Quantification of white-matter connectivity in the ventral occipitotemporal cortex

Is vision necessary for the development of the categorical organization of the Ventral Occipito-Temporal Cortex (VOTC)? We used fMRI to characterize VOTC responses to eight categories presented acoustically in sighted and early blind individuals, and visually in a separate sighted group. We observed that VOTC reliably encodes sound categories in sighted and blind people using a representational structure and connectivity partially similar to the one found in vision. Sound categories were, however, more reliably encoded in the blind than the sighted group, using a representational format closer to the one found in vision. Crucially, VOTC in blind represents the categorical membership of sounds rather than their acoustic features. Our results suggest that sounds trigger categorical responses in the VOTC of congenitally blind and sighted people that partially match the topography and functional profile of the visual response, despite qualitative nuances in the categorical organization of VOTC between modalities and groups.

Functional neuroimaging studies consistently report that the visual perception of faces and bodies strongly activates regions within ventral occipitotemporal cortex (VOTC) and, in particular, within the mid-lateral fusiform gyrus. One unresolved issue is the degree to which faces and bodies activate discrete or overlapping cortical regions within this region. Here, we examined VOTC activity to faces and bodies at high spatial resolution, using univariate and multivariate analysis approaches sensitive to differences in both the strength and spatial pattern of activation. Faces and bodies evoked substantially overlapping activations in the fusiform gyrus when each was compared to the control category of houses. No discrete regions of activation for faces and bodies in the fusiform gyrus survived a direct statistical comparison using standard univariate statistics. However, multi-voxel pattern analysis differentiated faces and bodies in regions where univariate analysis found no significant difference in the strength of activation. Using a whole-brain multivariate searchlight approach, we also found that extensive regions in VOTC beyond those defined as fusiform face and body areas using standard criteria where the spatial pattern of activation discriminated faces and bodies. These findings provide insights into the spatial distribution of face- and body-specific activations in VOTC and the identification of functionally specialized regions.

Representational content of occipitotemporal and parietal tool areas

Review for "Person identity-specific adaptation effects in the ventral occipito-temporal cortex"

Author response for "Person identity-specific adaptation effects in the ventral occipito-temporal cortex"

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.

Neuroimaging studies have identified a network of regions in the human ventral occipito-temporal cortex (VOTC) sensitive to faces. Using intra-cerebral electrophysiological recordings, we compared the relative responsivity of the different regions to face-structure using a periodic visual stimulation paradigm. Recordings were made in 17 epileptic patients implanted with linear-array depth-electrodes (>1000 contacts in the VOTC). In Experiment 1, we presented sequences of phase-scrambled and intact face stimuli (equalised for low-level image properties) alternating at a fixed frequency of 3Hz (6 images/s) while patients completed an orthogonal task. Significant periodic EEG responses (SSVEPs) reflecting high-level face structure processing were found at 3 Hz, while responses reflecting low-level visual processing (e.g. local contrast change) were recorded at 6 Hz. An index of high-level processing (3Hz/(3Hz+6Hz)) showed a posterior-to-anterior gradient, reflecting increased sensitivity to face structure going from the occipital to the temporo-polar cortex, with a right hemisphere lateralisation. In Experiment 2, we further investigated face structure processing with a sweep VEP paradigm (Ales et al., 2012; 4/17 patients). Stimulation was similar to Experiment 1 except the visibility (phase coherence) of the face image was parametrically varied so that a face gradually emerged over the course of a sequence. The patients performed a face detection task during the trials. Responses at 3Hz, objective markers of face detection, were found in all patients on contacts in the lateral fusiform gyrus and inferior occipital gyrus that overlapped with those defined in Experiment 1. All regions showed non-linear voltage vs coherence functions at 3Hz, with thresholds lying around ≈40% coherence. Sites in the lateral fusiform gyrus had a distinct step-like response profile suggestive of categorical face detection. These findings demonstrate that face-sensitive regions are organised with a posterior-to-anterior gradient of increasingly selective high-level visual processing. These regions appear to detect face structure in a non-linear/categorical manner. Meeting abstract presented at VSS 2015.

How does sensory experience shape the development of the visual brain? To answer this eluding question, we examine brain responses to visual categories in a rare group of cataract-reversal individuals who experienced a short transient period of early blindness. Encoding of low-level visual properties is impaired in the early visual cortex (EVC) of cataract-reversal participants, whereas categorical responses in downstream ventral occipito-temporal cortex (VOTC) are preserved. In controls, degrading visual input to mimic the visual deficits of cataracts produces cascading disruptions extending from EVC to VOTC, unlike in the cataract group. A deep neural network trained on altered visual input reproduces this dissociation, supporting the brain findings. These results demonstrate that while EVC is permanently affected by early deprivation, categorical coding in VOTC shows resilience, highlighting different sensitive periods for specific brain regions and computations.

