The sudden onset of a face image leads to a prominent face‐selective response in human scalp electroencephalographic (EEG) recordings, peaking 170 ms after stimulus onset at occipito–temporal (OT) ...scalp sites: the N170 (or M170 in magnetoencephalography). According to a widely held view, the main cortical source of the N170 lies in the fusiform gyrus (FG), whereas the posteriorly located inferior occipital gyrus (IOG) would rather generate earlier face‐selective responses. Here, we report neural responses to upright and inverted faces recorded in a unique patient using multicontact intracerebral electrodes implanted in the right IOG and in the OT sulcus above the right lateral FG (LFG). Simultaneous EEG recordings on the scalp identified the N170 over the right OT scalp region. The latency and amplitude of this scalp N170 were correlated at the single‐trial level with the N170 recorded in the lateral IOG, close to the scalp lateral occipital surface. In addition, a positive component maximal around the latency of the N170 (a P170) was prominent above the internal LFG, whereas this region typically generates an N170 (or “N200”) over its external/ventral surface. This suggests that electrophysiological responses in the LFG manifest as an equivalent dipole oriented mostly along the vertical axis with likely minimal projection to the lateral OT scalp region. Altogether, these observations provide evidence that the IOG is a major cortical generator of the face‐selective scalp N170, qualifying the potential contribution of the FG and questioning a strict serial spatiotemporal organization of the human cortical face network.
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.
Stereo-electroencephalography (sEEG) is a method that uses stereotactically implanted depth electrodes for extra-operative mapping of epileptogenic and functional networks. sEEG derived functional ...mapping is achieved using electrical cortical stimulations (ECS) that are currently the gold standard for delineating eloquent cortex. As this stands true especially for primary cortices (e.g., visual, sensitive, motor, etc.), ECS applied to higher order brain areas determine more subtle behavioral responses. While anterior and posterior language areas in the dorsal language stream seem to share characteristics with primary cortices, basal temporal language area (BTLA) in the ventral temporal cortex (VTC) behaves as a highly associative cortex. After a short introduction and considerations about methodological aspects of ECS using sEEG, we review the sEEG language mapping literature in this perspective. We first establish the validity of this technique to map
language cortices in the dorsal language stream. Second, we highlight the contrast between the growing empirical ECS experience and the lack of understanding regarding the fundamental mechanisms underlying ECS behavioral effects, especially concerning the dispensable language cortex in the VTC. Evidences for considering network architecture as determinant for ECS behavioral response complexities are discussed. Further, we address the importance of designing new research in network organization of language as this could enhance ECS ability to map interindividual variability, pathology driven reorganization, and ultimately identify network resilience markers in order to better predict post-operative language deficit. Finally, based on a whole body of available studies, we believe there is strong evidence to consider sEEG as a valid, safe and reliable method for defining eloquent language cortices although there have been no proper comparisons between surgical resections with or without extra-operative or intra-operative language mapping.
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.
Understanding how the human brain recognizes faces is a primary scientific goal in cognitive neuroscience. Given the limitations of the monkey model of human face recognition, a key approach in this ...endeavor is the recording of electrophysiological activity with electrodes implanted inside the brain of human epileptic patients. However, this approach faces a number of challenges that must be overcome for meaningful scientific knowledge to emerge. Here we synthesize a 10 year research program combining the recording of intracerebral activity (StereoElectroEncephaloGraphy, SEEG) in the ventral occipito-temporal cortex (VOTC) of large samples of participants and fast periodic visual stimulation (FPVS), to objectively define, quantify, and characterize the neural basis of human face recognition. These large-scale studies reconcile the wide distribution of neural face recognition activity with its (right) hemispheric and regional specialization and extend face-selectivity to anterior regions of the VOTC, including the ventral anterior temporal lobe (VATL) typically affected by magnetic susceptibility artifacts in functional magnetic resonance imaging (fMRI). Clear spatial dissociations in category-selectivity between faces and other meaningful stimuli such as landmarks (houses, medial VOTC regions) or written words (left lateralized VOTC) are found, confirming and extending neuroimaging observations while supporting the validity of the clinical population tested to inform about normal brain function. The recognition of face identity - arguably the ultimate form of recognition for the human brain - beyond mere differences in physical features is essentially supported by selective populations of neurons in the right inferior occipital gyrus and the lateral portion of the middle and anterior fusiform gyrus. In addition, low-frequency and high-frequency broadband iEEG signals of face recognition appear to be largely concordant in the human association cortex. We conclude by outlining the challenges of this research program to understand the neural basis of human face recognition in the next 10 years.
