The impact of bilateral versus unilateral anterior temporal lobe damage on face recognition, person knowledge and semantic memory.

The functional importance of the anterior temporal lobes (ATLs) has come to prominence in two active, albeit unconnected literatures-(i) face recognition and (ii) semantic memory. To generate a unified account of the ATLs, we tested the predictions from each literature and examined the effects of bilateral versus unilateral ATL damage on face recognition, person knowledge, and semantic memory. Sixteen people with bilateral ATL atrophy from semantic dementia (SD), 17 people with unilateral ATL resection for temporal lobe epilepsy (TLE; left = 10, right = 7), and 14 controls completed tasks assessing perceptual face matching, person knowledge and general semantic memory. People with SD were impaired across all semantic tasks, including person knowledge. Despite commensurate total ATL damage, unilateral resection generated mild impairments, with minimal differences between left- and right-ATL resection. Face matching performance was largely preserved but slightly reduced in SD and right TLE. All groups displayed the familiarity effect in face matching; however, it was reduced in SD and right TLE and was aligned with the level of item-specific semantic knowledge in all participants. We propose a neurocognitive framework whereby the ATLs underpin a resilient bilateral representation system that supports semantic memory, person knowledge and face recognition.

Neurophysiological evidence for crossmodal (face-name) person-identity representation in the human left ventral temporal cortex.

Putting a name to a face is a highly common activity in our daily life that greatly enriches social interactions. Although this specific person-identity association becomes automatic with learning, it remains difficult and can easily be disrupted in normal circumstances or neurological conditions. To shed light on the neural basis of this important and yet poorly understood association between different input modalities in the human brain, we designed a crossmodal frequency-tagging paradigm coupled to brain activity recording via scalp and intracerebral electroencephalography. In Experiment 1, 12 participants were presented with variable pictures of faces and written names of a single famous identity at a 4-Hz frequency rate while performing an orthogonal task. Every 7 items, another famous identity appeared, either as a face or a name. Robust electrophysiological responses were found exactly at the frequency of identity change (i.e., 4 Hz / 7 = 0.571 Hz), suggesting a crossmodal neural response to person identity. In Experiment 2 with twenty participants, two control conditions with periodic changes of identity for faces or names only were added to estimate the contribution of unimodal neural activity to the putative crossmodal face-name responses. About 30% of the response occurring at the frequency of crossmodal identity change over the left occipito-temporal cortex could not be accounted for by the linear sum of unimodal responses. Finally, intracerebral recordings in the left ventral anterior temporal lobe (ATL) in 7 epileptic patients tested with this paradigm revealed a small number of "pure" crossmodal responses, i.e., with no response to changes of identity for faces or names only. Altogether, these observations provide evidence for integration of verbal and nonverbal person identity-specific information in the human brain, highlighting the contribution of the left ventral ATL in the automatic retrieval of face-name identity associations.

Neural Correlates of Naturally Occurring Speech Errors during Picture Naming in Healthy Participants.

Most of our knowledge about the neuroanatomy of speech errors comes from lesion-symptom mapping studies in people with aphasia and laboratory paradigms designed to elicit primarily phonological errors in healthy adults, with comparatively little evidence from naturally occurring speech errors. In this study, we analyzed perfusion fMRI data from 24 healthy participants during a picture naming task, classifying their responses into correct and different speech error types (e.g., semantic, phonological, omission errors). Total speech errors engaged a wide set of left-lateralized frontal, parietal, and temporal regions that were almost identical to those involved during the production of correct responses. We observed significant perfusion signal decreases in the left posterior middle temporal gyrus and inferior parietal lobule (angular gyrus) for semantic errors compared to correct trials matched on various psycholinguistic variables. In addition, the left dorsal caudate nucleus showed a significant perfusion signal decrease for omission (i.e., anomic) errors compared with matched correct trials. Surprisingly, we did not observe any significant perfusion signal changes in brain regions proposed to be associated with monitoring mechanisms during speech production (e.g., ACC, superior temporal gyrus). Overall, our findings provide evidence for distinct neural correlates of semantic and omission error types, with anomic speech errors likely resulting from failures to initiate articulatory-motor processes rather than semantic knowledge impairments as often reported for people with aphasia.

Intracerebral electrical stimulation of the right anterior fusiform gyrus impairs human face identity recognition.

