RESUMO
The amygdala is present in a diverse range of vertebrate species, such as lizards, rodents, and primates; however, its structure and connectivity differs across species. The increased connections to visual sensory areas in primate species suggests that understanding the visual selectivity of the amygdala in detail is critical to revealing the principles underlying its function in primate cognition. Therefore, we designed a high-resolution, contrast-agent enhanced, event-related fMRI experiment, and scanned 3 adult rhesus macaques, while they viewed 96 naturalistic stimuli. Half of these stimuli were social (defined by the presence of a conspecific), the other half were nonsocial. We also nested manipulations of emotional valence (positive, neutral, and negative) and visual category (faces, nonfaces, animate, and inanimate) within the stimulus set. The results reveal widespread effects of emotional valence, with the amygdala responding more on average to inanimate objects and animals than faces, bodies, or social agents in this experimental context. These findings suggest that the amygdala makes a contribution to primate vision that goes beyond an auxiliary role in face or social perception. Furthermore, the results highlight the importance of stimulus selection and experimental design when probing the function of the amygdala and other visually responsive brain regions.
Assuntos
Tonsila do Cerebelo , Macaca mulatta , Imageamento por Ressonância Magnética , Estimulação Luminosa , Animais , Tonsila do Cerebelo/fisiologia , Tonsila do Cerebelo/diagnóstico por imagem , Masculino , Estimulação Luminosa/métodos , Emoções/fisiologia , Mapeamento Encefálico , Percepção Visual/fisiologia , Feminino , Reconhecimento Visual de Modelos/fisiologiaRESUMO
Despite our fluency in reading human faces, sometimes we mistakenly perceive illusory faces in objects, a phenomenon known as face pareidolia. Although illusory faces share some neural mechanisms with real faces, it is unknown to what degree pareidolia engages higher-level social perception beyond the detection of a face. In a series of large-scale behavioral experiments (ntotal = 3,815 adults), we found that illusory faces in inanimate objects are readily perceived to have a specific emotional expression, age, and gender. Most strikingly, we observed a strong bias to perceive illusory faces as male rather than female. This male bias could not be explained by preexisting semantic or visual gender associations with the objects, or by visual features in the images. Rather, this robust bias in the perception of gender for illusory faces reveals a cognitive bias arising from a broadly tuned face evaluation system in which minimally viable face percepts are more likely to be perceived as male.
Assuntos
Face/fisiologia , Ilusões/fisiologia , Adulto , Reconhecimento Facial/fisiologia , Feminino , Humanos , Masculino , Estimulação Luminosa/métodosRESUMO
According to a prominent view in neuroscience, visual stimuli are coded by discrete cortical networks that respond preferentially to specific categories, such as faces or objects. However, it remains unclear how these category-selective networks respond when viewing conditions are cluttered, i.e., when there is more than one stimulus in the visual field. Here, we asked three questions: (1) Does clutter reduce the response and selectivity for faces as a function of retinal location? (2) Is the preferential response to faces uniform across the visual field? And (3) Does the ventral visual pathway encode information about the location of cluttered faces? We used fMRI to measure the response of the face-selective network in awake, fixating macaques (2 female, 5 male). Across a series of four experiments, we manipulated the presence and absence of clutter, as well as the location of the faces relative to the fovea. We found that clutter reduces the response to peripheral faces. When presented in isolation, without clutter, the selectivity for faces is fairly uniform across the visual field, but, when clutter is present, there is a marked decrease in the selectivity for peripheral faces. We also found no evidence of a contralateral visual field bias when faces were presented in clutter. Nonetheless, multivariate analyses revealed that the location of cluttered faces could be decoded from the multivoxel response of the face-selective network. Collectively, these findings demonstrate that clutter blunts the selectivity of the face-selective network to peripheral faces, although information about their retinal location is retained.SIGNIFICANCE STATEMENTNumerous studies that have measured brain activity in macaques have found visual regions that respond preferentially to faces. Although these regions are thought to be essential for social behavior, their responses have typically been measured while faces were presented in isolation, a situation atypical of the real world. How do these regions respond when faces are presented with other stimuli? We report that, when clutter is present, the preferential response to foveated faces is spared but preferential response to peripheral faces is reduced. Our results indicate that the presence of clutter changes the response of the face-selective network.
