Attention spotlight in V1-based cortico-cortical interactions in human visual hierarchy.

Attention is often viewed as a mental spotlight, which can be scaled like a zoom lens at specific spatial locations and features a center-surround gradient. Here, we demonstrate a neural signature of attention spotlight in signal transmission along the visual hierarchy. fMRI background connectivity analysis was performed between retinotopic V1 and downstream areas to characterize the spatial distribution of inter-areal interaction under two attentional states. We found that, compared to diffused attention, focal attention sharpened the spatial gradient in the strength of the background connectivity. Dynamic causal modeling analysis further revealed the effect of attention in both the feedback and feedforward connectivity between V1 and extrastriate cortex. In a context which induced a strong effect of crowding, the effect of attention in the background connectivity profile diminished. Our findings reveal a context-dependent attention prioritization in information transmission via modulating the recurrent processing across the early stages in human visual cortex.

Individual Brain Charting dataset extension, third release for movie watching and retinotopy data.

The Individual Brain Charting (IBC) is a multi-task functional Magnetic Resonance Imaging dataset acquired at high spatial-resolution and dedicated to the cognitive mapping of the human brain. It consists in the deep phenotyping of twelve individuals, covering a broad range of psychological domains suitable for functional-atlasing applications. Here, we present the inclusion of task data from both naturalistic stimuli and trial-based designs, to uncover structures of brain activation. We rely on the Fast Shared Response Model (FastSRM) to provide a data-driven solution for modelling naturalistic stimuli, typically containing many features. We show that data from left-out runs can be reconstructed using FastSRM, enabling the extraction of networks from the visual, auditory and language systems. We also present the topographic organization of the visual system through retinotopy. In total, six new tasks were added to IBC, wherein four trial-based retinotopic tasks contributed with a mapping of the visual field to the cortex. IBC is open access: source plus derivatives imaging data and meta-data are available in public repositories.

The large-scale organization of shape processing in the ventral and dorsal pathways is dissociable from attention.

The two visual pathways model posits that visual information is processed through two distinct cortical systems: The ventral pathway promotes visual recognition, while the dorsal pathway supports visuomotor control. Recent evidence suggests the dorsal pathway is also involved in shape processing and may contribute to object perception, but it remains unclear whether this sensitivity is independent of attentional mechanisms that were localized to overlapping cortical regions. To address this question, we conducted two fMRI experiments that utilized different parametric scrambling manipulations in which human participants viewed novel objects in different levels of scrambling and were instructed to attend to either the object or to another aspect of the image (e.g. color of the background). Univariate and multivariate analyses revealed that the large-scale organization of shape selectivity along the dorsal and ventral pathways was preserved regardless of the focus of attention. Attention did modulate shape sensitivity, but these effects were similar across the two pathways. These findings support the idea that shape processing is at least partially dissociable from attentional processes and relies on a distributed set of cortical regions across the visual pathways.

Disparate nonlinear neural dynamics measured with different techniques in macaque and human V1.

Diverse neuro-imaging techniques measure different aspects of neural responses with distinct spatial and temporal resolutions. Relating measured neural responses across different methods has been challenging. Here, we take a step towards overcoming this challenge, by comparing the nonlinearity of neural dynamics measured across methods. We used widefield voltage-sensitive dye imaging (VSDI) to measure neural population responses in macaque V1 to visual stimuli with a wide range of temporal waveforms. We found that stimulus-evoked VSDI responses are surprisingly near-additive in time. These results are qualitatively different from the strong sub-additive dynamics previously measured using fMRI and electrocorticography (ECoG) in human visual cortex with a similar set of stimuli. To test whether this discrepancy is specific to VSDI-a signal dominated by subthreshold neural activity, we repeated our measurements using widefield imaging of a genetically encoded calcium indicator (GcaMP6f)-a signal dominated by spiking activity, and found that GCaMP signals in macaque V1 are also near-additive. Therefore, the discrepancies in the extent of sub-additivity between the macaque and the human measurements are unlikely due to differences between sub- and supra-threshold neural responses. Finally, we use a simple yet flexible delayed normalization model to capture these different dynamics across measurements (with different model parameters). The model can potentially generalize to a broader set of stimuli, which aligns with previous suggestion that dynamic gain-control is a canonical computation contributing to neural processing in the brain.

