Retinotopic and lateralized processing of spatial frequencies in human visual cortex during scene categorization.

International audienceUsing large natural scenes filtered in spatial frequencies, we aimed to demonstrate that spatial frequency processing could not only be retinotopically mapped but could also be lateralized in both hemispheres. For this purpose, participants performed a categorization task using large black and white photographs of natural scenes (indoors vs. outdoors, with a visual angle of 24° × 18°) filtered in low spatial frequencies (LSF), high spatial frequencies (HSF), and nonfiltered scenes, in block-designed fMRI recording sessions. At the group level, the comparison between the spatial frequency content of scenes revealed first that, compared with HSF, LSF scene categorization elicited activation in the anterior half of the calcarine fissures linked to the peripheral visual field, whereas, compared with LSF, HSF scene categorization elicited activation in the posterior part of the occipital lobes, which are linked to the fovea, according to the retinotopic property of visual areas. At the individual level, functional activations projected on retinotopic maps revealed that LSF processing was mapped in the anterior part of V1, whereas HSF processing was mapped in the posterior and ventral part of V2, V3, and V4. Moreover, at the group level, direct interhemispheric comparisons performed on the same fMRI data highlighted a right-sided occipito-temporal predominance for LSF processing and a left-sided temporal cortex predominance for HSF processing, in accordance with hemispheric specialization theories. By using suitable method of analysis on the same data, our results enabled us to demonstrate for the first time that spatial frequencies processing is mapped retinotopically and lateralized in human occipital cortex

Etude du traitement visuel rétinotopique des fréquences spatiales de scènes et plasticité cérébrale au cours du vieillissement normal et pathologique

Visual analysis begins with the parallel extraction of different attributes at different spatial frequencies. The aim of this thesis was to investigatethe mechanisms and the cerebral basis of spatial frequencies processing during scene categorization and their evolution during normal and pathological aging. As a first step, we performed two functional Magnetic Resonance Imaging (fMRI) studies on young adults with normal vision in order to design a retinotopic mapping tool that allows to localize cerebral activations, which is both fast and accurate (studies 1 and 2). As a second step, we studied via fMRI (study 3) the cerebral basis involved in spatial frequencies processing during scenes categorization in young adults with normal vision (study 3). We also assessedthe influence of RMS luminance contrast (“root mean square”) normalization of filtered scenes. Within the occipital cortex, we showed a retinotopic organization of spatial frequencies processing for large visual scenes. Within the occipito-temporal cortex, we showed that scenes-selective regions (the parahippocampal place area, retrosplenial cortex and occipital place area) are specifically involved in spatial frequencies processing. Also, we highlighted the factthat luminance contrast normalization changesboth the intensity and the size of cerebral activations. As a last step, we studiedspatial frequencies processing in normal and pathological aging. We first highlighted in normal aging (study 4) a specific deficit in the ability to categorize scenes with high spatial frequencies (HSF); this deficit was associated with a decrease of activation within the occipital cortex and scenes selective regions. In patients suffering from a loss in central vision due to Age-Related Macular Degeneration (AMD patients, studies 5 and 6), we showed an even more pronounced deficit of HSF processing than observed in normal aging. Interestingly, with respect to the assistance of AMD patients, we observed that increasing the contrast luminance of HSF scenes significantly improved their ability to categorize such scenes. In the end, these results allow us to better understand the neurofunctional mechanisms involved in the visual perception of scenes and to distinguish the cortical changes related to normal aging from those resulting from a visual pathology.Keywords: Visual scenes, Spatial frequencies, fMRI, Visual cortex, Retinotopy, Scene-selective regions, Normal aging, AMD.L'analyse visuelle de scènes débute par l'extraction en parallèle de différentes caractéristiques visuelles élémentaires à différentes fréquences spatiales. L'objectif de cette thèse a été de préciser les mécanismes et les bases cérébrales du traitement des fréquences spatiales lors de la catégorisation de scènes et leur évolution au cours du vieillissement normal et pathologique. Nous avons tout d'abord mené deux études en Imagerie par Résonance Magnétique fonctionnelle (IRMf) sur des adultes jeunes avec une vision normale afin de proposer un outil de cartographie rétinotopique des aires visuelles permettant une localisation fine des activations cérébrales qui soit à la fois rapide et précis (Expériences 1 et 2). Dans un second temps, nous avons étudié via IRMf les bases cérébrales du traitement des fréquences spatiales lors de la catégorisation de scènes chez de jeunes adultes avec vision normale(Expérience 3). Nous avons également étudié l'influence de la normalisation RMS (« root mean square ») du contraste de luminance des scènes filtrées. Au sein du cortex occipital, nous avons montré une organisation rétinotopique du traitement des fréquences spatiales contenues dans de larges scènes visuelles. Au sein du cortex occipito-temporal, nous avons montré que les régions sélectives aux scènes (la « parahippocampal place area », le cortex retrosplenial et l'« occipital place area ») participent de façon distincte au traitement des fréquences spatiales. Enfin, nous avons montré que la normalisation du contraste de luminance modifiait l'intensité et l'étendue des activations cérébrales. Dans un dernier temps, nous avons ensuite étudié le traitement des fréquences spatiales au cours du vieillissement normal et pathologique. Nous avons tout d'abord montré, dans le cas du vieillissement normal (Expérience 4), un déficit spécifique de la catégorisation de scènes en hautes fréquences spatiales (HFS), associé à une hypo activation du cortex occipital et des régions sélectives aux scènes. Dans le cas de la perte de la vision centrale consécutive à une dégénérescence maculaire liée à l'âge (patients DMLA, Expériences 5 et 6), nous avons mis en évidence un déficit du traitement des HFS encore plus marqué que celui observé au cours du vieillissement normal. De façon intéressante pour l'aide aux patients DMLA, l'augmentation du contraste de luminance des scènes en HFS améliorait significativement leur catégorisation des scènes en HFS. Les résultats de ces travaux nous permettent de mieux comprendre les mécanismes neuro-fonctionnels impliqués dans la perception visuelle de scènes et de différencier les changements au niveau cortical liés au vieillissement normal de ceux résultant d'une pathologie visuelle.Mots clés : Scènes visuelles, Fréquences spatiales, IRMf, Cortex visuel, Rétinotopie, Régions sélectives aux scènes, Vieillissement normal, DMLA