RESUMO
Facial expressions are vital for social communication, yet the underlying mechanisms are still being discovered. Illusory faces perceived in objects (face pareidolia) are errors of face detection that share some neural mechanisms with human face processing. However, it is unknown whether expression in illusory faces engages the same mechanisms as human faces. Here, using a serial dependence paradigm, we investigated whether illusory and human faces share a common expression mechanism. First, we found that images of face pareidolia are reliably rated for expression, within and between observers, despite varying greatly in visual features. Second, they exhibit positive serial dependence for perceived facial expression, meaning an illusory face (happy or angry) is perceived as more similar in expression to the preceding one, just as seen for human faces. This suggests illusory and human faces engage similar mechanisms of temporal continuity. Third, we found robust cross-domain serial dependence of perceived expression between illusory and human faces when they were interleaved, with serial effects larger when illusory faces preceded human faces than the reverse. Together, the results support a shared mechanism for facial expression between human faces and illusory faces and suggest that expression processing is not tightly bound to human facial features.
Assuntos
Reconhecimento Facial , Ilusões , Expressão Facial , Felicidade , HumanosRESUMO
In free-viewing experiments, primates orient preferentially toward faces and face-like stimuli. To investigate the neural basis of this behavior, we measured the spontaneous viewing preferences of monkeys with selective bilateral amygdala lesions. The results revealed that when faces and nonface objects were presented simultaneously, monkeys with amygdala lesions had no viewing preference for either conspecific faces or illusory facial features in everyday objects. Instead of directing eye movements toward socially relevant features in natural images, we found that, after amygdala loss, monkeys are biased toward features with increased low-level salience. We conclude that the amygdala has a role in our earliest specialized response to faces, a behavior thought to be a precursor for efficient social communication and essential for the development of face-selective cortex.
Assuntos
Tonsila do Cerebelo/fisiologia , Reconhecimento Visual de Modelos , Percepção Visual , Animais , Movimentos Oculares , Face , Feminino , Macaca mulatta , MasculinoRESUMO
Multivariate pattern analysis is a powerful technique; however, a significant theoretical limitation in neuroscience is the ambiguity in interpreting the source of decodable information used by classifiers. This is exemplified by the continued controversy over the source of orientation decoding from fMRI responses in human V1. Recently Carlson (2014) identified a potential source of decodable information by modeling voxel responses based on the Hubel and Wiesel (1972) ice-cube model of visual cortex. The model revealed that activity associated with the edges of gratings covaries with orientation and could potentially be used to discriminate orientation. Here we empirically evaluate whether "edge-related activity" underlies orientation decoding from patterns of BOLD response in human V1. First, we systematically mapped classifier performance as a function of stimulus location using population receptive field modeling to isolate each voxel's overlap with a large annular grating stimulus. Orientation was decodable across the stimulus; however, peak decoding performance occurred for voxels with receptive fields closer to the fovea and overlapping with the inner edge. Critically, we did not observe the expected second peak in decoding performance at the outer stimulus edge as predicted by the edge account. Second, we evaluated whether voxels that contribute most to classifier performance have receptive fields that cluster in cortical regions corresponding to the retinotopic location of the stimulus edge. Instead, we find the distribution of highly weighted voxels to be approximately random, with a modest bias toward more foveal voxels. Our results demonstrate that edge-related activity is likely not necessary for orientation decoding. SIGNIFICANCE STATEMENT: A significant theoretical limitation of multivariate pattern analysis in neuroscience is the ambiguity in interpreting the source of decodable information used by classifiers. For example, orientation can be decoded from BOLD activation patterns in human V1, even though orientation columns are at a finer spatial scale than 3T fMRI. Consequently, the source of decodable information remains controversial. Here we test the proposal that information related to the stimulus edges underlies orientation decoding. We map voxel population receptive fields in V1 and evaluate orientation decoding performance as a function of stimulus location in retinotopic cortex. We find orientation is decodable from voxels whose receptive fields do not overlap with the stimulus edges, suggesting edge-related activity does not substantially drive orientation decoding.