Brain regions located between the right fusiform face area (FFA) in the middle fusiform gyrus and the temporal pole may play a critical role in human face identity recognition but their investigation is limited by a large signal drop-out in functional magnetic resonance imaging (fMRI). Here we report an original case who is suddenly unable to recognize the identity of faces when electrically stimulated on a focal location inside this intermediate region of the right anterior fusiform gyrus. The reliable transient identity recognition deficit occurs without any change of percept, even during nonverbal face tasks (i.e., pointing out the famous face picture among three options; matching pictures of unfamiliar or familiar faces for their identities), and without difficulty at recognizing visual objects or famous written names. The effective contact is associated with the largest frequency-tagged electrophysiological signals of face-selectivity and of familiar and unfamiliar face identity recognition. This extensive multimodal investigation points to the right anterior fusiform gyrus as a critical hub of the human cortical face network, between posterior ventral occipito-temporal face-selective regions directly connected to low-level visual cortex, the medial temporal lobe involved in generic memory encoding, and ventral anterior temporal lobe regions holding semantic associations to people's identity.

Implicit, automatic semantic word categorisation in the left occipito-temporal cortex as revealed by fast periodic visual stimulation.

Conceptual knowledge allows the categorisation of items according to their meaning beyond their physical similarities. This ability to respond to different stimuli (e.g., a leek, a cabbage, etc.) based on similar semantic representations (e.g., belonging to the vegetable category) is particularly important for language processing, because word meaning and the stimulus form are unrelated. The neural basis of this core human ability is debated and is complicated by the strong reliance of most neural measures on explicit tasks, involving many non-semantic processes. Here we establish an implicit method, i.e., fast periodic visual stimulation (FPVS) coupled with electroencephalography (EEG), to study neural conceptual categorisation processes with written word stimuli. Fourteen neurotypical participants were presented with different written words belonging to the same semantic category (e.g., different animals) alternating at 4 Hz rate. Words from a different semantic category (e.g., different cities) appeared every 4 stimuli (i.e., at 1 Hz). Following a few minutes of recording, objective electrophysiological responses at 1 Hz, highlighting the human brain's ability to implicitly categorize stimuli belonging to distinct conceptual categories, were found over the left occipito-temporal region. Topographic differences were observed depending on whether the periodic change involved living items, associated with relatively more ventro-temporal activity as compared to non-living items associated with relatively more dorsal posterior activity. Overall, this study demonstrates the validity and high sensitivity of an implicit frequency-tagged marker of word-based semantic memory abilities.

The neural basis of rapid unfamiliar face individuation with human intracerebral recordings.

Rapid individuation of conspecifics' faces is ecologically important in the human species, whether the face belongs to a familiar or unfamiliar individual. Here we tested a large group (N = 69) of epileptic patients implanted with intracerebral electrodes throughout the ventral occipito-temporal cortex (VOTC). We used a frequency-tagging visual stimulation paradigm optimized to objectively measure face individuation with direct neural recordings. This enabled providing an extensive map of the significantly larger neural responses to upright than to inverted unfamiliar faces, i.e. reflecting visual face individuation processes that go beyond physical image differences. These high-level face individuation responses are both distributed and anatomically confined to a strip of cortex running from the inferior occipital gyrus all along the lateral fusiform gyrus, with a large right hemispheric dominance. Importantly, face individuation responses are limited anteriorly to the bilateral anterior fusiform gyrus and surrounding sulci, with a near absence of significant responses in the extensively sampled temporal pole. This large-scale mapping provides original evidence that face individuation is supported by a distributed yet anatomically constrained population of neurons in the human VOTC, and highlights the importance of probing this function with face stimuli devoid of associated semantic, verbal and affective information.

The neuropsychological evaluation of face identity recognition.

Facial identity recognition (FIR) is arguably the ultimate form of recognition for the adult human brain. Even if the term prosopagnosia is reserved for exceptionally rare brain-damaged cases with a category-specific abrupt loss of FIR at adulthood, subjective and objective impairments or difficulties of FIR are common in the neuropsychological population. Here we provide a critical overview of the evaluation of FIR both for clinicians and researchers in neuropsychology. FIR impairments occur following many causes that should be identified objectively by both general and specific, behavioral and neural examinations. We refute the commonly used dissociation between perceptual and memory deficits/tests for FIR, since even a task involving the discrimination of unfamiliar face images presented side-by-side relies on cortical memories of faces in the right-lateralized ventral occipito-temporal cortex. Another frequently encountered confusion is between specific deficits of the FIR function and a more general impairment of semantic memory (of people), the latter being most often encountered following anterior temporal lobe damage. Many computerized tests aimed at evaluating FIR have appeared over the last two decades, as reviewed here. However, despite undeniable strengths, they often suffer from ecological limitations, difficulties of instruction, as well as a lack of consideration for processing speed and qualitative information. Taking into account these issues, a recently developed behavioral test with natural images manipulating face familiarity, stimulus inversion, and correct response times as a key variable appears promising. The measurement of electroencephalographic (EEG) activity in the frequency domain from fast periodic visual stimulation also appears as a particularly promising tool to complete and enhance the neuropsychological assessment of FIR.

