understand face recognition, it is necessary to identify not only which brain structures are implicated but also the dynamics of the neuronal activity in these structures. Latencies can then be compared to unravel the temporal dynamics of information processing at the distributed network level. To achieve high spatial and temporal resolution, we used intracerebral recordings in epileptic subjects while they performed a famous/unfamiliar face recognition task. The first components peaked at 110 ms in the fusiform gyrus (FG) and simultaneously in the inferior frontal gyrus, suggesting the early establishment of a large-scale network. This was followed by components peaking at 160 ms in 2 areas along the FG. Important stages of distributed parallel processes ensued at 240 and 360 ms involving up to 6 regions along the ventral visual pathway. The final components peaked at 480 ms in the hippocampus. These stages largely overlapped. Importantly, event-related potentials to famous faces differed from unfamiliar faces and control stimuli in all medial temporal lobe structures. The network was bilateral but more right sided. Thus, recognition of famous faces takes place through the establishment of a complex set of local and distributed processes that interact dynamically and may be an emergent property of these interactions.     

Task-specific repetition priming in left inferior prefrontal cortex

Previous neuroimaging studies have shown that activation in left inferior prefrontal cortices (LIPC) is reduced during repeated (primed) relative to initial (unprimed) stimulus processing. These reductions in anterior (approximately BA 45/47) and posterior (approximately BA 44/6) LIPC activation have been interpreted as reflecting implicit memory for initial semantic or phonological processing. However, prior studies do not unambiguously indicate that LIPC priming effects are specific to the recapitulation of higher-level (semantic and/or phonological), rather than lower-level (perceptual), processes. Moreover, no prior study has shown that the patterns of priming in anterior and posterior LIPC regions are dissociable. To address these issues, the present fMRI study examined the nature of priming in LIPC by examining the task-specificity of these effects. Participants initially processed words in either a semantic or a nonsemantic manner. Subsequently, participants were scanned while they made semantic decisions about words that had been previously processed in a semantic manner (within-task repetition), words that had been previously processed in a nonsemantic manner (across-task repetition), and words that had not been previously processed (novel words). Behaviorally, task-specific priming was observed: reaction times to make the semantic decision declined following prior semantic processing but not following prior nonsemantic processing of a word. Priming in anterior LIPC paralleled these results with signal reductions being observed following within-task, but not following across-task, repetition. Importantly, neural priming in posterior LIPC demonstrated a different pattern: priming was observed following both within-task and across-task repetition, with the magnitude of priming tending to be greater in the within-task condition. Direct comparison between anterior and posterior LIPC regions revealed a significant interaction. These findings indicate that anterior and posterior LIPC demonstrate distinct patterns of priming, with priming in the anterior region being task-specific, suggesting that this facilitation derives from repeated semantic processing of a stimulus.     

Sound to language: different cortical processing for first and second languages in elementary school children as revealed by a large-scale study using fNIRS

A large-scale study of 484 elementary school children (6-10 years) performing word repetition tasks in their native language (L1-Japanese) and a second language (L2-English) was conducted using functional near-infrared spectroscopy. Three factors presumably associated with cortical activation, language (L1/L2), word frequency (high/low), and hemisphere (left/right), were investigated. L1 words elicited significantly greater brain activation than L2 words, regardless of semantic knowledge, particularly in the superior/middle temporal and inferior parietal regions (angular/supramarginal gyri). The greater L1-elicited activation in these regions suggests that they are phonological loci, reflecting processes tuned to the phonology of the native language, while phonologically unfamiliar L2 words were processed like nonword auditory stimuli. The activation was bilateral in the auditory and superior/middle temporal regions. Hemispheric asymmetry was observed in the inferior frontal region (right dominant), and in the inferior parietal region with interactions: low-frequency words elicited more right-hemispheric activation (particularly in the supramarginal gyrus), while high-frequency words elicited more left-hemispheric activation (particularly in the angular gyrus). The present results reveal the strong involvement of a bilateral language network in children's brains depending more on right-hemispheric processing while acquiring unfamiliar/low-frequency words. A right-to-left shift in laterality should occur in the inferior parietal region, as lexical knowledge increases irrespective of language.     

