Ventral Visual Pathway Research Articles

The visual ventral network is disconnected in Lewy body dementia with visual hallucinations

AbstractBackgroundVisual hallucinations (VH) are a common symptom in Lewy body dementias (LBD), which comprise dementia with Lewy bodies (DLB) and Parkinson’s disease dementia (PDD). Previous studies investigated functional brain network alteration associated with VH in different diseases. However, there is a lack of studies on VH in LBD, and a clear picture of the affected pathways is still missing. In this study, we used electroencephalography (EEG) to detect the weakened cortical connections and the functionally disconnected cortical regions in LBD with VH.MethodResting state eyes closed EEG signals (128 channels) were recorded from 45 LBD participants: 18 without VH (eight DLB) and 27 with VH (13 DLB). EEG time series were filtered (bandpass: 8‐13 Hz), and cleaned from artefacts. Magnetic resonance imaging (MRI) recordings were individually obtained with magnetisation prepared rapid gradient echo (MPRAGE) sequence, and source estimation was performed with sLORETA technique (Destrieux atlas). Connectivity was measured with weighted phase lag index (WPLI), and assessed with Network Based Statistics (NBS), including the MMSE score as covariate. Node strengths of the subnetworks detected with NBS was computed. The visual hallucination score was collected through the NPI questionnaire.ResultThe NBS revealed two subnetworks affected in VH, both comprising regions belonging to the visual ventral pathway (p<0.05, t>3.8). The first one (Figure 1) comprised connections between the right temporal lobe and the prefrontal cortex, which showed reduced strength. In the second one (Figure 2), contra‐lateral connectivity between occipital and right infra‐temporal lobe was significantly weakened.ConclusionWe propose a topography of the subnetworks affected in LBD with VH. The first and second subnetworks comprise regions involved respectively in the top‐down and bottom‐up visual perception streams. Our results resonate with the literature related to the pathology of LBD and VH. We found indeed that both affected subnetworks comprise the right inferior temporal lobe, which has been previously found to show a great burden of Lewy bodies in patients with VH. Our results support EEG as a suitable biomarker for assessing the severity of the pathology, and providing useful insights into the disease.

Spatiotemporal dynamics of orthographic and lexical processing in the ventral visual pathway.

Reading is a rapid, distributed process that engages multiple components of the ventral visual stream. To understand the neural constituents and their interactions that allow us to identify written words, we performed direct intra-cranial recordings in a large cohort of humans. This allowed us to isolate the spatiotemporal dynamics of visual word recognition across the entire left ventral occipitotemporal cortex. We found that mid-fusiform cortex is the first brain region sensitive to lexicality, preceding the traditional visual word form area. The magnitude and duration of its activation are driven by the statistics of natural language. Information regarding lexicality and word frequency propagates posteriorly from this region to visual word form regions and to earlier visual cortex, which, while active earlier, show sensitivity to words later. Further, direct electrical stimulation of this region results in reading arrest, further illustrating its crucial role in reading. This unique sensitivity of mid-fusiform cortex to sub-lexical and lexical characteristics points to its central role as the orthographic lexicon-the long-term memory representations of visual word forms.

A cell model in the ventral visual pathway for the detection of circles of curvature constituting figures

The contour of an arbitrary figure can be represented as a group of circles of curvature in contact with it, with each curvature circle represented by its center OC and radius r. We propose a series of cell models for detecting this circle, which is composed of a lateral geniculate nucleus (LGN) cell, nondirectionally selective (NDS) simple cell, and curvature-circle detection cell (CDC). The LGN and NDS simple cells were previously modeled. The CDC has been modeled as follows. Each tangent in contact with this circle is detected by an NDS simple cell that performs the Hough transformation of LGN cell responses, and then this tangent is transformed to a three-dimensional (3D) normal line in a CDC column. This transformation has been named a 3D normal-line transform. Performing this transformation for all tangents causes a CDC at the intersection of these normal lines to fire most intensively, and thus the OC and r of the circle is detected as the coordinates of this intersection. Therefore, the CDC has been modeled as this 3D normal-line transform. Based on this CDC, we model two types of constancy CDC: a position-invariant CDC and a curvature-invariant CDC. These three types of CDC reflect the response to various stimuli in actual area V4 cells. In order to validate these CDC types neurophysiologically, we propose an experimental method using microelectrodes. Cell models previously reported correspond to this hierarchy: the S1, S2, and C2 cells correspond to the NDS simple cell, CDC, and position-invariant CDC, respectively.