Visual Cortex

The neurosciences have experienced tremendous and wonderful progress in many areas, and the spectrum encompassing the neurosciences is expansive. Suffice it to mention a few classical fields: electrophysiology, genetics, physics, computer sciences, and more recently, social and marketing neurosciences. Of course, this large growth resulted in the production of many books. Perhaps the visual system and the visual cortex were in the vanguard because most animals do not produce their own light and offer thus the invaluable advantage of allowing investigators to conduct experiments in full control of the stimulus. In addition, the fascinating evolution of scientific techniques, the immense productivity of recent research, and the ensuing literature make it virtually impossible to publish in a single volume all worthwhile work accomplished throughout the scientific world. The days when a single individual, as Diderot, could undertake the production of an encyclopedia are gone forever. Indeed most approaches to studying the nervous system are valid and neuroscientists produce an almost astronomical number of interesting data accompanied by extremely worthy hypotheses which in turn generate new ventures in search of brain functions. Yet, it is fully justified to make an encore and to publish a book dedicated to visual cortex and beyond. Many reasons validate a book assembling chapters written by active researchers. Each has the opportunity to bind together data and explore original ideas whose fate will not fall into the hands of uncompromising reviewers of traditional journals. This book focuses on the cerebral cortex with a large emphasis on vision. Yet it offers the reader diverse approaches employed to investigate the brain, for instance, computer simulation, cellular responses, or rivalry between various targets and goal directed actions. This volume thus covers a large spectrum of research even though it is impossible to include all topics in the extremely diverse field of neurosciences

From Coarse to Fine? Spatial and Temporal Dynamics of Cortical Face Processing

Primary vision segregates information along 2 main dimensions: orientation and spatial frequency (SF). An important question is how this primary visual information is integrated to support high-level representations. It is generally assumed that the information carried by different SF is combined following a coarse-to-fine sequence. We directly addressed this assumption by investigating how the network of face-preferring cortical regions processes distinct SF over time. Face stimuli were flashed during 75, 150, or 300 ms and masked. They were filtered to preserve low SF (LSF), middle SF (MSF), or high SF (HSF). Most face-preferring regions robustly responded to coarse LSF, face information in early stages of visual processing (i.e., until 75 ms of exposure duration). LSF processing decayed as a function of exposure duration (mostly until 150 ms). In contrast, the processing of fine HSF, face information became more robust over time in the bilateral fusiform face regions and in the right occipital face area. The present evidence suggests the coarse-to-fine strategy as a plausible modus operandi in high-level visual cortex