Neural basis for priming of pop-out during visual search revealed with fMRI

Maljkovic and Nakayama first showed that visual search efficiency can be influenced by priming effects. Even "pop-out" targets (defined by unique color) are judged quicker if they appear at the same location and/or in the same color as on the preceding trial, in an unpredictable sequence. Here, we studied the potential neural correlates of such priming in human visual search using functional magnetic resonance imaging (fMRI). We found that repeating either the location or the color of a singleton target led to repetition suppression of blood oxygen level-dependent (BOLD) activity in brain regions traditionally linked with attentional control, including bilateral intraparietal sulci. This indicates that the attention system of the human brain can be "primed," in apparent analogy to repetition-suppression effects on activity in other neural systems. For repetition of target color but not location, we also found repetition suppression in inferior temporal areas that may be associated with color processing, whereas repetition of target location led to greater reduction of activation in contralateral inferior parietal and frontal areas, relative to color repetition. The frontal eye fields were also implicated, notably when both target properties (color and location) were repeated together, which also led to further BOLD decreases in anterior fusiform cortex not seen when either property was repeated alone. These findings reveal the neural correlates for priming of pop-out search, including commonalities, differences, and interactions between location and color repetition. fMRI repetition-suppression effects may arise in components of the attention network because these settle into a stable "attractor state" more readily when the same target property is repeated than when a different attentional state is required.     

The M170 reflects a viewpoint-dependent representation for both familiar and unfamiliar faces

The aim of this study was to determine the extent to which the neural representation of faces in visual cortex is viewpoint dependent or viewpoint invariant. Magnetoencephalography was used to measure evoked responses to faces during an adaptation paradigm. Using familiar and unfamiliar faces, we compared the amplitude of the M170 response to repeated images of the same face with images of different faces. We found a reduction in the M170 amplitude to repeated presentations of the same face image compared with images of different faces when shown from the same viewpoint. To establish if this adaptation to the identity of a face was invariant to changes in viewpoint, we varied the viewing angle of the face within a block. We found a reduction in response was no longer evident when images of the same face were shown from different viewpoints. This viewpoint-dependent pattern of results was the same for both familiar and unfamiliar faces. These results imply that either the face-selective M170 response reflects an early stage of face processing or that the computations underlying face recognition depend on a viewpoint-dependent neuronal representation.     

Altered bidirectional plasticity and reduced implicit motor learning in concussed athletes

Persistent motor/cognitive alterations and increased prevalence of Alzheimer's disease are known consequences of recurrent sports concussions, the most prevalent cause of mild traumatic brain injury (TBI) among youth. Animal models of TBI demonstrated that impaired learning was related to persistent synaptic plasticity suppression in the form of long-term potentiation (LTP) and depression (LTD). In humans, single and repeated concussive injuries lead to lifelong and cumulative enhancements of gamma-aminobutyric acid (GABA)-mediated inhibition, which is known to suppress LTP/LTD plasticity. To test the hypothesis that increased GABAergic inhibition after repeated concussions suppresses LTP/LTD and contributes to learning impairments, we used a paired associative stimulation (PAS) protocol to induce LTP/LTD-like effects in primary motor cortex (M1) jointly with an implicit motor learning task (serial reaction time task, SRTT). Our results indicate that repeated concussions induced persistent elevations of GABA(B)-mediated intracortical inhibition in M1, which was associated with suppressed PAS-induced LTP/LTD-like synaptic plasticity. This synaptic plasticity suppression was related to reduced implicit motor learning on the SRTT task relative to normal LTP/LTD-like synaptic plasticity in unconcussed teammates. These findings identify GABA neurotransmission alterations after repeated concussions and suggest that impaired learning after multiple concussions could at least partly be related to compromised GABA-dependent LTP/LTD synaptic plasticity.     