Early Emergence of Solid Shape Coding in Natural and Deep Network Vision

Area V4 is the first object-specific processing stage in the ventral visual pathway, just as area MT is the first motion-specific processing stage in the dorsal pathway. For almost 50 years, coding of object shape in V4 has been studied and conceived in terms of flat pattern processing, given its early position in the transformation of 2D visual images. Here, however, in awake monkey recording experiments, we found that roughly half of V4 neurons are more tuned and responsive to solid, 3D shape-in-depth, as conveyed by shading, specularity, reflection, refraction, or disparity cues in images. Using 2-photon functional microscopy, we found that flat- and solid-preferring neurons were segregated into separate modules across the surface of area V4. These findings should impact early shape-processing theories and models, which have focused on 2D pattern processing. In fact, our analyses of early object processing in AlexNet, a standard visual deep network, revealed a similar distribution of sensitivities to flat and solid shape in layer 3. Early processing of solid shape, in parallel with flat shape, could represent a computational advantage discovered by both primate brain evolution and deep-network training.

Localizing feature- and conjunction-coding in the ventral visual pathway for objects and scenes

Localizing feature- and conjunction-coding in the ventral visual pathway for objects and scenes

Resting EEG in alpha band predicts individual differences in visual size perception

Human visual size perception results from an interaction of external sensory information and internal state. The cognitive mechanisms involved in the processing of context-dependent visual size perception have been found to be innate in nature to some extent, suggesting that visual size perception might correlate with human intrinsic brain activity. Here we recorded human resting alpha activity (8–12 Hz), which is an inverse indicator of sustained alertness. Moreover, we measured an object’s perceived size in a two-alternative forced-choice manner and the Ebbinghaus illusion magnitude which is a classic illustration of context-dependent visual size perception. The results showed that alpha activity along the ventral visual pathway, including left V1, right LOC and bilateral inferior temporal gyrus, negatively correlated with an object’s perceived size. Moreover, alpha activity in the left superior temporal gyrus positively correlated with size discrimination threshold and size illusion magnitude. The findings provide clear evidence that human visual size perception scales as a function of intrinsic alertness, with higher alertness linking to larger perceived size of objects and better performance in size discrimination and size illusion tasks, and suggest that individual variation in resting-state brain activity provides a neural explanation for individual variation in cognitive performance of normal participants.

Drawing on the brain: An ALE meta-analysis of functional brain activation during drawing

Art therapy researchers and practitioners are increasingly interested in the brain mechanisms underlying art therapy, an investigation area associated with almost no neuroimaging research. Lusebrink (2010) hypothesized that expression at different levels of the Expressive Therapies Continuum (ETC) would be supported by different patterns of functional brain activation. In the current study, we tested Lusebrink’s (2010) hypotheses through an activation likelihood estimation (ALE) meta-analysis of past neuroimaging research as participants engaged in different drawing tasks. Results supported our predictions that cognitive drawing, operationalized by internally-cued drawing stimuli or objective drawing content, would be associated with activation of the prefrontal and cingulate cortices. However, results failed to support our predictions that perceptual drawing, operationalized by externally-cued drawing stimuli and nonobjective drawing content, would be associated with activation of the ventral visual pathway in the temporal lobe. Perceptual drawing was associated with cerebellum, frontal, and parietal lobe activation (including the motor and somatosensory cortices). The dorsal visual pathway, largely in the parietal lobe, was engaged during cognitive and perceptual drawing. Our findings on patterns of brain activation can inform broader neuroscientific conceptualizations of the ETC framework and future directions for art therapy research and practice.

Automatic Encoding of a View-Centered Background Image in the Macaque Temporal Lobe.

