Temporal dynamics of short-term neural adaptation across human visual cortex.

Neural responses in visual cortex adapt to prolonged and repeated stimuli. While adaptation occurs across the visual cortex, it is unclear how adaptation patterns and computational mechanisms differ across the visual hierarchy. Here we characterize two signatures of short-term neural adaptation in time-varying intracranial electroencephalography (iEEG) data collected while participants viewed naturalistic image categories varying in duration and repetition interval. Ventral- and lateral-occipitotemporal cortex exhibit slower and prolonged adaptation to single stimuli and slower recovery from adaptation to repeated stimuli compared to V1-V3. For category-selective electrodes, recovery from adaptation is slower for preferred than non-preferred stimuli. To model neural adaptation we augment our delayed divisive normalization (DN) model by scaling the input strength as a function of stimulus category, enabling the model to accurately predict neural responses across multiple image categories. The model fits suggest that differences in adaptation patterns arise from slower normalization dynamics in higher visual areas interacting with differences in input strength resulting from category selectivity. Our results reveal systematic differences in temporal adaptation of neural population responses between lower and higher visual brain areas and show that a single computational model of history-dependent normalization dynamics, fit with area-specific parameters, accounts for these differences.

Normalization by orientation-tuned surround in human V1-V3.

An influential account of neuronal responses in primary visual cortex is the normalized energy model. This model is often implemented as a multi-stage computation. The first stage is linear filtering. The second stage is the extraction of contrast energy, whereby a complex cell computes the squared and summed outputs of a pair of the linear filters in quadrature phase. The third stage is normalization, in which a local population of complex cells mutually inhibit one another. Because the population includes cells tuned to a range of orientations and spatial frequencies, the result is that the responses are effectively normalized by the local stimulus contrast. Here, using evidence from human functional MRI, we show that the classical model fails to account for the relative responses to two classes of stimuli: straight, parallel, band-passed contours (gratings), and curved, band-passed contours (snakes). The snakes elicit fMRI responses that are about twice as large as the gratings, yet a traditional divisive normalization model predicts responses that are about the same. Motivated by these observations and others from the literature, we implement a divisive normalization model in which cells matched in orientation tuning ("tuned normalization") preferentially inhibit each other. We first show that this model accounts for differential responses to these two classes of stimuli. We then show that the model successfully generalizes to other band-pass textures, both in V1 and in extrastriate cortex (V2 and V3). We conclude that even in primary visual cortex, complex features of images such as the degree of heterogeneity, can have large effects on neural responses.

Structural covariance and heritability of the optic tract and primary visual cortex in living human brains.

Individual differences among human brains exist at many scales, spanning gene expression, white matter tissue properties, and the size and shape of cortical areas. One notable example is an approximately 3-fold range in the size of human primary visual cortex (V1), a much larger range than is found in overall brain size. A previous study (Andrews et al., 1997) reported a correlation between optic tract cross-section area and V1 size in post-mortem human brains, suggesting that there may be a common developmental mechanism for multiple components of the visual pathways. We evaluated the relationship between properties of the optic tract and V1 in a much larger sample of living human brains by analyzing the Human Connectome Project 7 Tesla Retinotopy Dataset (including 107 females and 71 males). This dataset includes retinotopic maps measured with functional MRI (fMRI) and fiber tract data measured with diffusion MRI (dMRI). We found a negative correlation between optic tract fractional anisotropy and V1 surface area (r = -0.19). This correlation, though small, was consistent across multiple dMRI datasets differing in acquisition parameters. Further, we found that both V1 size and optic tract properties were correlated among twins, with higher correlations for monozygotic than dizygotic twins, indicating a high degree of heritability for both properties. Together, these results demonstrate covariation across individuals in properties of the retina (optic tract) and cortex (V1) and show that each is influenced by genetic factors.SIGNIFICANCE STATEMENT:The size of human primary visual cortex (V1) has large inter-individual differences. These differences do not scale with overall brain size. A previous post-mortem study reported a correlation between the size of the human optic tract and V1. In this study, we evaluated the relationship between the optic tract and V1 in living humans by analyzing a neuroimaging dataset that included functional and diffusion MRI data. We found a small, but robust correlation between optic tract tissue properties and V1 size, supporting the existence of structural covariance between the optic tract and V1 in living humans. The results suggest that characteristics of retinal ganglion cells, reflected in optic tract measurements, are related to individual differences in human V1.