Assuntos
Orientação Espacial/fisiologia , Reconhecimento Visual de Modelos/fisiologia , Córtex Visual/fisiologia , Mapeamento Encefálico , Feminino , Humanos , Processamento de Imagem Assistida por Computador , Imageamento por Ressonância Magnética , Masculino , Modelos Neurológicos , Estimulação LuminosaRESUMO
Multivariate pattern analysis (MVPA) or brain decoding methods have become standard practice in analyzing fMRI data. Although decoding methods have been extensively applied in brain-computer interfaces, these methods have only recently been applied to time series neuroimaging data such as MEG and EEG to address experimental questions in cognitive neuroscience. In a tutorial style review, we describe a broad set of options to inform future time series decoding studies from a cognitive neuroscience perspective. Using example MEG data, we illustrate the effects that different options in the decoding analysis pipeline can have on experimental results where the aim is to "decode" different perceptual stimuli or cognitive states over time from dynamic brain activation patterns. We show that decisions made at both preprocessing (e.g., dimensionality reduction, subsampling, trial averaging) and decoding (e.g., classifier selection, cross-validation design) stages of the analysis can significantly affect the results. In addition to standard decoding, we describe extensions to MVPA for time-varying neuroimaging data including representational similarity analysis, temporal generalization, and the interpretation of classifier weight maps. Finally, we outline important caveats in the design and interpretation of time series decoding experiments.
Assuntos
Encéfalo/fisiologia , Potenciais Evocados/fisiologia , Neuroimagem Funcional/métodos , Magnetoencefalografia/métodos , Análise Multivariada , Processamento de Sinais Assistido por Computador , HumanosRESUMO
Animacy is a robust organizing principle among object category representations in the human brain. Using multivariate pattern analysis methods, it has been shown that distance to the decision boundary of a classifier trained to discriminate neural activation patterns for animate and inanimate objects correlates with observer RTs for the same animacy categorization task [Ritchie, J. B., Tovar, D. A., & Carlson, T. A. Emerging object representations in the visual system predict reaction times for categorization. PLoS Computational Biology, 11, e1004316, 2015; Carlson, T. A., Ritchie, J. B., Kriegeskorte, N., Durvasula, S., & Ma, J. Reaction time for object categorization is predicted by representational distance. Journal of Cognitive Neuroscience, 26, 132-142, 2014]. Using MEG decoding, we tested if the same relationship holds when a stimulus manipulation (degradation) increases task difficulty, which we predicted would systematically decrease the distance of activation patterns from the decision boundary and increase RTs. In addition, we tested whether distance to the classifier boundary correlates with drift rates in the linear ballistic accumulator [Brown, S. D., & Heathcote, A. The simplest complete model of choice response time: Linear ballistic accumulation. Cognitive Psychology, 57, 153-178, 2008]. We found that distance to the classifier boundary correlated with RT, accuracy, and drift rates in an animacy categorization task. Split by animacy, the correlations between brain and behavior were sustained longer over the time course for animate than for inanimate stimuli. Interestingly, when examining the distance to the classifier boundary during the peak correlation between brain and behavior, we found that only degraded versions of animate, but not inanimate, objects had systematically shifted toward the classifier decision boundary as predicted. Our results support an asymmetry in the representation of animate and inanimate object categories in the human brain.
Assuntos
Encéfalo/fisiologia , Reconhecimento Visual de Modelos/fisiologia , Percepção Espacial/fisiologia , Adulto , Análise de Variância , Comportamento de Escolha/fisiologia , Feminino , Humanos , Julgamento/fisiologia , Magnetoencefalografia , Masculino , Testes Neuropsicológicos , Estimulação Luminosa , Tempo de Reação , Processamento de Sinais Assistido por ComputadorRESUMO
Perceptual similarity is a cognitive judgment that represents the end-stage of a complex cascade of hierarchical processing throughout visual cortex. Previous studies have shown a correspondence between the similarity of coarse-scale fMRI activation patterns and the perceived similarity of visual stimuli, suggesting that visual objects that appear similar also share similar underlying patterns of neural activation. Here we explore the temporal relationship between the human brain's time-varying representation of visual patterns and behavioral judgments of perceptual similarity. The visual stimuli were abstract patterns constructed from identical perceptual units (oriented Gabor patches) so that each pattern had a unique global form or perceptual 'Gestalt'. The visual stimuli were decodable from evoked neural activation patterns measured with magnetoencephalography (MEG), however, stimuli differed in the similarity of their neural representation as estimated by differences in decodability. Early after stimulus onset (from 50ms), a model based on retinotopic organization predicted the representational similarity of the visual stimuli. Following the peak correlation between the retinotopic model and neural data at 80ms, the neural representations quickly evolved so that retinotopy no longer provided a sufficient account of the brain's time-varying representation of the stimuli. Overall the strongest predictor of the brain's representation was a model based on human judgments of perceptual similarity, which reached the limits of the maximum correlation with the neural data defined by the 'noise ceiling'. Our results show that large-scale brain activation patterns contain a neural signature for the perceptual Gestalt of composite visual features, and demonstrate a strong correspondence between perception and complex patterns of brain activity.