Repetition suppression and reactivation in auditory-verbal short-term recognition memory

The neural response to stimulus repetition is not uniform across brain regions, stimulus modalities, or task contexts. For instance, it has been observed in many functional magnetic resonance imaging (fMRI) studies that sometimes stimulus repetition leads to a relative reduction in neural activity (repetition suppression), whereas in other cases repetition results in a relative increase in activity (repetition enhancement). In the present study, we hypothesized that in the context of a verbal short-term recognition memory task, repetition-related "increases" should be observed in the same posterior temporal regions that have been previously associated with "persistent activity" in working memory rehearsal paradigms. We used fMRI and a continuous recognition memory paradigm with short lags to examine repetition effects in the posterior and anterior regions of the superior temporal cortex. Results showed that, consistent with our hypothesis, the 2 posterior temporal regions consistently associated with working memory maintenance, also show repetition increases during short-term recognition memory. In contrast, a region in the anterior superior temporal lobe showed repetition suppression effects, consistent with previous research work on perceptual adaptation in the auditory-verbal domain. We interpret these results in light of recent theories of the functional specialization along the anterior and posterior axes of the superior temporal lobe.     

Cognitive response profile of the human fusiform face area as determined by MEG

Activation in or near the fusiform gyrus was estimated to faces and control stimuli. Activation peaked at 165 ms and was strongest to digitized photographs of human faces, regardless of whether they were presented in color or grayscale, suggesting that face- and color-specific areas are functionally separate. Schematic sketche evoked approximately 30% less activation than did face photographs. Scrambling the locations of facial features reduced the response by approximately 25% in either hemisphere, suggesting that configurational versus analytic processing is not lateralized at this latency. Animal faces evoked approximately 50% less activity, and common objects, animal bodies or sensory controls evoked approximately 80% less activity than human faces. The (small) responses evoked by meaningless control images were stronger when they included surfaces and shading, suggesting that the fusiform gyrus may use these features in constructing its face-specific response. Putative fusiform activation was not significantly related to stimulus repetition, gender or emotional expression. A midline occipital source significantly distinguished between faces and control images as early as 110 ms, but was more sensitive to sensory qualities. This source significantly distinguished happy and sad faces from those with neutral expressions. We conclude that the fusiform gyrus may selectively encode faces at 165 ms, transforming sensory input for further processing.     

Distinct and convergent visual processing of high and low spatial frequency information in faces

We tested for differential brain response to distinct spatialfrequency (SF) components in faces. During a functional magneticresonance imaging experiment, participants were presented with"hybrid" faces containing superimposed low and high SF informationfrom different identities. We used a repetition paradigm wherefaces at either SF range were independently repeated or changedacross consecutive trials. In addition, we manipulated whichSF band was attended. Our results suggest that repetition andattention affected partly overlapping occipitotemporal regionsbut did not interact. Changes of high SF faces increased responsesof the right inferior occipital gyrus (IOG) and left inferiortemporal gyrus (ITG), with the latter response being also modulatedadditively by attention. In contrast, the bilateral middle occipitalgyrus (MOG) responded to repetition and attention manipulationsof low SF. A common effect of high and low SF repetition wasobserved in the right fusiform gyrus (FFG). Follow-up connectivityanalyses suggested direct influence of the MOG (low SF), IOG,and ITG (high SF) on the FFG responses. Our results reveal thatdifferent regions within occipitotemporal cortex extract distinctvisual cues at different SF ranges in faces and that the outputsfrom these separate processes project forward to the right FFG,where the different visual cues may converge.     

Familiarity and conceptual priming engage distinct cortical networks

Familiarity refers to an explicit recognition experience without any necessary retrieval of specific detail related to the episode during which initial learning transpired. Prior experience can also implicitly influence subsequent processing through a memory phenomenon termed conceptual priming, which occurs without explicit awareness of recognition. Resolving current theoretical controversy on relationships between familiarity and conceptual priming requires a clarification of their neural substrates. Accordingly, we obtained functional magnetic resonance images in a novel paradigm for separately assessing neural correlates of familiarity and conceptual priming using famous and nonfamous faces. Conceptual priming, as shown by more accurate behavioral responses to strongly conceptually primed than to weakly conceptually primed faces, was associated with activity reductions in left prefrontal cortex, whereas familiarity was associated with activity enhancements in right parietal cortex for more-familiar compared with less-familiar faces. This neuroimaging evidence implicates separate neurocognitive processes operative in explicit stimulus recognition versus implicit conceptual priming.     