Convolutional neural network models applied to neuronal responses in macaque V1 reveal limited nonlinear processing.

Computational models of the primary visual cortex (V1) have suggested that V1 neurons behave like Gabor filters followed by simple nonlinearities. However, recent work employing convolutional neural network (CNN) models has suggested that V1 relies on far more nonlinear computations than previously thought. Specifically, unit responses in an intermediate layer of VGG-19 were found to best predict macaque V1 responses to thousands of natural and synthetic images. Here, we evaluated the hypothesis that the poor performance of lower layer units in VGG-19 might be attributable to their small receptive field size rather than to their lack of complexity per se. We compared VGG-19 with AlexNet, which has much larger receptive fields in its lower layers. Whereas the best-performing layer of VGG-19 occurred after seven nonlinear steps, the first convolutional layer of AlexNet best predicted V1 responses. Although the predictive accuracy of VGG-19 was somewhat better than that of standard AlexNet, we found that a modified version of AlexNet could match the performance of VGG-19 after only a few nonlinear computations. Control analyses revealed that decreasing the size of the input images caused the best-performing layer of VGG-19 to shift to a lower layer, consistent with the hypothesis that the relationship between image size and receptive field size can strongly affect model performance. We conducted additional analyses using a Gabor pyramid model to test for nonlinear contributions of normalization and contrast saturation. Overall, our findings suggest that the feedforward responses of V1 neurons can be well explained by assuming only a few nonlinear processing stages.

The influence of electrode types to the visually induced gamma oscillations in mouse primary visual cortex.

The local field potential (LFP) is an extracellular electrical signal associated with neural ensemble input and dendritic signaling. Previous studies have linked gamma band oscillations of the LFP in cortical circuits to sensory stimuli encoding, attention, memory, and perception. Inconsistent results regarding gamma tuning for visual features were reported, but it remains unclear whether these discrepancies are due to variations in electrode properties. Specifically, the surface area and impedance of the electrode are important characteristics in LFP recording. To comprehensively address these issues, we conducted an electrophysiological study in the V1 region of lightly anesthetized mice using two types of electrodes: one with higher impedance (1 MΩ) and a sharp tip (10 µm), while the other had lower impedance (100 KΩ) but a thicker tip (200 µm). Our findings demonstrate that gamma oscillations acquired by sharp-tip electrodes were significantly stronger than those obtained from thick-tip electrodes. Regarding size tuning, most gamma power exhibited surround suppression at larger gratings when recorded from sharp-tip electrodes. However, the majority showed enhanced gamma power at larger gratings when recorded from thick-tip electrodes. Therefore, our study suggests that microelectrode parameters play a significant role in accurately recording gamma oscillations and responsive tuning to sensory stimuli.

Neuroplasticity of visual brain network induced by hypoxia.

The effects of hypoxia on brain function remain largely unknown. This study aimed to clarify this issue by visual-stimulated functional magnetic resonance imaging design. Twenty-three college students with a 30-d high-altitude exposure were tested before, 1 week and 3 months after returning to sea level. Brain functional magnetic resonance imaging and retinal electroretinogram were acquired. One week after returning to sea level, decreased blood oxygenation level dependent in the right lingual gyrus accompanied with increased blood oxygenation level dependent in the frontal cortex and insular cortex, and decreased amplitude of electroretinogram a-wave in right eye; moreover, the bilateral lingual gyri showed increased functional connectivity within the dorsal visual stream pathway, and the blood oxygenation level dependent signals in the right lingual gyrus showed positive correlation with right retinal electroretinogram a-wave. Three months after returning to sea level, the blood oxygenation level dependent signals recovered to normal level, while intensively increased blood oxygenation level dependent signals in a broad of brain regions and decreased retinal electroretinogram were also existed. In conclusion, hypoxic exposure has long-term effects on visual cortex, and the impaired retinal electroretinogram may contribute to it. The increased functional connectivity of dorsal stream may compensate for the decreased function of retinal photoreceptor cells to maintain normal visual function.