Assuntos
Encéfalo/fisiologia , Julgamento/fisiologia , Reconhecimento Visual de Modelos/fisiologia , Adulto , Feminino , Humanos , Magnetoencefalografia , Masculino , Estimulação Luminosa , Adulto JovemRESUMO
Perceived stereoscopic slant around a vertical axis is strongly underestimated for isolated surfaces, suggesting that neither uniocular image compression nor linear gradients of absolute disparity are very effective cues. However, slant increases to a level close to geometric prediction if gradients of relative disparity are introduced, for example by placing flanking frontal-parallel surfaces at the horizontal boundaries of the slanted surface. Here we examine the mechanisms underlying this slant enhancement by manipulating properties of the slanted surface or the flanking surfaces. Perceived slant was measured using a probe bias method. In Experiment 1, an outlined surface and a randomly textured surface showed similar slant underestimation when presented in isolation, but the enhancement in slant produced by flankers was significantly greater for the textured surface. In Experiment 2, we degraded the relative disparity gradient by (a) reducing overall texture density, (b) reducing flanker width, or (c) adding disparity noise to the flankers. Density had no effect while adding noise to the flankers, or reducing their width significantly decreased perceived slant of the central surface. These results support the view that the enhancement of slant produced by adding flanking surfaces is attributable to the presence of a relative disparity gradient and that the flanker effect can spread to regions of the surface not directly above or below the gradient.
Assuntos
Percepção de Profundidade/fisiologia , Disparidade Visual/fisiologia , Sinais (Psicologia) , Percepção de Forma , Humanos , Ilusões Ópticas , OrientaçãoRESUMO
Multivariate pattern analysis (MVPA) has become an increasingly popular approach to fMRI research because these methods offer the attractive possibility of "decoding" the content of brain representations. One weakness of MVPA is that the source of decodable information is not always apparent, as evidenced by the ongoing debate about orientation decoding in human visual cortex. In a recent study (Carlson, 2014), we used an unbiased model of visual cortex to reveal a new source of decodable information that may account for orientation decoding. Clifford and Mannion (2015) take issue with the model's capacity to decode spiral sense. Here, we discuss their findings in the context of the ongoing debate on orientation decoding and further highlight the limitations of using MVPA to infer the content of brain representations.
Assuntos
Encéfalo/fisiologia , Processamento de Imagem Assistida por Computador/métodos , Imageamento por Ressonância Magnética/métodos , Análise Multivariada , Mapeamento Encefálico/métodos , Humanos , Modelos Neurológicos , Córtex Visual/fisiologiaRESUMO
Motion in depth can be perceived from binocular cues alone, yet it is unclear whether these cues support speed sensitivity in the absence of the monocular cues that normally co-occur in natural viewing. We measure threshold contours in space-time for the discrimination of three-dimensional (3D) motion to determine whether observers use speed to discriminate a test 3D motion from two identical standards. We compare thresholds for random-dot stereograms (RDS) containing both binocular cues to 3D motion-interocular velocity difference and changing disparity over time-with performance for dynamic random-dot stereograms (DRDS), which contain only the second cue. Threshold contours are tilted along the axis of constant velocity in space-time for RDS stimuli at slow speeds (0.5 m/s), evidence for speed sensitivity. However, for higher speeds (1.5 m/s) and DRDS stimuli, observers rely on the component cues of duration and disparity. In a second experiment, noise of constant velocity is added to the standards to degrade the reliability of these separate components. Again there is evidence for speed tuning for RDS, but not for DRDS. Considerable variation is observed in the ability of individual observers to use the different cues in both experiments, however, in general the results emphasize the importance of interocular velocity difference as a critical cue for speed sensitivity to motion in depth, and suggest that speed sensitivity to stereomotion from binocular cues is restricted to relatively slow speeds.