The priming method: imaging unconscious repetition priming reveals an abstract representation of number in the parietal lobes.

Most of the current brain imaging methods are limited by the low spatial resolution of neuroimaging techniques and remain unable to measure activity at the scale of single neurons or small columns of neurons, which are the coding elements of the nervous system. In this work we have adapted the priming method, an emerging research strategy that can overcome some of these spatial limitations, to investigate the coding of numerical quantities in the human brain. This approach combines the logic of psychological priming experiments with the recently discovered neurophysiological phenomenon called repetition suppression (RS). In each trial, while subjects perform a constant task, a subliminal prime is presented prior to each target. By varying the relationship between prime and target, one can detect which brain areas present RS specifically for any given level of prime-target repetition. We first expose the general logic, potential and limitations of the priming method and then illustrate it by demonstrating that a region of parietal cortex is coding for numbers at the quantity level, independently of other stimulus attributes, and that this region processes both consciously and unconsciously perceived stimuli.     

Distinctive Forms of Partial Retrograde Amnesia after Asymmetric Temporal Lobe Lesions: Possible Role of the Occipitotemporal Gyri in Memory

We tested the hypothesis that partial forms of retrograde amnesiawere associated with highly asymmetric lesions to the inferiorand anterior-medial temporal lobe. Postencephalitic subjectsEK and DR were both impaired on standardized retrograde memorytests, but showed strikingly different profiles in cognitivetasks of name stem completion, name;face matching, temporalordering, forced choice recognition, and occupational judgmentsof famous names and faces from the past 3 decades. EK sustainedleft inferior and anterior-medial temporal lobe lesion witha small right temporal polar lesion, and showed near-completeloss of retrieval, knowledge, and familiarity associated withfamous names but minimal deficiencies with famous faces. DRsustained right inferior and anterior-medial temporal lobe lesionand showed a milder retrograde loss limited to utilizing famousface prompts in name stem completion, name;face matching, occupationaljudgments, and forced choice recognition. These impairmentswere also different from the memory retrieval deficit, but intactrecognition shown by a case of ruptured anterior communicatingartery aneurysm with presumed basal forebrain damage. We hypothesizethat Ek's extensive loss of famous name knowledge was relatedto left inferior temporal lobe damage, particularly in the lateraland medial occipitotemporal gyri. This region in the left temporallobe may serve as a critical processing area for retrogradememory that permits activation of established semantic, temporal,and visual (i.e., facial) associations biographically dependenton the category of proper names. On the basis of connectionalanatomy patterns in the nonhuman primate, this region receivesextensive hippocampal output and is interconnected with thetemporal polar region and cortical association areas, whichhave been implicated in retrieval and storage aspects of retrogradememory. In the right hemisphere, the occipitotemporal gyri mayserve an important role in famous face processing as part ofa bilateral neural network.     

Increased neural efficiency with repeated performance of a working memory task is information-type dependent

Unlike tasks in which practice leads to an automatic stimulus-response association, it is thought working memory (WM) tasks continue to require cognitive control processes after repeated performance. Previous studies investigating WM task repetition are in accord with this. However, it is unclear whether changes in neural activity after repetition imply alterations in general control processes common to all WM tasks or are specific to the selection, encoding and maintenance of the relevant information. In the present study, functional magnetic resonance imaging (fMRI) was used to examine changes during sample, delay and test periods during repetition of both object and spatial delayed recognition tasks. We found decreases in fMRI activation in both spatial and object-selective areas after spatial WM task repetition, independent of behavioral performance. Few areas showed changed activity after object WM task repetition. These results indicate that spatial task repetition leads to increased efficiency of maintaining task-relevant information and improved ability to filter out task-irrelevant information. The specificity of this repetition effect to the spatial task suggests a difference exists in the nature of the representation of object and spatial information and that their maintenance in WM is likely subserved by different neural systems.     