Nonuniform and pathway-specific laminar processing of spatial frequencies in the primary visual cortex of primates.

The neocortex comprises six cortical layers that play a crucial role in information processing; however, it remains unclear whether laminar processing is consistent across all regions within a single cortex. In this study, we demonstrate diverse laminar response patterns in the primary visual cortex (V1) of three male macaque monkeys when exposed to visual stimuli at different spatial frequencies (SFs). These response patterns can be categorized into two groups. One group exhibit suppressed responses in the output layers for all SFs, while the other type shows amplified responses specifically at high SFs. Further analysis suggests that both magnocellular (M) and parvocellular (P) pathways contribute to the suppressive effect through feedforward mechanisms, whereas amplification is specific to local recurrent mechanisms within the parvocellular pathway. These findings highlight the non-uniform distribution of neural mechanisms involved in laminar processing and emphasize how pathway-specific amplification selectively enhances representations of high-SF information in primate V1.

Subclinical structural atypicality of retinal thickness and its association with gray matter volume in the visual cortex of maltreated children.

Childhood maltreatment is reportedly associated with atypical gray matter structures in the primary visual cortex (V1). This study explores the hypothesis that retinal structures, the sensory organs of vision, are associated with brain atypicality and child maltreatment and examines their interrelation. General ophthalmologic examinations, visual cognitive tasks, retinal imaging, and structural magnetic resonance imaging (MRI) were conducted in children and adolescents aged 9-18 years with maltreatment experiences (CM) and typically developing (TD) children. The retinal nerve fiber layer (RNFL), the most superficial of the ten distinct retinal layers, was found to be significantly thinner in both eyes in CM. While whole-brain analysis using Voxel-based morphometry revealed a significantly larger gray matter volume (GMV) in the thalamus in CM, no significant correlation with RNFL thickness was observed. However, based on region-of-interest analysis, a thinner RNFL was associated with a larger GMV in the right V1. Although it cannot be ruled out that this outcome resulted from maltreatment alone, CM demonstrated subclinical structural atypicality in the retina, which may also correlate with the immaturity of V1 development. Examination of retinal thickness offers a novel clinical approach to capturing characteristics associated with childhood maltreatment.

Multisensory-inspired modeling and neural correlates for two key binocular interactions.

Most binocular vision models assume that the two eyes sum incompletely. However, some facilitatory cortical neurons fire for only one eye, but amplify their firing rates if both eyes are stimulated. These 'binocular gate' neurons closely resemble subthreshold multisensory neurons. Binocular amplification for binocular gate neurons follows a power law, with a compressive exponent. Unexpectedly, this rule also applies to facilitatory true binocular neurons; although driven by either eye, binocular neurons are well modeled as gated amplifiers of their strongest monocular response, if both eyes are stimulated. Psychophysical data follows the same power law as the neural data, with a similar exponent; binocular contrast sensitivity can be modeled as a gated amplification of the more sensitive eye. These results resemble gated amplification phenomena in multisensory integration, and other non-driving modulatory interactions that affect sensory processing. Models of incomplete summation seem unnecessary for V1 facilitatory neurons or contrast sensitivity. However, binocular combination of clearly visible monocular stimuli follows Schrödinger's nonlinear magnitude-weighted average. We find that putatively suppressive binocular neurons closely follow Schrödinger's equation. Similar suppressive multisensory neurons are well documented but seldom studied. Facilitatory binocular neurons and mildly suppressive binocular neurons are likely neural correlates of binocular sensitivity and binocular appearance respectively.

Atypical functional connectivity between the amygdala and visual, salience regions in infants with genetic liability for autism.