Assuntos
Sinais (Psicologia) , Percepção de Profundidade/fisiologia , Percepção de Forma/fisiologia , Movimento (Física) , Limiar Sensorial , Disparidade Visual/fisiologia , Visão Binocular/fisiologia , HumanosRESUMO
In binocular viewing of natural three-dimensional scenes, occlusion relationships between objects at different depths create regions of the background that are visible to only one eye. These monocular regions can support depth perception. There are two viewing conditions in which a monocular region can be on the nasal side of a binocular surface--(a) when a background surface is viewed through an aperture and (b) when a region is camouflaged against the background in one eye's view. We created stimuli with a monocular region using complex textures in which camouflage was not possible, and for which there was no physical aperture. For these stimuli, observers perceived a strong phantom contour in near depth at the edge of the monocular region, with the monocular texture perceived behind at the depth of the binocular surface. Depth-matching with a probe showed that the depth of the phantom occluding surface was as precise as for stimuli with regular binocular disparity. Monocular regions of texture on the opposite (temporal) side of the binocular surface were perceived behind, as predicted by occlusion geometry, and there was no phantom surface. We discuss the implications for models of da Vinci stereopsis and stereoscopic edge processing, and consider the involvement of a form of Panum's limiting case. We conclude that the visual system uses a combination of occlusion geometry and complex matching to precisely locate edges in depth that lack a luminance contour.
Assuntos
Percepção de Profundidade/fisiologia , Percepção de Forma/fisiologia , Imagens de Fantasmas , Disparidade Visual/fisiologia , Visão Binocular/fisiologia , Visão Monocular/fisiologia , Humanos , MasculinoRESUMO
The recall and visualization of people and places from memory is an everyday occurrence, yet the neural mechanisms underpinning this phenomenon are not well understood. In particular, the temporal characteristics of the internal representations generated by active recall are unclear. Here, we used magnetoencephalography (MEG) and multivariate pattern analysis to measure the evolving neural representation of familiar places and people across the whole brain when human participants engage in active recall. To isolate self-generated imagined representations, we used a retro-cue paradigm in which participants were first presented with two possible labels before being cued to recall either the first or second item. We collected personalized labels for specific locations and people familiar to each participant. Importantly, no visual stimuli were presented during the recall period, and the retro-cue paradigm allowed the dissociation of responses associated with the labels from those corresponding to the self-generated representations. First, we found that following the retro-cue it took on average â¼1000 ms for distinct neural representations of freely recalled people or places to develop. Second, we found distinct representations of personally familiar concepts throughout the 4 s recall period. Finally, we found that these representations were highly stable and generalizable across time. These results suggest that self-generated visualizations and recall of familiar places and people are subserved by a stable neural mechanism that operates relatively slowly when under conscious control.
Assuntos
Sinais (Psicologia) , Rememoração Mental , Humanos , Rememoração Mental/fisiologia , Encéfalo/fisiologia , Mapeamento Encefálico , MagnetoencefalografiaRESUMO
Face pareidolia is the experience of seeing illusory faces in inanimate objects. While children experience face pareidolia, it is unknown whether they perceive gender in illusory faces, as their face evaluation system is still developing in the first decade of life. In a sample of 412 children and adults from 4 to 80 years of age we found that like adults, children perceived many illusory faces in objects to have a gender and had a strong bias to see them as male rather than female, regardless of their own gender identification. These results provide evidence that the male bias for face pareidolia emerges early in life, even before the ability to discriminate gender from facial cues alone is fully developed. Further, the existence of a male bias in children suggests that any social context that elicits the cognitive bias to see faces as male has remained relatively consistent across generations.