Perceptual processing along the ventral visual pathway to the hippocampus (HPC) is hypothesized to be substantiated by signal transformation from retinotopic space to relational space, which represents interrelations among constituent visual elements. However, our visual perception necessarily reflects the first person's perspective based on the retinotopic space. To investigate this two-facedness of visual perception, we compared neural activities in the temporal lobe (anterior inferotemporal cortex, perirhinal and parahippocampal cortices, and HPC) between when monkeys gazed on an object and when they fixated on the screen center with an object in their peripheral vision. We found that in addition to the spatially invariant object signal, the temporal lobe areas automatically represent a large-scale background image, which specify the subject's viewing location. These results suggest that a combination of two distinct visual signals on relational space and retinotopic space may provide the first person's perspective serving for perception and presumably subsequent episodic memory.

Mesoscopic Mapping of Stimulus-Selective Response Plasticity in the Visual Pathways Modulated by the Cholinergic System.

The cholinergic potentiation of visual conditioning enhances visual acuity and discrimination of the trained stimulus. To determine if this also induces long-term plastic changes on cortical maps and connectivity in the visual cortex and higher associative areas, mesoscopic calcium imaging was performed in head-fixed awake GCaMP6s adult mice before and after conditioning. The conditioned stimulus (0.03 cpd, 30°, 100% contrast, 1 Hz-drifting gratings) was presented 10 min daily for a week. Saline or Donepezil (DPZ, 0.3 mg/kg, s.c.), a cholinesterase inhibitor that potentiates cholinergic transmission, were injected prior to each conditioning session and compared to a sham-conditioned group. Cortical maps of resting state and evoked response to the monocular presentation of conditioned or non-conditioned stimulus (30°, 50 and 75% contrast; 90°, 50, 75, and 100% contrast) were established. Amplitude, duration, and latency of the peak response, as well as size of activation were measured in the primary visual cortex (V1), secondary visual areas (AL, A, AM, PM, LM, RL), retrosplenial cortex (RSC), and higher cortical areas. Visual stimulation increased calcium signaling in all primary and secondary visual areas, the RSC, but no other cortices. There were no significant effects of sham-conditioning or conditioning alone, but DPZ treatment during conditioning significantly decreased the integrated neuronal activity of superficial layers evoked by the conditioned stimulus in V1, AL, PM, and LM. The activity of downstream cortical areas was not changed. The size of the activated area was decreased in V1 and PM, and the signal-to-noise ratio was decreased in AL and PM. Interestingly, signal correlation was seen only between V1, the ventral visual pathway, and the RSC, and was decreased by DPZ administration. The resting state activity was slightly correlated and rarely affected by treatments, except between binocular and monocular V1 in both hemispheres. In conclusion, cholinergic potentiation of visual conditioning induced change in visual processing in the superficial cortical layers. This effect might be a key mechanism in the establishment of the fine cortical tuning in response to the conditioned visual stimulus.

Visual Functions of Primate Area V4.

Area V4-the focus of this review-is a mid-level processing stage along the ventral visual pathway of the macaque monkey. V4 is extensively interconnected with other visual cortical areas along the ventral and dorsal visual streams, with frontal cortical areas, and with several subcortical structures. Thus, it is well poised to play a broad and integrative role in visual perception and recognition-the functional domain of the ventral pathway. Neurophysiological studies in monkeys engaged in passive fixation and behavioral tasks suggest that V4 responses are dictated by tuning in a high-dimensional stimulus space defined by form, texture, color, depth, and other attributes of visual stimuli. This high-dimensional tuning may underlie the development of object-based representations in the visual cortex that are critical for tracking, recognizing, and interacting with objects. Neurophysiological and lesion studies also suggest that V4 responses are important for guiding perceptual decisions and higher-order behavior.