The amygdala undergoes a period of overgrowth in the first year of life, resulting in enlarged volume by 12 months in infants later diagnosed with ASD. The overgrowth of the amygdala may have functional consequences during infancy. We investigated whether amygdala connectivity differs in 12-month-olds at high likelihood (HL) for ASD (defined by having an older sibling with autism), compared to those at low likelihood (LL). We examined seed-based connectivity of left and right amygdalae, hypothesizing that the HL and LL groups would differ in amygdala connectivity, especially with the visual cortex, based on our prior reports demonstrating that components of visual circuitry develop atypically and are linked to genetic liability for autism. We found that HL infants exhibited weaker connectivity between the right amygdala and the left visual cortex, as well as between the left amygdala and the right anterior cingulate, with evidence that these patterns occur in distinct subgroups of the HL sample. Amygdala connectivity strength with the visual cortex was related to motor and communication abilities among HL infants. Findings indicate that aberrant functional connectivity between the amygdala and visual regions is apparent in infants with genetic liability for ASD and may have implications for early differences in adaptive behaviors.

An edge-simplicity bias in the visual input to young infants.

The development of sparse edge coding in the mammalian visual cortex depends on early visual experience. In humans, there are multiple indicators that the statistics of early visual experiences has unique properties that may support these developments. However, there are no direct measures of the edge statistics of infant daily-life experience. Using head-mounted cameras to capture egocentric images of young infants and adults in the home, we found infant images to have distinct edge statistics relative to adults. For infants, scenes with sparse edge patterns-few edges and few orientations-dominate. The findings implicate biased early input at the scale of daily life that is likely specific to the early months after birth and provide insights into the quality, amount, and timing of the visual experiences during the foundational developmental period for human vision.

Melanopsin-mediated amplification of cone signals in the human visual cortex.

The ambient daylight variation is coded by melanopsin photoreceptors and their luxotonic activity increases towards midday when colour temperatures are cooler, and irradiances are higher. Although melanopsin and cone photoresponses can be mediated via separate pathways, the connectivity of melanopsin cells across all levels of the retina enables them to modify cone signals. The downstream effects of melanopsin-cone interactions on human vision are however, incompletely understood. Here, we determined how the change in daytime melanopsin activation affects the human cone pathway signals in the visual cortex. A 5-primary silent-substitution method was developed to evaluate the dependence of cone-mediated signals on melanopsin activation by spectrally tuning the lights and stabilizing the rhodopsin activation under a constant cone photometric luminance. The retinal (white noise electroretinogram) and cortical responses (visual evoked potential) were simultaneously recorded with the photoreceptor-directed lights in 10 observers. By increasing the melanopsin activation, a reverse response pattern was observed with cone signals being supressed in the retina by 27% (p = 0.03) and subsequently amplified by 16% (p = 0.01) as they reach the cortex. We infer that melanopsin activity can amplify cone signals at sites distal to retinal bipolar cells to cause a decrease in the psychophysical Weber fraction for cone vision.

A user-friendly visual brain-computer interface based on high-frequency steady-state visual evoked fields recorded by OPM-MEG.

Objective. Magnetoencephalography (MEG) shares a comparable time resolution with electroencephalography. However, MEG excels in spatial resolution, enabling it to capture even the subtlest and weakest brain signals for brain-computer interfaces (BCIs). Leveraging MEG's capabilities, specifically with optically pumped magnetometers (OPM-MEG), proves to be a promising avenue for advancing MEG-BCIs, owing to its exceptional sensitivity and portability. This study harnesses the power of high-frequency steady-state visual evoked fields (SSVEFs) to build an MEG-BCI system that is flickering-imperceptible, user-friendly, and highly accurate.Approach.We have constructed a nine-command BCI that operates on high-frequency SSVEF (58-62 Hz with a 0.5 Hz interval) stimulation. We achieved this by placing the light source inside and outside the magnetic shielding room, ensuring compliance with non-magnetic and visual stimulus presentation requirements. Five participants took part in offline experiments, during which we collected six-channel multi-dimensional MEG signals along both the vertical (Z-axis) and tangential (Y-axis) components. Our approach leveraged the ensemble task-related component analysis algorithm for SSVEF identification and system performance evaluation.Main Results.The offline average accuracy of our proposed system reached an impressive 92.98% when considering multi-dimensional conjoint analysis using data from both theZandYaxes. Our method achieved a theoretical average information transfer rate (ITR) of 58.36 bits min-1with a data length of 0.7 s, and the highest individual ITR reached an impressive 63.75 bits min-1.Significance.This study marks the first exploration of high-frequency SSVEF-BCI based on OPM-MEG. These results underscore the potential and feasibility of MEG in detecting subtle brain signals, offering both theoretical insights and practical value in advancing the development and application of MEG in BCI systems.