Non-neural factors influencing BOLD response magnitudes within individual subjects.

To what extent is the size of the blood-oxygen-level-dependent (BOLD) response influenced by factors other than neural activity? In a re-analysis of three neuroimaging datasets (male and female human participants), we find large systematic inhomogeneities in the BOLD response magnitude in primary visual cortex (V1): stimulus-evoked BOLD responses, expressed in units of percent signal change, are up to 50% larger along the representation of the horizontal meridian than the vertical meridian. To assess whether this surprising effect can be interpreted as differences in local neural activity, we quantified several factors that potentially contribute to the size of the BOLD response. We find relationships between BOLD response magnitude and cortical thickness, curvature, depth and macrovasculature. These relationships are consistently found across subjects and datasets and suggest that variation in BOLD response magnitudes across cortical locations reflects, in part, differences in anatomy and vascularization. To compensate for these factors, we implement a regression-based correction method and show that after correction, BOLD responses become more homogeneous across V1. The correction reduces the horizontal/vertical difference by about half, indicating that some of the difference is likely not due to neural activity differences. We conclude that interpretation of variation in BOLD response magnitude across cortical locations should consider the influence of the potential confounding factors of thickness, curvature, depth and vascularization.SIGNIFICANCE STATEMENTThe magnitude of the BOLD signal is often used as a surrogate of neural activity, but the exact factors that contribute to its strength have not been studied on a voxel-wise level. Here, we examined several anatomical and measurement-related factors to assess their relationship with BOLD signal magnitude. We find that BOLD magnitude correlates with cortical anatomy, depth and macrovasculature. To remove the contribution of these factors, we propose a simple, data-driven correction method that can be used in any functional magnetic resonance imaging (fMRI) experiment. After accounting for the confounding factors, BOLD magnitude becomes more spatially homogenous. Our correction method improves the ability to make more accurate inferences about local neural activity from fMRI data.

Variability of the Surface Area of the V1, V2, and V3 Maps in a Large Sample of Human Observers.

How variable is the functionally defined structure of early visual areas in human cortex and how much variability is shared between twins? Here we quantify individual differences in the best understood functionally defined regions of cortex: V1, V2, V3. The Human Connectome Project 7T Retinotopy Dataset includes retinotopic measurements from 181 subjects (109 female, 72 male), including many twins. We trained four "anatomists" to manually define V1-V3 using retinotopic features. These definitions were more accurate than automated anatomical templates and showed that surface areas for these maps varied more than threefold across individuals. This threefold variation was little changed when normalizing visual area size by the surface area of the entire cerebral cortex. In addition to varying in size, we find that visual areas vary in how they sample the visual field. Specifically, the cortical magnification function differed substantially among individuals, with the relative amount of cortex devoted to central vision varying by more than a factor of 2. To complement the variability analysis, we examined the similarity of visual area size and structure across twins. Whereas the twin sample sizes are too small to make precise heritability estimates (50 monozygotic pairs, 34 dizygotic pairs), they nonetheless reveal high correlations, consistent with strong effects of the combination of shared genes and environment on visual area size. Collectively, these results provide the most comprehensive account of individual variability in visual area structure to date, and provide a robust population benchmark against which new individuals and developmental and clinical populations can be compared.SIGNIFICANCE STATEMENT Areas V1, V2, and V3 are among the best studied functionally defined regions in human cortex. Using the largest retinotopy dataset to date, we characterized the variability of these regions across individuals and the similarity between twin pairs. We find that the size of visual areas varies dramatically (up to 3.5×) across healthy young adults, far more than the variability of the cerebral cortex size as a whole. Much of this variability appears to arise from inherited factors, as we find very high correlations in visual area size between monozygotic twin pairs, and lower but still substantial correlations between dizygotic twin pairs. These results provide the most comprehensive assessment of how functionally defined visual cortex varies across the population to date.

