Abstract
Faces are critical for social interactions and their recognition constitutes one of the most important and challenging functions of the human brain. While neurons responding selectively to ...faces have been recorded for decades in the monkey brain, face-selective neural activations have been reported with neuroimaging primarily in the human midfusiform gyrus. Yet, the cellular mechanisms producing selective responses to faces in this hominoid neuroanatomical structure remain unknown. Here we report single neuron recordings performed in 5 human subjects (1 male, 4 females) implanted with intracerebral microelectrodes in the face-selective midfusiform gyrus, while they viewed pictures of familiar and unknown faces and places. We observed similar responses to faces and places at the single cell level, but a significantly higher number of neurons responding to faces, thus offering a mechanistic account for the face-selective activations observed in this region. Although individual neurons did not respond preferentially to familiar faces, a population level analysis could consistently determine whether or not the faces (but not the places) were familiar, only about 50 ms after the initial recognition of the stimuli as faces. These results provide insights into the neural mechanisms of face processing in the human brain.
During intracerebral stimulation of the right inferior occipital cortex, a patient with refractory epilepsy was transiently impaired at discriminating two simultaneously presented photographs of ...unfamiliar faces. The critical electrode contact was located in the most posterior face-selective brain area of the human brain (right “occipital face area”, rOFA) as shown both by low- (ERP) and high-frequency (gamma) electrophysiological responses as well as a face localizer in fMRI. At this electrode contact, periodic visual presentation of 6 different faces by second evoked a larger electrophysiological periodic response at 6Hz than when the same face identity was repeated at the same rate. This intracerebral EEG repetition suppression effect was markedly reduced when face stimuli were presented upside-down, a manipulation that impairs individual face discrimination. These findings provide original evidence for a causal relationship between the face-selective right inferior occipital cortex and individual face discrimination, independently of long-term memory representations. More generally, they support the functional value of electrophysiological repetition suppression effects, indicating that these effects can be used as an index of a necessary neural representation of the changing stimulus property.
•Electrical stimulation of the right OFA impairs individual face discrimination.•There is a causal link between the right OFA and individual face discrimination.•Repetition suppression with periodic visual stimulation is functionally relevant.
According to neuropsychological evidence, a distributed network of regions of the ventral visual pathway – from the lateral occipital cortex to the temporal pole – supports face recognition. However, ...functional magnetic resonance imaging (fMRI) studies have generally confined ventral face-selective areas to the posterior section of the occipito-temporal cortex, i.e., the inferior occipital gyrus occipital face area (OFA) and the posterior and middle fusiform gyrus fusiform face area (FFA). There is recent evidence that intracranial electrical stimulation of these areas in the right hemisphere elicits face matching and recognition impairments (i.e., prosopagnosia) as well as perceptual face distortions. Here we report a case of transient inability to recognize faces following electrical stimulation of the right anterior fusiform gyrus, in a region located anteriorly to the FFA. There was no perceptual face distortion reported during stimulation. Although no fMRI face-selective responses were found in this region due to a severe signal drop-out as in previous studies, intracerebral face-selective event-related potentials and gamma range electrophysiological responses were found at the critical site of stimulation. These results point to a causal role in face recognition of the right anterior fusiform gyrus and more generally of face-selective areas located beyond the “core” face-processing network in the right ventral temporal cortex. It also illustrates the diagnostic value of intracerebral electrophysiological recordings and stimulation in understanding the neural basis of face recognition and visual recognition in general.
To identify the clinical determinants of occurrence of postictal generalized EEG suppression (PGES) after generalized convulsive seizures (GCS).
We reviewed the video-EEG recordings of 417 patients ...included in the REPO2MSE study, a multicenter prospective cohort study of patients with drug-resistant focal epilepsy. According to ictal semiology, we classified GCS into 3 types: tonic-clonic GCS with bilateral and symmetric tonic arm extension (type 1), clonic GCS without tonic arm extension or flexion (type 2), and GCS with unilateral or asymmetric tonic arm extension or flexion (type 3). Association between PGES and person-specific or seizure-specific variables was analyzed after correction for individual effects and the varying number of seizures.