Brain representations of motion and position in the double-drift illusion.

In the 'double-drift' illusion, local motion within a window moving in the periphery of the visual field alters the window's perceived path. The illusion is strong even when the eyes track a target whose motion matches the window so that the stimulus remains stable on the retina. This implies that the illusion involves the integration of retinal signals with non-retinal eye-movement signals. To identify where in the brain this integration occurs, we measured BOLD fMRI responses in visual cortex while subjects experienced the double-drift illusion. We then used a combination of univariate and multivariate decoding analyses to identify (1) which brain areas were sensitive to the illusion and (2) whether these brain areas contained information about the illusory stimulus trajectory. We identified a number of cortical areas that responded more strongly during the illusion than a control condition that was matched for low-level stimulus properties. Only in area hMT+ was it possible to decode the illusory trajectory. We additionally performed a number of important controls that rule out possible low-level confounds. Concurrent eye tracking confirmed that subjects accurately tracked the moving target; we were unable to decode the illusion trajectory using eye position measurements recorded during fMRI scanning, ruling out explanations based on differences in oculomotor behavior. Our results provide evidence for a perceptual representation in human visual cortex that incorporates extraretinal information.

Decision-related activity and movement selection in primate visual cortex.

Fluctuations in the activity of sensory neurons often predict perceptual decisions. This connection can be quantified with a metric called choice probability (CP), and there is a longstanding debate about whether CP reflects a causal influence on decisions or an echo of decision-making activity elsewhere in the brain. Here, we show that CP can reflect a third variable, namely, the movement used to indicate the decision. In a standard visual motion discrimination task, neurons in the middle temporal (MT) area of primate cortex responded more strongly during trials that involved a saccade toward their receptive fields. This variability accounted for much of the CP observed across the neuronal population, and it arose through training. Moreover, pharmacological inactivation of MT biased behavioral responses away from the corresponding visual field locations. These results demonstrate that training on a task with fixed sensorimotor contingencies introduces movement-related activity in sensory brain regions and that this plasticity can shape the neural circuitry of perceptual decision-making.

The execution of saccadic eye movements suppresses visual processing of both color and luminance in the early visual cortex of humans.

Our eyes execute rapid, directional movements known as saccades, occurring several times per second, to focus on objects of interest in our environment. During these movements, visual sensitivity is temporarily reduced. Despite numerous studies on this topic, the underlying mechanism remains elusive, including a lingering debate on whether saccadic suppression affects the parvocellular visual pathway. To address this issue, we conducted a study employing steady-state visual evoked potentials (SSVEPs) elicited by chromatic and luminance stimuli while observers performed saccadic eye movements. We also employed an innovative analysis pipeline to enhance the signal-to-noise ratio, yielding superior results compared to the previous method. Our findings revealed a clear suppression effect on SSVEP signals during saccades compared to fixation periods. Notably, this suppression effect was comparable for both chromatic and luminance stimuli. We went further to measure the suppression effect across various contrast levels, which enabled us to model SSVEP responses with contrast response functions. The results suggest that saccades primarily reduce response gain without significantly affecting contrast gain and that this reduction applies uniformly to both chromatic and luminance pathways. In summary, our study provides robust evidence that saccades similarly suppress visual processing in both the parvocellular and magnocellular pathways within the human early visual cortex, as indicated by SSVEP responses. The observation that saccadic eye movements impact response gain rather than contrast gain implies that they influence visual processing through a multiplicative mechanism.NEW & NOTEWORTHY The present study demonstrates that saccadic eye movements reduce the processing of both luminance and chromatic stimuli in the early visual cortex of humans. By modeling the contrast response function, the study further shows that saccades affect visual processing by reducing the response gain rather than altering the contrast gain, suggesting that a multiplicative mechanism of visual attenuation affects both parvocellular and magnocellular pathways.