Who is who: areas of the brain associated with recognizing and naming famous faces

OBJECT: It has been hypothesized that specific brain regions involved in face naming may exist in the brain. To spare these areas and to gain a better understanding of their organization, the authors studied patients who underwent surgery by using direct electrical stimulation mapping for brain tumors, and they compared an object-naming task to a famous face-naming task. METHODS: Fifty-six patients with brain tumors (39 and 17 in the left and right hemispheres, respectively) and with no significant preoperative overall language deficit were prospectively studied over a 2-year period. Four patients who had a partially selective famous face anomia and 2 with prosopagnosia were not included in the final analysis. RESULTS: Face-naming interferences were exclusively localized in small cortical areas (< 1 cm2). Among 35 patients whose dominant left hemisphere was studied, 26 face-naming specific areas (that is, sites of interference in face naming only and not in object naming) were found. These face naming-specific sites were significantly detected in 2 regions: in the left frontal areas of the superior, middle, and inferior frontal gyri (p < 0.001) and in the anterior part of the superior and middle temporal gyri (p < 0.01). Variable patterns of interference were observed (speech arrest, anomia, phonemic, or semantic paraphasia) probably related to the different stages in famous face processing. Only 4 famous face-naming interferences were found in the right hemisphere. CONCLUSIONS: Relative anatomical segregation of naming categories within language areas was detected. This study showed that famous face naming was preferentially processed in the left frontal and anterior temporal gyri. The authors think it is necessary to adapt naming tasks in neurosurgical patients to the brain region studied.     

Hippocampal and brain stem activation during word retrieval after repeated and semantic encoding

Repeated word presentation during learning and the use of a semantic encoding task both increase the accuracy of subsequent word retrieval. Previous neuroimaging studies have shown that successful word retrieval depends on the recruitment of the hippocampus, whereas the effort of retrieval is linked to activation of prefrontal cortex modules. We studied the effects of repetition (4x versus 1x presentation) and encoding task (semantic versus perceptual) on hippocampal and prefrontal cortex activation during word-stem cued recall using positron emission tomography. Repeated and semantic encoding resulted in increased recall accuracy, with word repetition showing a greater effect when using a semantic encoding task. The more successful retrieval of words presented repeatedly compared with words presented once was associated with activation of the left anterior hippocampus. The more successful retrieval of words encoded using a semantic compared with a perceptual task was associated with activation of the right posterior and, less significantly, the left anterior hippocampus. The greater benefit of repeated learning when using the semantic task was linked to activation of the right brainstem, in the region of the ventral tegmentum. Our results suggest that word repetition and semantic encoding increase recall accuracy during subsequent word retrieval via distinct hippocampal mechanisms and that ventral tegmentum activation is relevant for word retrieval after semantic encoding. These findings confirm the importance of hippocampal recruitment during word retrieval and provide novel evidence for a role of brainstem neurons in word retrieval after semantic encoding.     

Dissociation between explicit memory and configural memory in the human medial temporal lobe

Using functional magnetic resonance imaging, the current study explored the differential mnemonic contributions of the hippocampus and surrounding medial temporal lobe (MTL) cortices to explicit recognition memory and configural learning. Using a task that required processing of repeated and novel visuospatial contexts across multiple trials, we examined MTL activation in relation to 3 forms of learning in a single paradigm: 1) context-independent procedural learning, 2) context-dependent configural learning, and 3) explicit recognition memory. Activations in hippocampus and parahippocampal cortex were associated with explicit memory, differentiating between subsequently remembered and forgotten repeated contexts, but were unrelated to context-dependent configural learning. Activations in regions of perirhinal and entorhinal cortex were associated with configural learning of repeated contexts independent from explicit memory for those contexts. Procedural learning was unrelated to activation in any MTL region. The time course of activation across learning further differed in MTL subregions with MTL cortex demonstrating repetition-related decreases and hippocampus repetition-related increases. These repetition effects were differentially sensitive to recognition with only activation in hippocampus and parahippocampal cortex tracking recognized items. These imaging findings converge with studies of amnesia and indicate dissociable roles for hippocampus in learning that supports explicit recognition and for anterior MTL cortex in configural learning.     