•Validation of a new face localizer for non-human primate (NHP) imaging.•Typical face-selective clusters in monkey STS with frequency-tagging.•Highest sensitivity and test-retest reliability of ...face-selective activations.•No face-selective activation in ventral occipito-temporal regions.•Face-selective activation significantly larger to monkey faces in middle STS.
Non-human primate (NHP) neuroimaging can provide essential insights into the neural basis of human cognitive functions. While functional magnetic resonance imaging (fMRI) localizers can play an essential role in reaching this objective (Russ et al., 2021), they often differ substantially across species in terms of paradigms, measured signals, and data analysis, biasing the comparisons. Here we introduce a functional frequency-tagging face localizer for NHP imaging, successfully developed in humans and outperforming standard face localizers (Gao et al., 2018). FMRI recordings were performed in two awake macaques. Within a rapid 6 Hz stream of natural non-face objects images, human or monkey face stimuli were presented in bursts every 9 s. We also included control conditions with phase-scrambled versions of all images. As in humans, face-selective activity was objectively identified and quantified at the peak of the face-stimulation frequency (0.111 Hz) and its second harmonic (0.222 Hz) in the Fourier domain. Focal activations with a high signal-to-noise ratio were observed in regions previously described as face-selective, mainly in the STS (clusters PL, ML, MF; also, AL, AF), both for human and monkey faces. Robust face-selective activations were also found in the prefrontal cortex of one monkey (PVL and PO clusters). Face-selective neural activity was highly reliable and excluded all contributions from low-level visual cues contained in the amplitude spectrum of the stimuli. These observations indicate that fMRI frequency-tagging provides a highly valuable approach to objectively compare human and monkey visual recognition systems within the same framework.
The extent to which faces and written words share neural circuitry in the human brain is actively debated. Here, we compare face-selective and word-selective responses in a large group of patients (
...N
= 37) implanted with intracerebral electrodes in the ventral occipito-temporal cortex (VOTC). Both face-selective (i.e., significantly different responses to faces vs. non-face visual objects) and word-selective (i.e., significantly different responses to words vs. pseudofonts) neural activity is isolated with frequency-tagging. Critically, this sensitive approach allows to objectively quantify category-selective neural responses and disentangle them from general visual responses. About 70% of significant electrode contacts show either face-selectivity or word-selectivity only, with the expected right and left hemispheric dominance, respectively. Spatial dissociations are also found within core regions of face and word processing, with a medio-lateral dissociation in the fusiform gyrus (FG) and surrounding sulci, respectively. In the 30% of overlapping face- and word-selective contacts across the VOTC or in the FG and surrounding sulci, between-category-selective amplitudes (faces vs. words) show no-to-weak correlations, despite strong correlations in both the within-category-selective amplitudes (face–face, word–word) and the general visual responses to words and faces. Overall, these observations support the view that category-selective circuitry for faces and written words is largely dissociated in the human adult VOTC.
In vivo intracranial recordings of neural activity offer a unique opportunity to understand human brain function. Intracranial electrophysiological (iEEG) activity related to sensory, cognitive or ...motor events manifests mostly in two types of signals: event-related local field potentials in lower frequency bands (<30 Hz, LF) and broadband activity in the higher end of the frequency spectrum (>30 Hz, High frequency, HF). While most current studies rely exclusively on HF, thought to be more focal and closely related to spiking activity, the relationship between HF and LF signals is unclear, especially in human associative cortex. Here, we provide a large-scale in-depth investigation of the spatial and functional relationship between these 2 signals based on intracranial recordings from 121 individual brains (8000 recording sites). We measure category-selective responses to complex ecologically salient visual stimuli – human faces – across a wide cortical territory in the ventral occipito-temporal cortex (VOTC), with a frequency-tagging method providing high signal-to-noise ratio (SNR) and the same objective quantification of signal and noise for the two frequency ranges. While LF face-selective activity has higher SNR across the VOTC, leading to a larger number of significant electrode contacts especially in the anterior temporal lobe, LF and HF display highly similar spatial, functional, and timing properties. Specifically, and contrary to a widespread assumption, our results point to nearly identical spatial distribution and local spatial extent of LF and HF activity at equal SNR. These observations go a long way towards clarifying the relationship between the two main iEEG signals and reestablish the informative value of LF iEEG to understand human brain function.
•Concurrent recordings of brain function measured with frequency-tagging iEEG and DES.•Different faces presented at 6Hz perceived as the same during DES to right FFA.•DES to right FFA reduces ...concurrent face-selective neural activity at remote sites.•Frequency-tagging provides artifact-free measures during concurrent DES.•Cortical sites affected by DES effects are functionally connected.
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.
PDF