The what and why of perceptual asymmetries in the visual domain

Perceptual asymmetry is one of the most important characteristics of our visual functioning. We carefully reviewed the scientific literature in order to examine such asymmetries, separating them into two major categories: within-visual field asymmetries and between-visual field asymmetries. We explain these asymmetries in terms of perceptual aspects or tasks, the what of the asymmetries; and in terms of underlying mechanisms, the why of the asymmetries. Tthe within-visual field asymmetries are fundamental to orientation, motion direction, and spatial frequency processing. between-visual field asymmetries have been reported for a wide range of perceptual phenomena. foveal dominance over the periphery, in particular, has been prominent for visual acuity, contrast sensitivity, and colour discrimination. Tthis also holds true for object or face recognition and reading performance. upper-lower visual field asymmetries in favour of the lower have been demonstrated for temporal and contrast sensitivities, visual acuity, spatial resolution, orientation, hue and motion processing. Iin contrast, the upper field advantages have been seen in visual search, apparent size, and object recognition tasks. left-right visual field asymmetries include the left field dominance in spatial (e.g., orientation) processing and the right field dominance in non-spatial (e.g., temporal) processing. left field is also better at low spatial frequency or global and coordinate spatial processing, whereas the right field is better at high spatial frequency or local and categorical spatial processing. All these asymmetries have inborn neural/physiological origins, the primary why, but can be also susceptible to visual experience, the critical why (promotes or blocks the asymmetries by altering neural functions)

Face perception: An integrative review of the role of spatial frequencies

The aim of this article is to reinterpret the results obtained from the research analyzing the role played by spatial frequencies in face perception. Two main working lines have been explored in this body of research: the critical bandwidth of spatial frequencies that allows face recognition to take place (the masking approach), and the role played by different spatial frequencies while the visual percept is being developed (the microgenetic approach). However, results obtained to date are not satisfactory in that no single explanation accounts for all the data obtained from each of the approaches. We propose that the main factor for understanding the role of spatial frequencies in face perception depends on the interaction between the demands of the task and the information in the image (the diagnostic recognition approach). Using this new framework, we review the most significant research carried out since the early 1970s to provide a reinterpretation of the data obtained

Holistic Face Categorization in Higher Order Visual Areas of the Normal and Prosopagnosic Brain: Toward a Non-Hierarchical View of Face Perception

How a visual stimulus is initially categorized as a face in a network of human brain areas remains largely unclear. Hierarchical neuro-computational models of face perception assume that the visual stimulus is first decomposed in local parts in lower order visual areas. These parts would then be combined into a global representation in higher order face-sensitive areas of the occipito-temporal cortex. Here we tested this view in fMRI with visual stimuli that are categorized as faces based on their global configuration rather than their local parts (two-tones Mooney figures and Arcimboldo's facelike paintings). Compared to the same inverted visual stimuli that are not categorized as faces, these stimuli activated the right middle fusiform gyrus (“Fusiform face area”) and superior temporal sulcus (pSTS), with no significant activation in the posteriorly located inferior occipital gyrus (i.e., no “occipital face area”). This observation is strengthened by behavioral and neural evidence for normal face categorization of these stimuli in a brain-damaged prosopagnosic patient whose intact right middle fusiform gyrus and superior temporal sulcus are devoid of any potential face-sensitive inputs from the lesioned right inferior occipital cortex. Together, these observations indicate that face-preferential activation may emerge in higher order visual areas of the right hemisphere without any face-preferential inputs from lower order visual areas, supporting a non-hierarchical view of face perception in the visual cortex

Diagnostic information use to understand brain mechanisms of facial expression categorization