Artificial Neural Network Simulations of Human Learning Suggest the Presence of Metastable Attractors in Visual Memory

The attractor hypothesis states that knowledge is encoded as topologically-defined, stable configurations of connected cell assemblies. Irrespective to its original state, a network encoding new information will thus self-organize to reach the necessary stable state. To investigate memory structure, a multimodular neural network architecture, termed Magnitron, has been developed. Magnitron is a biologically-inspired cognitive architecture that simulates digit recognition. It implements perceptual input, human visual long-term memory in the ventral visual pathway and, to a lesser extent, working memory processes. To test the attractor hypothesis a Monte Carlo simulation of 10,000 individuals has been run. Each simulated learner was trained in recognizing the ten digits from novice to expert stage. The results replicate several features of human learning. First, they show that random connectivity in long-term visual memory accounts for novices’ performance. Second, the learning curves revealed that Magnitron simulates the well-known psychological power law of practice. Third, after learning took place, performance departed from chance level and reached a minimum target of 95% of correct hits; hence simulating human performance in children (i.e., when digits are learned). Magnitron also replicates biological findings. In line with research using voxel-based morphometry, Magnitron showed that matter density increases while training is taken place. Crucially, the spatial analysis of the connectivity patterns in long-term visual memory supported the hypothesis of a stable attractor. The significance of these results regarding memory theory is discussed.

Increased Dendritic Orientation Dispersion in the Left Occipital Gyrus is Associated with Atypical Visual Processing in Adults with Autism Spectrum Disorder.

In autism spectrum disorder (ASD), the complexity-specific hypothesis explains that atypical visual processing is attributable to selective functional changes in visual pathways. We investigated dendritic microstructures and their associations with functional connectivity (FC). Participants included 28 individuals with ASD and 29 typically developed persons. We explored changes in neurite orientation dispersion and density imaging (NODDI) and brain areas whose FC was significantly correlated with NODDI parameters in the explored regions of interests. Individuals with ASD showed significantly higher orientation dispersion index (ODI) values in the left occipital gyrus (OG) corresponding to the secondary visual cortex (V2). FC values between the left OG and the left middle temporal gyrus (MTG) were significantly negatively correlated with mean ODI values. The mean ODI values in the left OG were significantly positively associated with low registration of the visual quadrants of the Adolescent/Adult Sensory Profile (AASP), resulting in a significant positive correlation with passive behavioral responses of the AASP visual quadrants; additionally, the FC values between the left OG and the left MTG were significantly negatively associated with reciprocal social interaction. Our results suggest that abnormal V2 dendritic arborization is associated with atypical visual processing by altered intermediation in the ventral visual pathway.

Dissociated modulations of multivoxel activation patterns in the ventral and dorsal visual pathways by the temporal dynamics of stimuli.

IntroductionPrevious studies suggested temporal limitations of visual object identification in the ventral pathway. Moreover, multivoxel pattern analyses (MVPA) of fMRI activation have shown reliable encoding of various object categories including faces and tools in the ventral pathway. By contrast, the dorsal pathway is involved in reaching a target and grasping a tool, and quicker in processing the temporal dynamics of stimulus change. However, little is known about how activation patterns in both pathways may change according to the temporal dynamics of stimulus change.MethodsHere, we measured fMRI responses of two consecutive stimuli with varying interstimulus intervals (ISIs), and we compared how the two visual pathways respond to the dynamics of stimuli by using MVPA and information‐based searchlight mapping.ResultsWe found that the temporal dynamics of stimuli modulate responses of the two visual pathways in opposite directions. Specifically, slower temporal dynamics (longer ISIs) led to greater activity and better MVPA results in the ventral pathway. However, faster temporal dynamics (shorter ISIs) led to greater activity and better MVPA results in the dorsal pathway.ConclusionsThese results are the first to show how temporal dynamics of stimulus change modulated multivoxel fMRI activation pattern change. And such temporal dynamic response function in different ROIs along the two visual pathways may shed lights on understanding functional relationship and organization of these ROIs.