Temporal Dynamics of Neural Responses in Human Visual Cortex.

Neural responses to visual stimuli exhibit complex temporal dynamics, including subadditive temporal summation, response reduction with repeated or sustained stimuli (adaptation), and slower dynamics at low contrast. These phenomena are often studied independently. Here, we demonstrate these phenomena within the same experiment and model the underlying neural computations with a single computational model. We extracted time-varying responses from electrocorticographic recordings from patients presented with stimuli that varied in duration, interstimulus interval (ISI) and contrast. Aggregating data across patients from both sexes yielded 98 electrodes with robust visual responses, covering both earlier (V1-V3) and higher-order (V3a/b, LO, TO, IPS) retinotopic maps. In all regions, the temporal dynamics of neural responses exhibit several nonlinear features. Peak response amplitude saturates with high contrast and longer stimulus durations, the response to a second stimulus is suppressed for short ISIs and recovers for longer ISIs, and response latency decreases with increasing contrast. These features are accurately captured by a computational model composed of a small set of canonical neuronal operations, that is, linear filtering, rectification, exponentiation, and a delayed divisive normalization. We find that an increased normalization term captures both contrast- and adaptation-related response reductions, suggesting potentially shared underlying mechanisms. We additionally demonstrate both changes and invariance in temporal response dynamics between earlier and higher-order visual areas. Together, our results reveal the presence of a wide range of temporal and contrast-dependent neuronal dynamics in the human visual cortex and demonstrate that a simple model captures these dynamics at millisecond resolution.SIGNIFICANCE STATEMENT Sensory inputs and neural responses change continuously over time. It is especially challenging to understand a system that has both dynamic inputs and outputs. Here, we use a computational modeling approach that specifies computations to convert a time-varying input stimulus to a neural response time course, and we use this to predict neural activity measured in the human visual cortex. We show that this computational model predicts a wide variety of complex neural response shapes, which we induced experimentally by manipulating the duration, repetition, and contrast of visual stimuli. By comparing data and model predictions, we uncover systematic properties of temporal dynamics of neural signals, allowing us to better understand how the brain processes dynamic sensory information.

Mnemonic Content and Hippocampal Patterns Shape Judgments of Time.

Our experience of time can feel dilated or compressed, rather than reflecting true "clock time." Although many contextual factors influence the subjective perception of time, it is unclear how memory accessibility plays a role in constructing our experience of and memory for time. Here, we used a combination of behavioral and functional MRI measures in healthy young adults (N = 147) to ask the question of how memory is incorporated into temporal duration judgments. Behaviorally, we found that event boundaries, which have been shown to disrupt ongoing memory integration processes, result in the temporal compression of duration judgments. Additionally, using a multivoxel pattern similarity analysis of functional MRI data, we found that greater temporal pattern change in the left hippocampus within individual trials was associated with longer duration judgments. Together, these data suggest that mnemonic processes play a role in constructing representations of time.

Asymmetries around the visual field: From retina to cortex to behavior.

Visual performance varies around the visual field. It is best near the fovea compared to the periphery, and at iso-eccentric locations it is best on the horizontal, intermediate on the lower, and poorest on the upper meridian. The fovea-to-periphery performance decline is linked to the decreases in cone density, retinal ganglion cell (RGC) density, and V1 cortical magnification factor (CMF) as eccentricity increases. The origins of polar angle asymmetries are not well understood. Optical quality and cone density vary across the retina, but recent computational modeling has shown that these factors can only account for a small percentage of behavior. Here, we investigate how visual processing beyond the cone photon absorptions contributes to polar angle asymmetries in performance. First, we quantify the extent of asymmetries in cone density, midget RGC density, and V1 CMF. We find that both polar angle asymmetries and eccentricity gradients increase from cones to mRGCs, and from mRGCs to cortex. Second, we extend our previously published computational observer model to quantify the contribution of phototransduction by the cones and spatial filtering by mRGCs to behavioral asymmetries. Starting with photons emitted by a visual display, the model simulates the effect of human optics, cone isomerizations, phototransduction, and mRGC spatial filtering. The model performs a forced choice orientation discrimination task on mRGC responses using a linear support vector machine classifier. The model shows that asymmetries in a decision maker's performance across polar angle are greater when assessing the photocurrents than when assessing isomerizations and are greater still when assessing mRGC signals. Nonetheless, the polar angle asymmetries of the mRGC outputs are still considerably smaller than those observed from human performance. We conclude that cone isomerizations, phototransduction, and the spatial filtering properties of mRGCs contribute to polar angle performance differences, but that a full account of these differences will entail additional contribution from cortical representations.

