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A causal role for V5/MT neurons coding motion-disparity conjunctions in resolving perceptual ambiguity
Judgments about the perceptual appearance of visual objects require the combination of multiple parameters, like location, direction, color, speed, and depth. Our understanding of perceptual judgments has been greatly informed by studies of ambiguous figures, which take on different appearances depending upon the brain state of the observer. Here we probe the neural mechanisms hypothesized as responsible for judging the apparent direction of rotation of ambiguous structure from motion (SFM) stimuli. Resolving the rotation direction of SFM cylinders requires the conjoint decoding of direction of motion and binocular depth signals [1, 2]. Within cortical visual area V5/MT of two macaque monkeys, we applied electrical stimulation at sites with consistent multiunit tuning to combinations of binocular depth and direction of motion, while the monkey made perceptual decisions about the rotation of SFM stimuli. For both ambiguous and unambiguous SFM figures, rotation judgments shifted as if we had added a specific conjunction of disparity and motion signals to the stimulus elements. This is the first causal demonstration that the activity of neurons in V5/MT contributes directly to the perception of SFM stimuli and by implication to decoding the specific conjunction of disparity and motion, the two different visual cues whose combination drives the perceptual judgment. © 2013 The Authors.
Stereoscopic Vision
The fundamental geometry underlying binocular stereoscopic depth perception was first appreciated in the mid-nineteenth century. Progress in understanding how brain mechanisms enable stereoscopic vision began about 50 years ago and has moved forward steadily since that time. The present view is that different areas of the extrastriate cortex have important and distinct roles in the elaboration of the stereoscopic visual percept. © 2009 Elsevier Ltd All rights reserved.
Human cortical responses to variations of the interocular correlation of binocular signals
The human visual system has an impressive ability to extract tiny differences from the left and right retinal images to produce the perception of depth. Moreover, the perception of depth is robust to a considerable amount of noise between the two images. Both these features of human vision contribute to the effectiveness of 3D imaging systems. Recent study of brain mechanisms for stereo has identified that there are multiple sites within the brain that respond to stereo depth, potentially implying that an effective 3D imaging system must deliver effective stimulation to multiple and differentiated brain systems. Here, we measure the neural responses of the visual cortex when tested a disparity-defined stimulus whose degree of interocular correlation was varied systematically. Neural responses were measured with functional magnetic resonance imaging (fMRI). This approach allowed us to obtain simultaneously measurements of the pattern of behavioral and neural responses to degraded binocular stimulation. Behavioral performance for the correct identification of binocular depth improved as expected with increasing degrees of binocular correlation. By comparison, the Blood Oxygen Level Dependent (BOLD) signal showed no consistent relationship with different levels of interocular correlation, although several of the visual cortical areas were strongly activated by the binocular stimuli. Preliminary analysis suggests that investigations of binocular vision that use fMRI need to adopt a multivariate approach to determine differences in neural responses to disparity-defined stimuli. © 2012 IEEE.
Responses to interocular disparity correlation in the human cerebral cortex.
PURPOSE: Perceiving binocular depth relies on the ability of our visual system to precisely match corresponding features in the left and right eyes. Yet how the human brain extracts interocular disparity correlation is poorly understood. METHODS: We used functional magnetic resonance imaging (fMRI) to characterize brain regions involved in processing interocular disparity correlation. By varying the amount of interocular correlation of a disparity-defined random-dot-stereogram, we concomitantly controlled the perception of binocular depth and measured the percent Blood-Oxygenation-Level-Dependent (%BOLD)-signal in multiple regions-of-interest in the human occipital cortex and along the intra-parietal sulcus. RESULTS: A linear support vector machine classification analysis applied to cortical responses showed patterns of activation that represented different disparity correlation levels within regions-of-interest in the visual cortex. These also revealed a positive trend between the difference in disparity correlation and classification accuracy in V1, V3 and lateral occipital cortex. Classifier performance was significantly related to behavioural performance in dorsal visual area V3. Cortical responses to random-dot-stereogram stimuli were greater in the right compared to the left hemisphere. CONCLUSIONS: Our results show that multiple regions in the cerebral cortex are sensitive to changes in interocular disparity correlation, and that dorsal area V3 may play an important role in the early transformation of binocular disparity to depth perception.