Neural representations of perceptual color experience in the human ventral visual pathway

Color is a perceptual construct that arises from neural processing in hierarchically organized cortical visual areas. Previous research, however, often failed to distinguish between neural responses driven by stimulus chromaticity versus perceptual color experience. An unsolved question is whether the neural responses at each stage of cortical processing represent a physical stimulus or a color we see. The present study dissociated the perceptual domain of color experience from the physical domain of chromatic stimulation at each stage of cortical processing by using a switch rivalry paradigm that caused the color percept to vary over time without changing the retinal stimulation. Using functional MRI (fMRI) and a model-based encoding approach, we found that neural representations in higher visual areas, such as V4 and VO1, corresponded to the perceived color, whereas responses in early visual areas V1 and V2 were modulated by the chromatic light stimulus rather than color perception. Our findings support a transition in the ascending human ventral visual pathway, from a representation of the chromatic stimulus at the retina in early visual areas to responses that correspond to perceptually experienced colors in higher visual areas.

Short-range and long-range neuronal oscillatory coupling in multiple frequency bands during face perception

Neuronal oscillatory activity has been considered to play a key role in face processing through its functional effect on information flow and exchange in human brain. Specifically, most neuronal oscillatory activity is measured in different rhythm based on the electrophysiological signal at single channel level. Although, the neuronal oscillatory coupling between neuronal assembles is associated with the information flow and exchange between brain regions, few studies focus on this type of neuronal oscillatory activity in face processing. In this study, the neuronal oscillatory coupling was investigated based on electroencephalographic (EEG) data of 20 participants, which were recorded when the participants were in a face/non-face perceptual task. The phase lag index (PLI) was used to assess the neuronal oscillatory coupling between brain regions in typical frequency bands. Enhanced short-range coupling was observed in theta (4–8 Hz) and alpha (8–12 Hz) band over the frontal region, in gamma1 (30–49 Hz) band over the left posterior and occipito-temporal regions, and in gamma2 (51–75 Hz) over the right temporal region during face perception compared with non-face perception. Long-range coupling was increased in theta and gamma band over the right hemisphere during face perception. Moreover, increased long-range coupling was observed in alpha band over the left and right hemisphere respectively during face perception. The results suggested that frequency-specific neuronal oscillatory coupling within and between regions of frontal cortex and the ventral visual pathway played an important role in face perception, which might reflect underlying neural mechanism of face perception.

Orthogonal Representations of Object Shape and Category in Deep Convolutional Neural Networks and Human Visual Cortex

Deep Convolutional Neural Networks (CNNs) are gaining traction as the benchmark model of visual object recognition, with performance now surpassing humans. While CNNs can accurately assign one image to potentially thousands of categories, network performance could be the result of layers that are tuned to represent the visual shape of objects, rather than object category, since both are often confounded in natural images. Using two stimulus sets that explicitly dissociate shape from category, we correlate these two types of information with each layer of multiple CNNs. We also compare CNN output with fMRI activation along the human visual ventral stream by correlating artificial with neural representations. We find that CNNs encode category information independently from shape, peaking at the final fully connected layer in all tested CNN architectures. Comparing CNNs with fMRI brain data, early visual cortex (V1) and early layers of CNNs encode shape information. Anterior ventral temporal cortex encodes category information, which correlates best with the final layer of CNNs. The interaction between shape and category that is found along the human visual ventral pathway is echoed in multiple deep networks. Our results suggest CNNs represent category information independently from shape, much like the human visual system.

Face-sensitive brain responses in the first year of life

Cortical areas in the ventral visual pathway become selectively tuned towards the processing of faces compared to non-face stimuli beginning around 3 months of age and continuing over the first year. Studies using event-related potentials in the EEG (ERPs) have found an ERP component, the N290, that displays specificity for human faces. Other components, such as the P1, P400, and Nc have been studied to a lesser degree in their responsiveness to human faces. However, little is known about the systematic changes in the neural responses to faces during the first year of life, and the localization of these responses in infants’ brain. We examined ERP responses to pictures of faces and objects in infants from 4.5 months through 12 months in a cross-sectional study. We investigated the activity of all the components reported to be involved in infant face processing, with particular interest to their amplitude variation and cortical localization. We identified neural regions responsible for the component through the application of cortical source localization methods. We found larger P1 and N290 responses to faces than objects, and these components were localized in the lingual and middle/posterior fusiform gyri, respectively. The amplitude of the P400 was not differentially sensitive to faces over objects. The Nc component was different for faces and objects, was influenced by the infant’s attentional state, and localized in medial-anterior brain areas. The implications of these results are discussed in the identification of developmental ERP precursors to face processing.