Asymmetries in the discrimination of motion direction around the visual field.

The discriminability of motion direction is asymmetric, with some motion directions that are better discriminated than others. For example, discrimination of directions near the cardinal axes (upward/downward/leftward/rightward) tends to be better than oblique directions. Here, we tested discriminability for multiple motion directions at multiple polar angle locations. We found three systematic asymmetries. First, we found a large cardinal advantage in a cartesian reference frame - better discriminability for motion near cardinal reference directions than oblique directions. Second, we found a moderate cardinal advantage in a polar reference frame - better discriminability for motion near radial (inward/outward) and tangential (clockwise/counterclockwise) reference directions than other directions. Third, we found a small advantage for discriminating motion near radial compared to tangential reference directions. The three advantages combine in an approximately linear manner, and together predict variation in motion discrimination as a function of both motion direction and location around the visual field. For example, best performance is found for radial motion on the horizontal and vertical meridians, as these directions encompass all three advantages, whereas poorest performance is found for oblique motion stimuli located on the horizontal and vertical meridians, as these directions encompass all three disadvantages. Our results constrain models of motion perception and suggest that reference frames at multiple stages of the visual processing hierarchy limit performance.

The Bouma law accounts for crowding in 50 observers.

Crowding is the failure to recognize an object due to surrounding clutter. Our visual crowding survey measured 13 crowding distances (or "critical spacings") twice in each of 50 observers. The survey includes three eccentricities (0, 5, and 10 deg), four cardinal meridians, two orientations (radial and tangential), and two fonts (Sloan and Pelli). The survey also tested foveal acuity, twice. Remarkably, fitting a two-parameter model-the well-known Bouma law, where crowding distance grows linearly with eccentricity-explains 82% of the variance for all 13 × 50 measured log crowding distances, cross-validated. An enhanced Bouma law, with factors for meridian, crowding orientation, target kind, and observer, explains 94% of the variance, again cross-validated. These additional factors reveal several asymmetries, consistent with previous reports, which can be expressed as crowding-distance ratios: 0.62 horizontal:vertical, 0.79 lower:upper, 0.78 right:left, 0.55 tangential:radial, and 0.78 Sloan-font:Pelli-font. Across our observers, peripheral crowding is independent of foveal crowding and acuity. Evaluation of the Bouma factor, b (the slope of the Bouma law), as a biomarker of visual health would be easier if there were a way to compare results across crowding studies that use different methods. We define a standardized Bouma factor b' that corrects for differences from Bouma's 25 choice alternatives, 75% threshold criterion, and linearly symmetric flanker placement. For radial crowding on the right meridian, the standardized Bouma factor b' is 0.24 for this study, 0.35 for Bouma (1970), and 0.30 for the geometric mean across five representative modern studies, including this one, showing good agreement across labs, including Bouma's. Simulations, confirmed by data, show that peeking can skew estimates of crowding (e.g., greatly decreasing the mean or doubling the SD of log b). Using gaze tracking to prevent peeking, individual differences are robust, as evidenced by the much larger 0.08 SD of log b across observers than the mere 0.03 test-retest SD of log b measured in half an hour. The ease of measurement of crowding enhances its promise as a biomarker for dyslexia and visual health.

Population Receptive Field Shapes in Early Visual Cortex Are Nearly Circular.