GABAergic inhibition in the human visual cortex relates to eye dominance.
Binocular vision is created by fusing the separate inputs arriving from the left and right eyes. 'Eye dominance' provides a measure of the perceptual dominance of one eye over the other. Theoretical models suggest that eye dominance is related to reciprocal inhibition between monocular units in the primary visual cortex, the first location where the binocular input is combined. As the specific inhibitory interactions in the binocular visual system critically depend on the presence of visual input, we sought to test the role of inhibition by measuring the inhibitory neurotransmitter GABA during monocular visual stimulation of the dominant and the non-dominant eye. GABA levels were measured in a single volume of interest in the early visual cortex, including V1 from both hemispheres, using a combined functional magnetic resonance imaging and magnetic resonance spectroscopy (combined fMRI-MRS) sequence on a 7-Tesla MRI scanner. Individuals with stronger eye dominance had a greater difference in GABAergic inhibition between the eyes. This relationship was present only when the visual system was actively processing sensory input and was not present at rest. We provide the first evidence that imbalances in GABA levels during ongoing sensory processing are related to eye dominance in the human visual cortex. Our finding supports the view that intracortical inhibition underlies normal eye dominance.
Correlated structure of neuronal firing in macaque visual cortex limits information for binocular depth discrimination.
Variability in cortical neural activity potentially limits sensory discriminations. Theoretical work shows that information required to discriminate two similar stimuli is limited by the correlation structure of cortical variability. We investigated these information-limiting correlations by recording simultaneously from visual cortical areas primary visual cortex (V1) and extrastriate area V4 in macaque monkeys performing a binocular, stereo depth discrimination task. Within both areas, noise correlations on a rapid temporal scale (20-30 ms) were stronger for neuron pairs with similar selectivity for binocular depth, meaning that these correlations potentially limit information for making the discrimination. Between-area correlations (V1 to V4) were different, being weaker for neuron pairs with similar tuning and having a slower temporal scale (100+ ms). Fluctuations in these information-limiting correlations just prior to the detection event were associated with changes in behavioral accuracy. Although these correlations limit the recovery of information about sensory targets, their impact may be curtailed by integrative processing of signals across multiple brain areas.NEW & NOTEWORTHY Correlated noise reduces the stimulus information in visual cortical neurons during experimental performance of binocular depth discriminations. The temporal scale of these correlations is important. Rapid (20-30 ms) correlations reduce information within and between areas V1 and V4, whereas slow (>100 ms) correlations between areas do not. Separate cortical areas appear to act together to maintain signal fidelity. Rapid correlations reduce the neuronal signal difference between stimuli and adversely affect perceptual discrimination.
Intermediate level cortical areas and the multiple roles of area V4
Despite advances in deep neural networks for object recognition, the function of the mid-level stages of visual processing in the mammalian cortex evades a simple description. This review focuses on the status of cortical area V4 to present evidence for a diversity of roles for mid-level visual areas. Some properties of V4 neurons resemble the static nature of mid-layers of neural networks when training has been completed. However, V4 also gates information flow to higher cortical areas in a dynamic way, reflecting the influences of attention, context, and reward. The most recent evidence suggests a role for mid-level cortical areas in the selective generation of responses to specific sensory inputs. The finding of signals relating to response selection in cortical areas whose role was thought to be fundamentally concerned with sensory representations will require a different approach to evaluating the roles of these areas in cognition.