A total of 99 GCS in 69 patients were included. Occurrence of PGES was independently associated with GCS type (p < 0.001) and lack of early administration of oxygen (p < 0.001). Odds ratio (OR) for GCS type 1 in comparison with GCS type 2 was 66.0 (95% confidence interval CI 5.4-801.6). In GCS type 1, risk of PGES was significantly increased when the seizure occurred during sleep (OR 5.0, 95% CI 1.2-20.9) and when oxygen was not administered early (OR 13.4, 95% CI 3.2-55.9).
The risk of PGES dramatically varied as a function of GCS semiologic characteristics. Whatever the type of GCS, occurrence of PGES was prevented by early administration of oxygen.
•Rare simultaneous video-intracranial EEG and transcranial electrical stimulation.•tDCS decreases amplitude spectrum and epileptogenicity index of seizure.•tDCS decreases seizure's duration and ...disabling clinical symptoms.
Mesial temporal sources are presumed to escape detection in scalp electroencephalographic recordings. This is attributed to the deep localization and infolded geometry of mesial temporal structures ...that leads to a cancellation of electrical potentials, and to the blurring effect of the superimposed neocortical background activity. In this study, we analyzed simultaneous scalp and intracerebral electroencephalographic recordings to delineate the contribution of mesial temporal sources to scalp electroencephalogram. Interictal intracerebral spike networks were classified in three distinct categories: solely mesial, mesial as well as neocortical, and solely neocortical. The highest and earliest intracerebral spikes generated by the leader source of each network were marked and the corresponding simultaneous intracerebral and scalp electroencephalograms were averaged and then characterized both in terms of amplitude and spatial distribution. In seven drug-resistant epileptic patients, 21 interictal intracerebral networks were identified: nine mesial, five mesial plus neocortical and seven neocortical. Averaged scalp spikes arising respectively from mesial, mesial plus neocortical and neocortical networks had a 7.1 (
n
= 1,949), 36.1 (
n
= 628) and 10 (
n
= 1,471) µV average amplitude. Their scalp electroencephalogram electrical field presented a negativity in the ipsilateral anterior and basal temporal electrodes in all networks and a significant positivity in the fronto-centro-parietal electrodes solely in the mesial plus neocortical and neocortical networks. Topographic consistency test proved the consistency of these different scalp electroencephalogram maps and hierarchical clustering clearly differentiated them. In our study, we have thus shown for the first time that mesial temporal sources (1) cannot be spontaneously visible (mean signal-to-noise ratio −2.1 dB) on the scalp at the single trial level and (2) contribute to scalp electroencephalogram despite their curved geometry and deep localization.
Recognizing people's identity by their faces is a key function in the human species, supported by regions of the ventral occipito‐temporal cortex (VOTC). In the last decade, there have been several ...reports of perceptual face distortion during direct electrical stimulation (DES) with subdural electrodes positioned over a well‐known face‐selective VOTC region of the right lateral middle fusiform gyrus (LatMidFG; i.e., the “Fusiform Face Area”, FFA). However, transient impairments of face identity recognition (FIR) have been extremely rare and only behaviorally quantified during DES with intracerebral (i.e., depth) electrodes in stereo‐electroencephalography (SEEG). The three detailed cases reported so far, summarized here, were specifically impaired at FIR during DES inside different anatomical VOTC regions of the right hemisphere: the inferior occipital gyrus (IOG) and the LatMidFG, as well as a region that lies at the heart of a large magnetic susceptibility artifact in functional magnetic resonance imaging (fMRI): the anterior fusiform gyrus (AntFG). In the first two regions, the eloquent electrode contacts were systematically associated with the highest face‐selective and (unfamiliar) face individuation responses as measured with intracerebral electrophysiology. Stimulation in the right AntFG did not lead to perceptual changes but also caused an inability to remember having been presented face pictures, as if the episode was never recorded in memory. These observations support the view of an extensive network of face‐selective VOTC regions subtending human FIR, with at least three critical nodes in the right hemisphere associated with differential intrinsic and extrinsic patterns of reentrant connectivity.
Face identity Recognition (FIR) is the most challenging recognition function in Humans but its critical brain regions remain unclear. Direct electrical brain stimulation studies performed with depth electrodes identified 3 right face‐selective critical regions for FIR, the inferior occipital gyrus, the middle fusiform gyrus and the fMRI “invisible” anterior fusiform gyri. Several sources of evidence show that these regions are primarily involved in visual discrimination of individual faces and associated with distinct patterns of intrinsic and extrinsic connectivity.