The visual field region where a stimulus evokes a neural response is called the receptive field (RF). Analytical tools combined with functional MRI (fMRI) can estimate the RF of the population of neurons within a voxel. Circular population RF (pRF) methods accurately specify the central position of the pRF and provide some information about the spatial extent (diameter) of the RF. A number of investigators developed methods to further estimate the shape of the pRF, for example, whether the shape is more circular or elliptical. There is a report that there are many pRFs with highly elliptical pRFs in early visual cortex (V1-V3; Silson et al., 2018). Large aspect ratios (>2) are difficult to reconcile with the spatial scale of orientation columns or visual field map properties in early visual cortex. We started to replicate the experiments and found that the software used in the publication does not accurately estimate RF shape: it produces elliptical fits to circular ground-truth data. We analyzed an independent data set with a different software package that was validated over a specific range of measurement conditions, to show that in early visual cortex the aspect ratios are <2. Furthermore, current empirical and theoretical methods do not have enough precision to discriminate ellipses with aspect ratios of 1.5 from circles. Through simulation we identify methods for improving sensitivity that may estimate ellipses with smaller aspect ratios. The results we present are quantitatively consistent with prior assessments using other methodologies.SIGNIFICANCE STATEMENT We evaluated whether the shape of many population receptive fields (RFs) in early visual cortex is elliptical and differs substantially from circular. We evaluated two tools for estimating elliptical models of the pRF; one tool was valid over the measured compliance range. Using the validated tool, we found no evidence that confidently rejects circular fits to the pRF in visual field maps V1, V2, and V3. The new measurements and analyses are consistent with prior theoretical and experimental assessments in the literature.

What has vision science taught us about functional MRI?

In the domain of human neuroimaging, much attention has been paid to the question of whether and how the development of functional magnetic resonance imaging (fMRI) has advanced our scientific knowledge of the human brain. However, the opposite question is also important; how has our knowledge of the brain advanced our understanding of fMRI? Here, we discuss how and why scientific knowledge about the human and animal visual system has been used to answer fundamental questions about fMRI as a brain measurement tool and how these answers have contributed to scientific discoveries beyond vision science.

Mapping spatial frequency preferences across human primary visual cortex.

Neurons in primate visual cortex (area V1) are tuned for spatial frequency, in a manner that depends on their position in the visual field. Several studies have examined this dependency using functional magnetic resonance imaging (fMRI), reporting preferred spatial frequencies (tuning curve peaks) of V1 voxels as a function of eccentricity, but their results differ by as much as two octaves, presumably owing to differences in stimuli, measurements, and analysis methodology. Here, we characterize spatial frequency tuning at a millimeter resolution within the human primary visual cortex, across stimulus orientation and visual field locations. We measured fMRI responses to a novel set of stimuli, constructed as sinusoidal gratings in log-polar coordinates, which include circular, radial, and spiral geometries. For each individual stimulus, the local spatial frequency varies inversely with eccentricity, and for any given location in the visual field, the full set of stimuli span a broad range of spatial frequencies and orientations. Over the measured range of eccentricities, the preferred spatial frequency is well-fit by a function that varies as the inverse of the eccentricity plus a small constant. We also find small but systematic effects of local stimulus orientation, defined in both absolute coordinates and relative to visual field location. Specifically, peak spatial frequency is higher for pinwheel than annular stimuli and for horizontal than vertical stimuli.

A visual encoding model links magnetoencephalography signals to neural synchrony in human cortex.

Synchronization of neuronal responses over large distances is hypothesized to be important for many cortical functions. However, no straightforward methods exist to estimate synchrony non-invasively in the living human brain. MEG and EEG measure the whole brain, but the sensors pool over large, overlapping cortical regions, obscuring the underlying neural synchrony. Here, we developed a model from stimulus to cortex to MEG sensors to disentangle neural synchrony from spatial pooling of the instrument. We find that synchrony across cortex has a surprisingly large and systematic effect on predicted MEG spatial topography. We then conducted visual MEG experiments and separated responses into stimulus-locked and broadband components. The stimulus-locked topography was similar to model predictions assuming synchronous neural sources, whereas the broadband topography was similar to model predictions assuming asynchronous sources. We infer that visual stimulation elicits two distinct types of neural responses, one highly synchronous and one largely asynchronous across cortex.