Attivita corticale umana evocata dall’assegnazione di autenticita durante la fruizione di opere d’arte
Le competenze altrui hanno una grande influenza socia- le sulle nostre decisioni e sulle nostre azioni quotidiane. Buona parte del pubblico dell’arte, che si tratti di esperti o meno, è convinto che il completo apprezzamento este- tico di un’opera d’arte dipenda dalla certezza che l’opera sia autentica piuttosto che un falso. I ritratti di Rembrandt offrono un interessante set di immagini per testare tale idea, in quanto ne esistono in gran numero, molti dei qua- li giudicati come falsi o copie da recenti ricerche. L’uso di questo set di immagini ci ha consentito di distinguere la risposta cerebrale di fronte a immagini di dipinti ef- fettivamente autentici o falsi, dalla risposta cerebrale di fronte all’assegnazione esterna di autenticità dei dipinti. Attraverso risonanza magnetica funzionale abbiamo vi- sto che, l’osservazione di opere d’arte designate come “copie”, piuttosto che “autentiche”, ha evocato una ri- sposta maggiore della corteccia frontopolare (FPC) e del precuneo destro, indipendentemente dalla reale autenti- cità del dipinto. Il parere di autenticità sulle opere non ha avuto nessun effetto diretto sulla risposta ai dipinti delle aree corticali visive, ma in questo caso abbiamo osservato un’intera- zione psico-fisiologica significativa tra la FPC e l’area occipitale laterale, la quale suggerisce che tali aree visive possano essere modulate dalla FPC. Qui proponiamo che l’attivazione di un network cerebra- le, piuttosto che di una singola area, in questo paradigma sperimentale sia a sostegno del punto di vista dei ricerca- tori in campo artistico, secondo il quale i giudizi estetici sono per natura sfaccettati e multidimensionali.
Neuro-aesthetics: Is it just Brains, Beauty and Babel?
Biologists regard humans as an exceptional and unusual species: we perform and engage in a range of activities like no other animals. Language, mathematics, making art, recording history are just a few examples. With increased knowledge about the biological roots of the human species, more and more scholars in the arts and humanities have begun to ask what this knowledge means for the traditional view of the human as a person. In this chapter, I follow one thread of this discussion by examining the impact of new research in cognitive neuroscience upon our understanding of visual art. Most particularly, I review the nascent field of neuro- aesthetics and ask whether it is in any way new, whether it is relevant to the activities of art historians and how this field is likely to develop. An important aim of the chapter is to deliver recent research and conceptual developments, which are current within cognitive neuroscience, to the community of art historians and critical theorists, so that they can begin to access the burgeoning cognitive neuroscience literature for themselves. Next, I examine what elements would be required to establish a continuity between our biologically-rooted activities as human animals and our view of ourselves as free agents able to form aesthetic judgments. Questions of natural vision in comparison with the visual content of art and the nature of expert judgment and its relation to connoisseurship are addressed. Finally, it is suggested that the most productive and interesting developments will come out of focussed, multidisciplinary collaborations between groups of experts (both scientists and art historians/critical theorists), who work together on a specific domain of issues for which the outcome is agreed as significant for advancement by each disciplinary community.
Stereopsis and Depth Perception
Humans and some animals can use their two eyes in cooperation to detect and discriminate parts of the visual scene based on depth. Owing to the horizontal separation of the eyes, each eye obtains a slightly different view of the scene in front of the head. These small differences are processed by the nervous system to generate a sense of binocular depth. As humans, we experience an impression of solidity that is fully three-dimensional; this impression is called stereopsis and is what we appreciate when we watch a 3D movie or look into a stereoscopic viewer. While the basic perceptual phenomena of stereoscopic vision have been known for some time, it is mainly within the last 50 years that we have gained an understanding of how the nervous system delivers this sense of depth. This period of research began with the identification of neuronal signals for binocular depth in the primary visual cortex. Building on that finding, subsequent work has traced the signaling pathways for binocular stereoscopic depth forward into extrastriate cortex and further on into cortical areas concerning with sensorimotor integration. Within these pathways, neurons acquire sensitivity to more complex, higher order aspects of stereoscopic depth. Signals relating to the relative depth of visual features can be identified in the extrastriate cortex, which is a form of selectivity not found in the primary visual cortex. Over the same time period, knowledge of the organization of binocular vision in animals that inhabit a wide diversity of ecological niches has substantially increased. The implications of these findings for developmental and adult plasticity of the visual nervous system and onset of the clinical condition of amblyopia are explored in this article. Amblyopic vision is associated with a cluster of different visual and oculomotor symptoms, but the loss of high-quality stereoscopic depth performance is one of the consistent clinical features. Understanding where and how those losses occur in the visual brain is an important goal of current research, for both scientific and clinical reasons.