We report a comprehensive cartography of selective responses to visual letters and words in the human ventral occipito-temporal cortex (VOTC) with direct neural recordings, clarifying key aspects of the neural basis of reading. Intracerebral recordings were performed in a large group of patients (n = 37) presented with visual words inserted periodically in rapid sequences of pseudofonts, nonwords, or pseudowords, enabling classification of responses at three levels of word processing: letter, prelexical, and lexical. While letter-selective responses are found in much of the VOTC, with a higher proportion in left posterior regions, prelexical/lexical responses are confined to the middle and anterior sections of the left fusiform gyrus. This region overlaps with and extends more anteriorly than the visual word form area typically identified with functional magnetic resonance imaging. In this region, prelexical responses provide evidence for populations of neurons sensitive to the statistical regularity of letter combinations independently of lexical responses to familiar words. Despite extensive sampling in anterior ventral temporal regions, there is no hierarchical organization between prelexical and lexical responses in the left fusiform gyrus. Overall, distinct word processing levels depend on neural populations that are spatially intermingled rather than organized according to a strict postero-anterior hierarchy in the left VOTC.

The perception of a meaningful facial pattern on a nebulous stimulus-face pareidolia-is a typical human experience. Neuroimaging and electrophysiological studies have generally shown similarities in the spatio-temporal responses to typical faces and objects eliciting face pareidolia, that is, facelike objects. However, the extent to which facelike objects engage the same neural basis as human faces remains unclear. To address this issue, we used direct measures of brain activity from intracerebral electrodes implanted in the ventral occipito-temporal cortex (VOTC) of a large group of patients (n = 44). Face selectivity was determined by contrasting a large set of naturalistic face or facelike object images with non-face object categories. High signal-to-noise ratio face-selective and facelike object-selective responses were objectively identified and quantified with frequency tagging and compared in space and time throughout the VOTC. Selective activity to facelike objects was found in all key regions of the human cortical face network, extending to the previously unexplored anterior temporal lobe (ATL). Although category-selective activity was markedly reduced for facelike objects compared with human faces, consistent with previous findings, 89% of facelike object-selective contacts spatially overlapped with human face-selective contacts, while the remaining spatially scattered contacts recorded negligible responses. Furthermore, the amplitude of the two face-selective neural signals showed high correlations across regions, recording contacts and time courses as well as concurrent early onset, challenging the view that facelike objects are interpreted as faces through feedback from higher order brain regions. Together, our findings demonstrate that the pareidolic perception of face in facelike objects engages the same ventro-temporal neural circuitry, with the same temporal dynamics, as human faces.

Neural correlates of phonological, orthographic and semantic reading processing in dyslexia.

Specific regions of the human occipito-temporal cortex are consistently activated in functional imaging studies of face processing. To understand the contribution of these regions to face processing, we examined the pattern of fMRI activation in four congenital prosopagnosic (CP) individuals who are markedly impaired at face processing despite normal vision and intelligence, and with no evidence of brain damage. These individuals evinced a normal pattern of fMRI activation in the fusiform gyrus (FFA) and in other ventral occipito-temporal areas, in response to faces, buildings, and other objects, shown both as line drawings in detection and discrimination tasks and under more naturalistic testing conditions when no task was required. CP individuals also showed normal adaptation levels in a block-design adaptation experiment and, like control subjects, exhibited evidence of global face representation in the FFA. The absence of a BOLD-behavioral correlation (profound behavioral deficit, normal face-related activation in the ventral occipito-temporal cortex) challenges existing accounts of face representation, and suggests that activation in these cortical regions per se is not sufficient to ensure intact face processing.

Functional dissociation of the left ventral occipito-temporal cortex in the direct and indirect retrieval of color features

Occipitotemporal activation evoked by the perception of human bodies is modulated by the presence or absence of the face

The ability to read relies on the rapid mapping of perceived visual letters and their combinations (i.e., visual word forms) to phonology and meaning. The central role of the left ventral occipito-temporal cortex (VOTC) in processing letter strings, initially suggested by lesion studies, is now widely accepted. Although this brain region has been extensively studied with functional magnetic resonance imaging (fMRI), its causal role as a critical node of a cortical network for reading remains unclear. Here we report a comprehensive case of pure alexia during direct electrical stimulation (DES) of the left VOTC (patient SV, female, 38 yr old, implanted with intracerebral electrodes for refractory epilepsy). During DES of the left posterior occipito-temporal sulcus, but not of neighboring and remote cortical sites, SV was transiently impaired at reading single words while being able to slowly read letter-by-letter. However, SV was impaired when presenting a single letter in a rapid serial visual presentation, which showed that their letter reading is not entirely preserved. In contrast, DES to the same critical sites left performance for oral naming, auditory naming, reading numbers, writing, auditory lexical decision, and semantic matching of pictures unaffected. Intracerebral electrophysiological frequency-tagging investigations showed highly word-selective neural responses at the critical sites. These functional responses were abolished by concurrent DES, which also affected remote word-selective neural activity in the left VOTC. Altogether, these observations provide original evidence for word-selective representations of the left VOTC as a critical node of the cortical reading network.