A Comparison of Denoising Approaches for Spoken Word Production Related Artefacts in Continuous Multiband fMRI Data.

It is well-established from fMRI experiments employing gradient echo echo-planar imaging (EPI) sequences that overt speech production introduces signal artefacts compromising accurate detection of task-related responses. Both design and post-processing (denoising) techniques have been proposed and implemented over the years to mitigate the various noise sources. Recently, fMRI studies of speech production have begun to adopt multiband EPI sequences that offer better signal-to-noise ratio (SNR) and temporal resolution allowing adequate sampling of physiological noise sources (e.g., respiration, cardiovascular effects) and reduced scanner acoustic noise. However, these new sequences may also introduce additional noise sources. In this study, we demonstrate the impact of applying several noise-estimation and removal approaches to continuous multiband fMRI data acquired during a naming-to-definition task, including rigid body motion regression and outlier censoring, principal component analysis for removal of cerebrospinal fluid (CSF)/edge-related noise components, and global fMRI signal regression (using two different approaches) compared to a baseline of realignment and unwarping alone. Our results show the strongest and most spatially extensive sources of physiological noise are the global signal fluctuations arising from respiration and muscle action and CSF/edge-related noise components, with residual rigid body motion contributing relatively little variance. Interestingly, denoising approaches tended to reduce and enhance task-related BOLD signal increases and decreases, respectively. Global signal regression using a voxel-wise linear model of the global signal estimated from unmasked data resulted in dramatic improvements in temporal SNR. Overall, these findings show the benefits of combining continuous multiband EPI sequences and denoising approaches to investigate the neurobiology of speech production.

Stability of face recognition abilities after left or right anterior temporal lobectomy.

Patients with anterior temporal lobe (ATL) resection due to mesial temporal lobe epilepsy (MTLE) have difficulties at identifying familiar faces and explicitly remembering newly learned faces but their ability to individuate unfamiliar faces remains largely unknown. Moreover, the extent to which their difficulties with familiar face identity recognition and learning is truly due to the ATL resection remains unknown. Here, we report a study of 24 MTLE patients and matched healthy controls tested with an extensive set of seven face and visual object recognition tasks (including three tasks evaluating unfamiliar face individuation) before and about 6 months after unilateral (nine left, 15 right) ATL resection. We found that ATL resection has little or no effect on the patients' preserved pre-surgical ability to perform unfamiliar face individuation, both at the group and individual levels. More surprisingly, ATL resection also has little effect on the patients' performance at recognizing and naming famous faces as well as at learning new faces. A substantial proportion of right MTLE patients (33%) even improved their response times on several tasks, which may indicate a functional release of visuo-spatial processing after resection in the right ATL. Altogether this study shows that face recognition abilities are mainly unaffected by ATL resection in MTLE, either because the critical regions for face recognition are spared or because performance at some tasks is already lower than normal preoperatively. Overall, these findings urge caution when interpreting the causal effect of brain lesions on face recognition ability in patients with ATL resection due to MTLE. They also illustrate the complexity of predicting cognitive outcomes after epilepsy surgery because of the influence of many different intertwined factors.

Linguistic and attentional factors - Not statistical regularities - Contribute to word-selective neural responses with FPVS-oddball paradigms.

Studies using frequency-tagging in electroencephalography (EEG) have dramatically increased in the past 10 years, in a variety of domains and populations. Here we used Fast Periodic Visual Stimulation (FPVS) combined with an oddball design to explore visual word recognition. Given the paradigm's high sensitivity, it is crucial for future basic research and clinical application to prove its robustness across variations of designs, stimulus types and tasks. This paradigm uses periodicity of brain responses to measure discrimination between two experimentally defined categories of stimuli presented periodically. EEG was recorded in 22 adults who viewed words inserted every 5 stimuli (at 2 Hz) within base stimuli presented at 10 Hz. Using two discrimination levels (deviant words among nonwords or pseudowords), we assessed the impact of relative frequency of item repetition (set size or item repetition controlled for deviant versus base stimuli), and of the orthogonal task (focused or deployed spatial attention). Word-selective occipito-temporal responses were robust at the individual level (significant in 95% of participants), left-lateralized, larger for the prelexical (nonwords) than lexical (pseudowords) contrast, and stronger with a deployed spatial attention task as compared to the typically used focused task. Importantly, amplitudes were not affected by item repetition. These results help understanding the factors influencing word-selective EEG responses and support the validity of FPVS-EEG oddball paradigms, as they confirm that word-selective responses are linguistic. Second, they show its robustness against design-related factors that could induce statistical (ir)regularities in item rate. They also confirm its high individual sensitivity and demonstrate how it can be optimized, using a deployed rather than focused attention task, to measure implicit word recognition processes in typical and atypical populations.