Stereoscopic vision
Stereoscopic vision describes the ability to perceive three-dimensional information from visual inputs. This article provides an overview of the history of scientific discoveries about binocular stereoscopic depth and gives an insight into our current understanding of how the primary cue for stereoscopic depth perception, called binocular disparity, is processed in the primate brain.
Relating Eye Dominance to Neurochemistry in the Human Visual Cortex Using Ultra High Field 7-Tesla MR Spectroscopy
Although our view of the world looks singular, it is combined from each eye's separate retinal image. If the balanced input between eyes is disrupted during early childhood, visual acuity and stereoscopic depth perception are impaired. This is because one eye dominates over the other, causing a neurological condition called 'amblyopia' [1]. In the normal, healthy visual system, the balance between eyes can be determined using various methods to provide a measure of 'eye dominance'. Eye dominance is the preference for using image from one eye over another [2], suggesting that the visual system applies different weights upon their input. Hence, eye dominance is relevant for understanding the mechanisms underlying binocular vision. As an investigative strategy to understand the binocular visual system in health in disease, we want to characterize eye dominance in the normal visual system. This information can then be used to serve as a baseline to compare to extreme eye dominance in 'amblyopia'. Specifically, we ask to which degree variations in eye dominance are related to visual cortex concentrations of major excitatory neurotransmitter and metabolite glutamate ('Glu') and inhibitory neurotransmitter γ-aminobutyric acid ('GABA'). Their relationship is formalised as the 'Glu/GABA' ratio. 13 participants took part in a 1-h psychophysical experiment to quantify eye dominance and a separate 1.5-h 7-Tesla MRI brain scan to measure hemodynamic and neurochemical responses during visual stimulation. The degree of eye dominance was predicted by the inter-ocular difference in V1 Glu/GABA balance. Stronger eye dominance correlated with an increase in inhibition during dominant relative to non-dominant eye viewing (r = -0.647, p = 0.023). In contrast the hemodynamic response, measured with functional magnetic resonance imaging, did not correlate with eye dominance. Our findings suggest that normally occurring eye dominance is associated with the balance of neurochemicals in the early visual cortex.
Colin Blakemore (1944-2022).
An obituary by Zoltán Molnár and Andrew Parker of neuroscientist Colin Blakemore, who made major contributions to our understanding of sensory systems and their neural plasticity, and who established a new culture of openness in science and the importance of dialogue with the general public.
Human primary visual cortex shows larger population receptive fields for binocular disparity-defined stimuli
1AbstractThe visual perception of 3D depth is underpinned by the brain’s ability to combine signals from the left and right eyes to produce a neural representation of binocular disparity for perception and behavior. Electrophysiological studies of binocular disparity over the past two decades have investigated the computational role of neurons in area V1 for binocular combination, while more recent neuroimaging investigations have focused on identifying specific roles for different extrastriate visual areas in depth perception. Here we investigate the population receptive field properties of neural responses to binocular information in striate and extrastriate cortical visual areas using ultra-high field fMRI. We measured BOLD fMRI responses while participants viewed retinotopic-mapping stimuli defined by different visual properties: contrast, luminance, motion, correlated and anti-correlated stereoscopic disparity. By fitting each condition with a population receptive field model, we compared quantitatively the size of the population receptive field for disparity-specific stimulation. We found larger population receptive fields for disparity compared with contrast and luminance in area V1, the first stage of binocular combination, which likely reflects the binocular integration zone, an interpretation supported by modelling of the binocular energy model. A similar pattern was found in region LOC, where it may reflect the role of disparity as a cue for 3D shape. These findings provide insight into the binocular receptive field properties underlying processing for human stereoscopic vision.
Finding Mutual Interest Between Neuroscience and Aesthetics: A Brush with Reality?
In the article under review in this chapter, a discussion between an art historian and neuroscientists led to a collaborative project to study the influence of authenticity on the reception of artwork. Brain-scanning with functional magnetic resonance imaging led to the identification of a number of distinct areas of the cortex that might be implicated in complex aesthetic judgments. This article provides an informal account of some of the background that led to this study.