Proficient categorization of facial expressions is crucial for normal social interaction. Neurophysiological, behavioural, event-related potential, lesion and functional neuroimaging techniques can be used to investigate the underlying brain mechanisms supporting this seemingly effortless process, and the associated arrangement of bilateral networks. These brain areas exhibit consistent and replicable activation patterns, and can be broadly defined to include visual (occipital and temporal), limbic (amygdala) and prefrontal (orbitofrontal) regions. Together, these areas support early perceptual processing, the formation of detailed representations and subsequent recognition of expressive faces. Despite the critical role of facial expressions in social communication and extensive work in this area, it is still not known how the brain decodes nonverbal signals in terms of expression-specific features. For these reasons, this thesis investigates the role of these so-called diagnostic facial features at three significant stages in expression recognition; the spatiotemporal inputs to the visual system, the dynamic integration of features in higher visual (occipitotemporal) areas, and early sensitivity to features in V1. In Chapter 1, the basic emotion categories are presented, along with the brain regions that are activated by these expressions. In line with this, the current cognitive theory of face processing reviews functional and anatomical dissociations within the distributed neural “face network”. Chapter 1 also introduces the way in which we measure and use diagnostic information to derive brain sensitivity to specific facial features, and how this is a useful tool by which to understand spatial and temporal organisation of expression recognition in the brain. In relation to this, hierarchical, bottom-up neural processing is discussed along with high-level, top-down facilitatory mechanisms. Chapter 2 describes an eye-movement study that reveals inputs to the visual system via fixations reflect diagnostic information use. Inputs to the visual system dictate the information distributed to cognitive systems during the seamless and rapid categorization of expressive faces. How we perform eye-movements during this task informs how task-driven and stimulus-driven mechanisms interact to guide the extraction of information supporting recognition. We recorded eye movements of observers who categorized the six basic categories of facial expressions. We use a measure of task-relevant information (diagnosticity) to discuss oculomotor behaviour, with focus on two findings. Firstly, fixated regions reveal expression differences. Secondly, by examining fixation sequences, the intersection of fixations with diagnostic information increases in a sequence of fixations. This suggests a top-down drive to acquire task-relevant information, with different functional roles for first and final fixations. A combination of psychophysical studies of visual recognition together with the EEG (electroencephalogram) signal is used to infer the dynamics of feature extraction and use during the recognition of facial expressions in Chapter 3. The results reveal a process that integrates visual information over about 50 milliseconds prior to the face-sensitive N170 event-related potential, starting at the eye region, and proceeding gradually towards lower regions. The finding that informative features for recognition are not processed simultaneously but in an orderly progression over a short time period is instructive for understanding the processes involved in visual recognition, and in particular the integration of bottom-up and top-down processes. In Chapter 4 we use fMRI to investigate the task-dependent activation to diagnostic features in early visual areas, suggesting top-down mechanisms as V1 traditionally exhibits only simple response properties. Chapter 3 revealed that diagnostic features modulate the temporal dynamics of brain signals in higher visual areas. Within the hierarchical visual system however, it is not known if an early (V1/V2/V3) sensitivity to diagnostic information contributes to categorical facial judgements, conceivably driven by top-down signals triggered in visual processing. Using retinotopic mapping, we reveal task-dependent information extraction within the earliest cortical representation (V1) of two features known to be differentially necessary for face recognition tasks (eyes and mouth). This strategic encoding of face images is beyond typical V1 properties and suggests a top-down influence of task extending down to the earliest retinotopic stages of visual processing. The significance of these data is discussed in the context of the cortical face network and bidirectional processing in the visual system. The visual cognition of facial expression processing is concerned with the interactive processing of bottom-up sensory-driven information and top-down mechanisms to relate visual input to categorical judgements. The three experiments presented in this thesis are summarized in Chapter 5 in relation to how diagnostic features can be used to explore such processing in the human brain leading to proficient facial expression categorization

“Left and right prefrontal routes to action comprehension”

Published online 20 March 2023Successful action comprehension requires the integration of motor information and semantic cues about objects in context. Previous evidence suggests that while motor features are dorsally encoded in the fronto-parietal action observation network (AON); semantic features are ventrally processed in temporal structures. Importantly, these dorsal and ventral routes seem to be preferentially tuned to low (LSF) and high (HSF) spatial frequencies, respectively. Recently, we proposed a model of action comprehension where we hypothesized an additional route to action understanding whereby coarse LSF information about objects in context is projected to the dorsal AON via the prefrontal cortex (PFC), providing a prediction signal of the most likely intention afforded by them. Yet, this model awaits for experimental testing. To this end, we used a perturb-and-measure continuous theta burst stimulation (cTBS) approach, selectively disrupting neural activity in the left and right PFC and then evaluating the participant's ability to recognize filtered action stimuli containing only HSF or LSF. We find that stimulation over PFC triggered different spatial-frequency modulations depending on lateralization: left-cTBS and right-cTBS led to poorer performance on HSF and LSF action stimuli, respectively. Our findings suggest that left and right PFC exploit distinct spatial frequencies to support action comprehension, providing evidence for multiple routes to social perception in humans.This work was supported by grants from the European Commission (MCSA-H2020-NBUCA; Grant 656881) to L.A., from the Italian Ministry of University and Research (PRIN 2017; Protocol 2017N7WCLP) to C.U., and from the Italian Ministry of Health (Ricerca Corrente 2022, Scientific Institute, IRCCS E. Medea) to A.F