A neural marker of the human face identity familiarity effect.

Human adults associate different views of an identity much better for familiar than for unfamiliar faces. However, a robust and consistent neural index of this behavioral face identity familiarity effect (FIFE)-not found in non-human primate species-is lacking. Here we provide such a neural FIFE index, measured implicitly and with one fixation per face. Fourteen participants viewed 70 s stimulation sequences of a large set (n = 40) of widely variable natural images of a face identity at a rate of 6 images/second (6 Hz). Different face identities appeared every 5th image (1.2 Hz). In a sequence, face images were either familiar (i.e., famous) or unfamiliar, participants performing a non-periodic task unrelated to face recognition. The face identity recognition response identified at 1.2 Hz over occipital-temporal regions in the frequency-domain electroencephalogram was 3.4 times larger for familiar than unfamiliar faces. The neural response to familiar faces-which emerged at about 180 ms following face onset-was significant in each individual but a case of prosopdysgnosia. Besides potential clinical and forensic applications to implicitly measure one's knowledge of a face identity, these findings open new perspectives to clarify the neurofunctional source of the FIFE and understand the nature of human face identity recognition.

Intracerebral electrical stimulation of the face-selective right lateral fusiform gyrus transiently impairs face identity recognition.

Neuroimaging and intracranial electrophysiological studies have consistently shown the largest and most consistent face-selective neural activity in the middle portion of the human right lateral fusiform gyrus ('fusiform face area(s)', FFA). Yet, direct evidence for the critical role of this region in face identity recognition (FIR) is still lacking. Here we report the first evidence of transient behavioral impairment of FIR during focal electrical stimulation of the right FFA. Upon stimulation of an electrode contact within this region, subject CJ, who shows typical FIR ability outside of stimulation, was transiently unable to point to pictures of famous faces among strangers and to match pictures of famous or unfamiliar faces presented simultaneously for their identity. Her performance at comparable tasks with other visual materials (written names, pictures of buildings) remained unaffected by stimulation at the same location. During right FFA stimulation, CJ consistently reported that simultaneously presented faces appeared as being the same identity, with little or no distortion of the spatial face configuration. Independent electrophysiological recordings showed the largest neural face-selective and face identity activity at the critical electrode contacts. Altogether, this extensive multimodal case report supports the causal role of the right FFA in FIR.

Typical visual unfamiliar face individuation in left and right mesial temporal epilepsy.

Patients with chronic mesial temporal lobe epilepsy have difficulties at identifying familiar faces as well as at explicit old/new face recognition tasks. However, the extent to which these difficulties can be attributed to visual individuation of faces, independently of general explicit learning and semantic memory processes, is unknown. We tested 42 mesial temporal lobe epilepsy patients divided into two groups according to the side of epilepsy (left and right) and 42 matched controls on an extensive series of individuation tasks of unfamiliar faces and control visual stimuli, as well as on face detection, famous face recognition and naming, and face and non-face learning. Overall, both patient groups had difficulties at identifying and naming famous faces, and at explicitly learning face and non-face images. However, there was no group difference in accuracy between patients and controls at the two most widely used neuropsychological tests assessing visual individuation of unfamiliar faces (Benton Facial Recognition Test and Cambridge Face Memory Test). While patients with right mesial temporal lobe epilepsy were slowed down at all tasks, this effect was not specific to faces or even high-level stimuli. Importantly, both groups showed the same profile of response as typical participants across various stimulus manipulations, showing no evidence of qualitative processing impairments. Overall, these results point to largely preserved visual face individuation processes in patients with mesial temporal lobe epilepsy, with semantic and episodic memory difficulties being consistent with the localization of the neural structures involved in their epilepsy (anterior temporal cortex and hippocampus). These observations have implications for the prediction of neuropsychological outcomes in the case of surgery and support the validity of intracranial electroencephalographic recordings performed in this population to understand neural mechanisms of human face individuation, notably through intracranial electrophysiological recordings and stimulations.