Comparison of Neurochemical and BOLD Signal Contrast Response Functions in the Human Visual Cortex.
We investigated the relationship between neurochemical and hemodynamic responses as a function of image contrast in the human primary visual cortex (V1). Simultaneously acquired BOLD-fMRI and single voxel proton MR spectroscopy signals were measured in V1 of 24 healthy human participants of either sex at 7 tesla field strength, in response to presentations (64 s blocks) of different levels of image contrast (3%, 12.5%, 50%, 100%). Our results suggest that complementary measures of neurotransmission and energy metabolism are in partial agreement: BOLD and glutamate signals were linear with image contrast; however, a significant increase in glutamate concentration was evident only at the highest intensity level. In contrast, GABA signals were steady across all intensity levels. These results suggest that neurochemical concentrations are maintained at lower ranges of contrast levels, which match the statistics of natural vision, and that high stimulus intensity may be critical to increase sensitivity to visually modulated glutamate signals in the early visual cortex using MR spectroscopy.SIGNIFICANCE STATEMENT Glutamate and GABA are the major excitatory and inhibitory neurotransmitters of the brain. To better understand the relationship between MRS-visible neurochemicals, the BOLD signal change, and stimulus intensity, we measured combined neurochemical and BOLD signals (combined fMRI-MRS) to different image contrasts in human V1 at 7 tesla. While a linear change to contrast was present for both signals, the increase in glutamate was significant only at the highest stimulus intensity. These results suggest that hemodynamic and neurochemical signals reflect common metabolic markers of neural activity, whereas the mismatch at lower contrast levels may indicate a sensitivity threshold for detecting neurochemical changes during visual processing. Our results highlight the challenge and importance of reconciling cellular and metabolic measures of neural activity in the human brain.
Normative cerebral cortical thickness for human visual areas
1 Abstract Studies of changes in cerebral neocortical thickness often rely on small control samples for comparison with specific populations with abnormal visual systems. We present a normative dataset for FreeSurfer-derived cortical thickness across 25 human visual areas derived from 960 participants in the Human Connectome Project. Cortical thickness varies systematically across visual areas, in broad agreement with canonical visual system hierarchies in the dorsal and ventral pathways. In addition, cortical thickness estimates show consistent within-subject variability and reliability. Importantly, cortical thickness estimates in visual areas are well described by a normal distribution, making them amenable to direct statistical comparison. Highlights Normative neocortical thickness values for human visual areas measured with FreeSurfer A gradient of increasing neocortical thickness with visual area hierarchy Consistent within- and between-subject variability in neocortical thickness across visual areas
Combined fMRI-MRS acquires simultaneous glutamate and BOLD-fMRI signals in the human brain.
Combined fMRI-MRS is a novel method to non-invasively investigate functional activation in the human brain using simultaneous acquisition of hemodynamic and neurochemical measures. The aim of the current study was to quantify neural activity using combined fMRI-MRS at 7T. BOLD-fMRI and semi-LASER localization MRS data were acquired from the visual cortex of 13 participants during short blocks (64s) of flickering checkerboards. We demonstrate a correlation between glutamate and BOLD-fMRI time courses (R=0.381, p=0.031). In addition, we show increases in BOLD-fMRI (1.43±0.17%) and glutamate concentrations (0.15±0.05 I.U., ~2%) during visual stimulation. In contrast, we observed no change in glutamate concentrations in resting state MRS data during sham stimulation periods. Spectral line width changes generated by the BOLD-response were corrected using line broadening. In summary, our results establish the feasibility of concurrent measurements of BOLD-fMRI and neurochemicals using a novel combined fMRI-MRS sequence. Our findings strengthen the link between glutamate and functional activity in the human brain by demonstrating a significant correlation of BOLD-fMRI and glutamate over time, and by showing ~2% glutamate increases during 64s of visual stimulation. Our tool may become useful for studies characterizing functional dynamics between neurochemicals and hemodynamics in health and disease.