Cross-dataset reproducibility of human retinotopic maps.

Population receptive field (pRF) models fit to fMRI data are used to non-invasively measure retinotopic maps in human visual cortex, and these maps are a fundamental component of visual neuroscience experiments. Here, we examined the reproducibility of retinotopic maps across two datasets: a newly acquired retinotopy dataset from New York University (NYU) (n = 44) and a public dataset from the Human Connectome Project (HCP) (n = 181). Our goal was to assess the degree to which pRF properties are similar across datasets, despite substantial differences in their experimental protocols. The two datasets simultaneously differ in their stimulus apertures, participant pool, fMRI protocol, MRI field strength, and preprocessing pipeline. We assessed the cross-dataset reproducibility of the two datasets in terms of the similarity of vertex-wise pRF estimates and in terms of large-scale polar angle asymmetries in cortical magnification. Within V1, V2, V3, and hV4, the group-median NYU and HCP vertex-wise polar angle estimates were nearly identical. Both eccentricity and pRF size estimates were also strongly correlated between the two datasets, but with a slope different from 1; the eccentricity and pRF size estimates were systematically greater in the NYU data. Next, to compare large-scale map properties, we quantified two polar angle asymmetries in V1 cortical magnification previously identified in the HCP data. The NYU dataset confirms earlier reports that more cortical surface area represents horizontal than vertical visual field meridian, and lower than upper vertical visual field meridian. Together, our findings show that the retinotopic properties of V1, V2, V3, and hV4 can be reliably measured across two datasets, despite numerous differences in their experimental design. fMRI-derived retinotopic maps are reproducible because they rely on an explicit computational model of the fMRI response. In the case of pRF mapping, the model is grounded in physiological evidence of how visual receptive fields are organized, allowing one to quantitatively characterize the BOLD signal in terms of stimulus properties (i.e., location and size). The new NYU Retinotopy Dataset will serve as a useful benchmark for testing hypotheses about the organization of visual areas and for comparison to the HCP 7T Retinotopy Dataset.

A population receptive field model of the magnetoencephalography response.

Computational models which predict the neurophysiological response from experimental stimuli have played an important role in human neuroimaging. One type of computational model, the population receptive field (pRF), has been used to describe cortical responses at the millimeter scale using functional magnetic resonance imaging (fMRI) and electrocorticography (ECoG). However, pRF models are not widely used for non-invasive electromagnetic field measurements (EEG/MEG), because individual sensors pool responses originating from several centimeter of cortex, containing neural populations with widely varying spatial tuning. Here, we introduce a forward-modeling approach in which pRFs estimated from fMRI data are used to predict MEG sensor responses. Subjects viewed contrast-reversing bar stimuli sweeping across the visual field in separate fMRI and MEG sessions. Individual subject's pRFs were modeled on the cortical surface at the millimeter scale using the fMRI data. We then predicted cortical time series and projected these predictions to MEG sensors using a biophysical MEG forward model, accounting for the pooling across cortex. We compared the predicted MEG responses to observed visually evoked steady-state responses measured in the MEG session. We found that pRF parameters estimated by fMRI could explain a substantial fraction of the variance in steady-state MEG sensor responses (up to 60% in individual sensors). Control analyses in which we artificially perturbed either pRF size or pRF position reduced MEG prediction accuracy, indicating that MEG data are sensitive to pRF properties derived from fMRI. Our model provides a quantitative approach to link fMRI and MEG measurements, thereby enabling advances in our understanding of spatiotemporal dynamics in human visual field maps.

A validation framework for neuroimaging software: The case of population receptive fields.