The temporal lobe is classically divided in two functional systems: the ventral visual pathway and the medial temporal memory system. However, their functional separation has been challenged by ...studies suggesting that the medial temporal lobe could be best understood as an extension of the hierarchically organized ventral visual pathway. Our purpose was to investigate (i) whether cerebral regions within the temporal lobe could be grouped into distinct functional assemblies, and (ii) which regions were central within these functional assemblies. We studied low intensity and low frequency electrical stimulations (0.5 mA, 1 Hz, 4 ms) performed during sixteen pre-surgical intracerebral EEG investigations in patients with medically intractable temporal or temporo-occipital lobe epilepsies. Eleven regions of interest were delineated per anatomical landmarks such as gyri and sulci. Effective connectivity based on electrophysiological feature (amplitude) of cortico-cortical evoked potentials (CCEPs) was evaluated and subjected to graph metrics. The amplitudes discriminated one medial module where the hippocampus could act as a signal amplifier. Mean amplitudes of CCEPs in regions of the temporal lobe showed a generalized Pareto distribution of probability suggesting neural synchronies to be self-organized critically. Our description of effective interactions within the temporal lobe provides a regional electrophysiological model of effective connectivity which is discussed in the context of the current hypothesis of pattern completion.
•Graph metrics applied on an effective connectivity matrix derived from CCEPs.•Detection of a medial functional module within the temporal lobe.•The anterior hippocampus is central within the temporal lobe.•The anterior hippocampus shows amplified CCEPs.
We aimed to prospectively assess the anatomical concordance of electric source localizations of interictal discharges with the epileptogenic zone (EZ) estimated by stereo-electroencephalography ...(SEEG) according to different subgroups: the type of epilepsy, the presence of a structural MRI lesion, the aetiology and the depth of the EZ.
In a prospective multicentric observational study, we enrolled 85 consecutive patients undergoing pre-surgical SEEG investigation for focal drug-resistant epilepsy. Electric source imaging (ESI) was performed before SEEG. Source localizations were obtained from dipolar and distributed source methods. Anatomical concordance between ESI and EZ was defined according to 36 predefined sublobar regions. ESI was interpreted blinded to- and subsequently compared with SEEG estimated EZ.
74 patients were finally analyzed. 38 patients had temporal and 36 extra-temporal lobe epilepsy. MRI was positive in 52. 41 patients had malformation of cortical development (MCD), 33 had another or an unknown aetiology. EZ was medial in 27, lateral in 13, and medio-lateral in 34. In the overall cohort, ESI completely or partly localized the EZ in 85%: full concordance in 13 cases and partial concordance in 50 cases. The rate of ESI full concordance with EZ was significantly higher in (i) frontal lobe epilepsy (46%;
= 0.05), (ii) cases of negative MRI (36%;
= 0.01) and (iii) MCD (27%;
= 0.03). The rate of ESI full concordance with EZ was not statistically different according to the depth of the EZ.
We prospectively demonstrated that ESI more accurately estimated the EZ in subgroups of patients who are often the most difficult cases in epilepsy surgery: frontal lobe epilepsy, negative MRI and the presence of MCD.
Face-selective regions in the human ventral occipito-temporal cortex (VOTC) have been defined for decades mainly with functional magnetic resonance imaging. This face-selective VOTC network is ...traditionally divided in a posterior ‘core’ system thought to subtend face perception, and regions of the anterior temporal lobe as a semantic memory component of an extended general system. In between these two putative systems lies the anterior fusiform gyrus and surrounding sulci, affected by magnetic susceptibility artifacts. Here we suggest that this methodological gap overlaps with and contributes to a conceptual gap between (visual) perception and semantic memory for faces. Filling this gap with intracerebral recordings and direct electrical stimulation reveals robust face-selectivity in the anterior fusiform gyrus and a crucial role of this region, especially in the right hemisphere, in identity recognition for both familiar and unfamiliar faces. Based on these observations, we propose an integrated theoretical framework for human face (identity) recognition according to which face-selective regions in the anterior fusiform gyrus join the dots between posterior and anterior cortical face memories.
•The human anterior fusiform gyrus (antFG) is affected by fMRI signal drop-out.•Intracerebral recordings show strong face-selectivity of antFG.•Direct electrical stimulation of right antFG specifically impairs face identity recognition.•The antFG is critically involved in recognizing both familiar and unfamiliar faces.•The antFG joins the dots between posterior and anterior cortical face memories.
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