Increased reading speed for stories presented during general anesthesia

BACKGROUND: In the absence of explicit memories such as the recall and recognition of intraoperative events, memory of auditory information played during general anesthesia has been demonstrated with several tests of implicit memory. In contrast to explicit memory, which requires conscious recollection, implicit memory does not require recollection of previous experiences and is evidenced by a priming effect on task performance. The authors evaluated the effect of a standardized anesthetic technique on implicit memory, first using a word stem completion task, and then a reading speed task in a subsequent study. METHODS: While undergoing lumbar disc surgery, 60 patients were exposed to auditory materials via headphones in two successive experiments. A balanced intravenous technique with propofol and alfentanil infusions and a nitrous oxide-oxygen mixture was used to maintain adequate anesthesia. In the first experiment, 30 patients were exposed randomly to one of the two lists of 34 repeated German nouns; in the second experiment, 30 patients were exposed to one of two tapes containing two short stories. Thirty control patients for each experiment heard the tapes without receiving anesthesia. All patients were tested for implicit memory 6-8 h later: A word stem completion task for the words and a reading speed task for the stories were used as measures of implicit memory. RESULTS: The control group completed the word stems significantly more often with the words that they had heard previously, but no such effect was found in the anesthetized group. However, both the control and patient groups showed a decreased reading time of about 40 ms per word for the previously presented stories compared with the new stories. The patients had no explicit memory of intraoperative events. CONCLUSIONS: Implicit memory was demonstrated after anesthesia by the reading speed task but not by the word stem completion task. Some methodologic aspects, such as using low frequency words or varying study and test modalities, may account for the negative results of the word stem completion task. Another explanation is that anesthesia with propofol, alfentanil, and nitrous oxide suppressed the word priming but not the reading speed measure of implicit memory. The reading speed paradigm seems to provide a stable and reliable measurement of implicit memory.     

An event-related fMRI study of explicit syntactic processing of normal/anomalous sentences in contrast to implicit syntactic processing

Using event-related functional magnetic resonance imaging (fMRI), we examined activation of cortical language areas for explicit syntactic processing. In a syntactic decision (Syn) task, the participants judged whether the presented sentence was syntactically correct, where syntactic knowledge about the distinction between transitive and intransitive verbs was required. In a semantic decision (Sem) task, lexico-semantic knowledge about selectional restrictions was indispensable. In a phonological decision (Pho) task, phonological knowledge about accent patterns was required. The Sem and Pho tasks involved implicit syntactic processing, as well as explicit semantic and phonological processing, respectively. We also tested a voice-pitch comparison (Voi) task in which no explicit linguistic knowledge was required. In the direct comparison of Syn - (Sem + Pho + Voi), we found localized activation in the left inferior frontal gyrus (F3op/F3t), indicating that activation of the left F3op/F3t is more prominently enhanced in explicit syntactic processing than in implicit syntactic processing. Moreover, we determined that its activation is selective to syntactic judgments regarding both normal and anomalous sentences. These results suggest that explicit information processing in the syntactic domain critically involves the left F3op/F3t, which is functionally separable from other regions.     

Functional significance of olfactory-induced oscillations in the human amygdala

We recorded directly from the amygdalar nucleus of nine epileptic patients performing a delayed odor-matching recognition memory task. Time-frequency analysis of the responses to the odorants revealed that the stimulations elicited induced oscillatory responses, as well as already described olfactory evoked potentials. These oscillatory responses were composed of two frequency components--one in the beta band (15-25 Hz) and a faster one, in the low gamma band (25-35 Hz)--both of which lasted during the full duration of the inspiration. In pairs of identical odorants, the power of gamma oscillations was weaker for the second odorant (the target) than for the first one (the sample). We observed no such difference when the first and second odorants of a pair were different. Thus, gamma oscillations in the amygdala are weaker for repeated stimuli, a mechanism known as repetition suppression. This is consistent with an involvement of the human amygdala in the encoding and retrieval of olfactory information independently of its hedonic properties, at least in epileptic patients. Altogether, our results corroborate in humans evidence found in animals that oscillations serve as a common coding process of olfactory information.