Effects of eccentricity on the attention-related N2pc component of the event-related potential waveform.

The N2pc ERP component has been widely used as a measure of lateralized visual attention. It is characterized by a negativity contralateral to the attended location or target, and it is thought to reflect contralaterally enhanced processing of attended information in intermediate to high levels of the ventral visual pathway. Given that the receptive fields in these areas often extend a few degrees into the ipsilateral hemifield, we might expect that near-midline stimuli would be processed by both the contralateral and ipsilateral hemispheres, resulting in a diminished N2pc. However, little is known about the effect of eccentricity on the N2pc component. To address this gap in knowledge, we recorded the EEG while participants performed a discrimination task with stimuli presented at one of five eccentricities (0°, 0.05°, 1°, 2°, 4° and 8° between the inner edge of the stimulus and the midline). We found that the N2pc amplitude remained relatively constant across eccentricities, including when the inner edge was at the midline, except that N2pc amplitude was reduced by more than 50% at the greatest eccentricity (8°). We also examined the contralateral positivity that often follows the N2pc. This positivity became progressively larger, and the transition from negative to positive occurred progressively later, as the eccentricity increased. These findings suggest that future experiments looking at the N2pc can use near-midline stimuli without compromising the N2pc amplitude, but should avoid large eccentricities. Implications about the neural generators of the N2pc are also discussed.

Enhancing multivariate pattern analysis for magnetoencephalography through relevant sensor selection

AbstractWhile the popularity of multivariate pattern classification is growing rapidly in magnetoencephalography (MEG) data analysis, the analysis pipelines used by the neuroscience community are still missing some fundamental machine‐learning techniques and principles that would increase their effectiveness. Here, we show that MEG decoding accuracy improves significantly with the addition of feature selection methods to the analysis pipeline. We compare one unsupervised and two supervised feature reduction methods in the current study. Our results show that supervised feature selection methods like statistical dependency and mutual information improve decoding performance and attain higher session‐to‐session reliability compared to unsupervised dimensionality reduction methods like principal component analysis. Furthermore, we demonstrate that the selected sensors in the data related to a visual task at each time point are consistent with the pattern reflecting the sweep of information in the ventral visual pathway.

Visuoperceptual disturbances in Parkinson's disease

IntroductionParkinson's disease (PD) shows a variety of visual deficits including visuoperceptual disturbances, however, the neural basis remains unclear. We aimed to clarify clinical and neural features of visuoperceptual disturbances in PD. MethodsThe visuospatial/perceptual abilities of ninety-six participants (48 patients with PD and 48 healthy controls) were evaluated using the subtest part 1 and 5–8 of the Visual Object and Space Perception battery (VOSP), cube/pentagon copying and clock drawing tasks. Resting-state fMRI images were acquired and analyzed the differences between PD with incomplete letters below the cut-off and above for intranetwork (primary/medial/higher visual networks) and interregional functional connectivity changes, and spectral dynamic causal modeling was performed to examine the causality. ResultsIn the PD group, position discrimination and incomplete letter scores were significantly decreased among VOSP subtests, the latter having the largest effect size. The incomplete letter scores correlated with the position discrimination while not with the dot counting, number location and cube analysis, cube/pentagon copying or clock drawing. The group with the incomplete letter scores below the cut-off had regions with decreased functional connectivity surrounding the calcarine sulcus in the primary visual network. These regions had decreased interregional functional connectivity with bilateral lingual gyri and cunei but increased with the thalamus. In this group, effective connectivity from the lingual gyrus to the calcarine sulcus was significantly decreased. ConclusionThe incomplete letters may be sensitive to detect visuoperceptual disturbances in PD. Decreased connectivity in the ventral visual feedback pathway may contribute to these deficits.