Assuntos
Face , Ilusões , Adulto , Humanos , Masculino , Criança , Feminino , Ilusões/psicologiaRESUMO
It is well-established that depth discrimination is finer in the fovea than the periphery. Here, we study the decline in depth discrimination thresholds with distance from the fovea using an equivalent noise analysis to separate the contributions of internal noise and sampling efficiency. Observers discriminated the mean depth of patches of "dead leaves" composed of ellipses varying in size, orientation, and luminance at varying levels of disparity noise between 0.05 and 13.56 arcmin and visual field locations between 0° and 9° eccentricity. At low levels of disparity noise, depth discrimination thresholds were lower in the fovea than in the periphery. At higher noise levels (above 3.39 arcmin), thresholds converged, and there was little difference between foveal and peripheral depth discrimination. The parameters estimated from the equivalent noise model indicate that an increase in internal noise is the limiting factor in peripheral depth discrimination with no decline in sampling efficiency. Sampling efficiency was uniformly low across the visual field. The results indicate that a loss of precision of local disparity estimates early in visual processing limits fine depth discrimination in the periphery.
Assuntos
Percepção de Profundidade/fisiologia , Discriminação Psicológica/fisiologia , Fóvea Central/fisiologia , Campos Visuais/fisiologia , Artefatos , Humanos , Estimulação Luminosa/métodos , Limiar Sensorial/fisiologiaRESUMO
Face detection is a foundational social skill for primates. This vital function is thought to be supported by specialized neural mechanisms; however, although several face-selective regions have been identified in both humans and nonhuman primates, there is no consensus about which region(s) are involved in face detection. Here, we used naturally occurring errors of face detection (i.e. objects with illusory facial features referred to as examples of 'face pareidolia') to identify regions of the macaque brain implicated in face detection. Using whole-brain functional magnetic resonance imaging to test awake rhesus macaques, we discovered that a subset of face-selective patches in the inferior temporal cortex, on the lower lateral edge of the superior temporal sulcus, and the amygdala respond more to objects with illusory facial features than matched non-face objects. Multivariate analyses of the data revealed differences in the representation of illusory faces across the functionally defined regions of interest. These differences suggest that the cortical and subcortical face-selective regions contribute uniquely to the detection of facial features. We conclude that face detection is supported by a multiplexed system in the primate brain.
Assuntos
Mapeamento Encefálico , Ilusões , Animais , Humanos , Reconhecimento Visual de Modelos , Macaca mulatta , Imageamento por Ressonância Magnética/métodos , Lobo TemporalRESUMO
Behavioural categorisation reaction times (RTs) provide a useful way to link behaviour to brain representations measured with neuroimaging. In this framework, objects are assumed to be represented in a multidimensional activation space, with the distances between object representations indicating their degree of neural similarity. Faster RTs have been reported to correlate with greater distances from a classification decision boundary for animacy. Objects inherently belong to more than one category, yet it is not known whether the RT-distance relationship, and its evolution over the time-course of the neural response, is similar across different categories. Here we used magnetoencephalography (MEG) to address this question. Our stimuli included typically animate and inanimate objects, as well as more ambiguous examples (i.e., robots and toys). We conducted four semantic categorisation tasks on the same stimulus set assessing animacy, living, moving, and human-similarity concepts, and linked the categorisation RTs to MEG time-series decoding data. Our results show a sustained RT-distance relationship throughout the time course of object processing for not only animacy, but also categorisation according to human-similarity. Interestingly, this sustained RT-distance relationship was not observed for the living and moving category organisations, despite comparable classification accuracy of the MEG data across all four category organisations. Our findings show that behavioural RTs predict representational distance for an organisational principle other than animacy, however further research is needed to determine why this relationship is observed only for some category organisations and not others.
Assuntos
Magnetoencefalografia , Reconhecimento Visual de Modelos , Encéfalo/diagnóstico por imagem , Mapeamento Encefálico , Humanos , Neuroimagem , Tempo de ReaçãoRESUMO
Face detection is a priority of both the human and primate visual system. However, occasionally we misperceive faces in inanimate objects -- "face pareidolia". A key feature of these 'false positives' is that face perception occurs in the absence of visual features typical of real faces. Human faces are known to be located faster than objects in visual search. Here we used a visual search paradigm to test whether illusory faces share this advantage. Search times were faster for illusory faces than for matched objects amongst both matched (Experiment 1) and diverse (Experiment 2) distractors, however search times for real human faces were faster and more efficient than objects with or without an illusory face. Importantly, this result indicates that illusory faces are processed quickly enough by the human brain to confer a visual search advantage, suggesting the engagement of a broadly-tuned mechanism that facilitates rapid face detection in cluttered environments.