Visual working memories are abstractions of percepts.

During perception, decoding the orientation of gratings depends on complex interactions between the orientation of the grating, aperture edges, and topographic structure of the visual map. Here, we aimed to test how aperture biases described during perception affect working memory (WM) decoding. For memoranda, we used gratings multiplied by radial and angular modulators to generate orthogonal aperture biases for identical orientations. Therefore, if WM representations are simply maintained sensory representations, they would have similar aperture biases. If they are abstractions of sensory features, they would be unbiased and the modulator would have no effect on orientation decoding. Neural patterns of delay period activity while maintaining the orientation of gratings with one modulator (e.g. radial) were interchangeable with patterns while maintaining gratings with the other modulator (e.g. angular) in visual and parietal cortex, suggesting that WM representations are insensitive to aperture biases during perception. Then, we visualized memory abstractions of stimuli using models of visual field map properties. Regardless of aperture biases, WM representations of both modulated gratings were recoded into a single oriented line. These results provide strong evidence that visual WM representations are abstractions of percepts, immune to perceptual aperture biases, and compel revisions of WM theory.

Training-induced changes in population receptive field properties in visual cortex: Impact of eccentric vision training on population receptive field properties and the crowding effect.

This study aimed to investigate the impact of eccentric-vision training on population receptive field (pRF) estimates to provide insights into brain plasticity processes driven by practice. Fifteen participants underwent functional magnetic resonance imaging (fMRI) measurements before and after behavioral training on a visual crowding task, where the relative orientation of the opening (gap position: up/down, left/right) in a Landolt C optotype had to be discriminated in the presence of flanking ring stimuli. Drifting checkerboard bar stimuli were used for pRF size estimation in multiple regions of interest (ROIs): dorsal-V1 (dV1), dorsal-V2 (dV2), ventral-V1 (vV1), and ventral-V2 (vV2), including the visual cortex region corresponding to the trained retinal location. pRF estimates in V1 and V2 were obtained along eccentricities from 0.5° to 9°. Statistical analyses revealed a significant decrease of the crowding anisotropy index (p = 0.009) after training, indicating improvement on crowding task performance following training. Notably, pRF sizes at and near the trained location decreased significantly (p = 0.005). Dorsal and ventral V2 exhibited significant pRF size reductions, especially at eccentricities where the training stimuli were presented (p < 0.001). In contrast, no significant changes in pRF estimates were found in either vV1 (p = 0.181) or dV1 (p = 0.055) voxels. These findings suggest that practice on a crowding task can lead to a reduction of pRF sizes in trained visual cortex, particularly in V2, highlighting the plasticity and adaptability of the adult visual system induced by prolonged training.

Diverse task-driven modeling of macaque V4 reveals functional specialization towards semantic tasks.

Responses to natural stimuli in area V4-a mid-level area of the visual ventral stream-are well predicted by features from convolutional neural networks (CNNs) trained on image classification. This result has been taken as evidence for the functional role of V4 in object classification. However, we currently do not know if and to what extent V4 plays a role in solving other computational objectives. Here, we investigated normative accounts of V4 (and V1 for comparison) by predicting macaque single-neuron responses to natural images from the representations extracted by 23 CNNs trained on different computer vision tasks including semantic, geometric, 2D, and 3D types of tasks. We found that V4 was best predicted by semantic classification features and exhibited high task selectivity, while the choice of task was less consequential to V1 performance. Consistent with traditional characterizations of V4 function that show its high-dimensional tuning to various 2D and 3D stimulus directions, we found that diverse non-semantic tasks explained aspects of V4 function that are not captured by individual semantic tasks. Nevertheless, jointly considering the features of a pair of semantic classification tasks was sufficient to yield one of our top V4 models, solidifying V4's main functional role in semantic processing and suggesting that V4's selectivity to 2D or 3D stimulus properties found by electrophysiologists can result from semantic functional goals.