Neuroimaging software methods are complex, making it a near certainty that some implementations will contain errors. Modern computational techniques (i.e., public code and data repositories, continuous integration, containerization) enable the reproducibility of the analyses and reduce coding errors, but they do not guarantee the scientific validity of the results. It is difficult, nay impossible, for researchers to check the accuracy of software by reading the source code; ground truth test datasets are needed. Computational reproducibility means providing software so that for the same input anyone obtains the same result, right or wrong. Computational validity means obtaining the right result for the ground-truth test data. We describe a framework for validating and sharing software implementations, and we illustrate its usage with an example application: population receptive field (pRF) methods for functional MRI data. The framework is composed of three main components implemented with containerization methods to guarantee computational reproducibility. In our example pRF application, those components are: (1) synthesis of fMRI time series from ground-truth pRF parameters, (2) implementation of four public pRF analysis tools and standardization of inputs and outputs, and (3) report creation to compare the results with the ground truth parameters. The framework was useful in identifying realistic conditions that lead to imperfect parameter recovery in all four pRF implementations, that would remain undetected using classic validation methods. We provide means to mitigate these problems in future experiments. A computational validation framework supports scientific rigor and creativity, as opposed to the oft-repeated suggestion that investigators rely upon a few agreed upon packages. We hope that the framework will be helpful to validate other critical neuroimaging algorithms, as having a validation framework helps (1) developers to build new software, (2) research scientists to verify the software's accuracy, and (3) reviewers to evaluate the methods used in publications and grants.

Neuronal synchrony and the relation between the blood-oxygen-level dependent response and the local field potential.

The most widespread measures of human brain activity are the blood-oxygen-level dependent (BOLD) signal and surface field potential. Prior studies report a variety of relationships between these signals. To develop an understanding of how to interpret these signals and the relationship between them, we developed a model of (a) neuronal population responses and (b) transformations from neuronal responses into the functional magnetic resonance imaging (fMRI) BOLD signal and electrocorticographic (ECoG) field potential. Rather than seeking a transformation between the two measures directly, this approach interprets each measure with respect to the underlying neuronal population responses. This model accounts for the relationship between BOLD and ECoG data from human visual cortex in V1, V2, and V3, with the model predictions and data matching in three ways: across stimuli, the BOLD amplitude and ECoG broadband power were positively correlated, the BOLD amplitude and alpha power (8-13 Hz) were negatively correlated, and the BOLD amplitude and narrowband gamma power (30-80 Hz) were uncorrelated. The two measures provide complementary information about human brain activity, and we infer that features of the field potential that are uncorrelated with BOLD arise largely from changes in synchrony, rather than level, of neuronal activity.

Modeling visual performance differences 'around' the visual field: A computational observer approach.

Visual performance depends on polar angle, even when eccentricity is held constant; on many psychophysical tasks observers perform best when stimuli are presented on the horizontal meridian, worst on the upper vertical, and intermediate on the lower vertical meridian. This variation in performance 'around' the visual field can be as pronounced as that of doubling the stimulus eccentricity. The causes of these asymmetries in performance are largely unknown. Some factors in the eye, e.g. cone density, are positively correlated with the reported variations in visual performance with polar angle. However, the question remains whether these correlations can quantitatively explain the perceptual differences observed 'around' the visual field. To investigate the extent to which the earliest stages of vision-optical quality and cone density-contribute to performance differences with polar angle, we created a computational observer model. The model uses the open-source software package ISETBIO to simulate an orientation discrimination task for which visual performance differs with polar angle. The model starts from the photons emitted by a display, which pass through simulated human optics with fixational eye movements, followed by cone isomerizations in the retina. Finally, we classify stimulus orientation using a support vector machine to learn a linear classifier on the photon absorptions. To account for the 30% increase in contrast thresholds for upper vertical compared to horizontal meridian, as observed psychophysically on the same task, our computational observer model would require either an increase of ~7 diopters of defocus or a reduction of 500% in cone density. These values far exceed the actual variations as a function of polar angle observed in human eyes. Therefore, we conclude that these factors in the eye only account for a small fraction of differences in visual performance with polar angle. Substantial additional asymmetries must arise in later retinal and/or cortical processing.

Predicting neuronal dynamics with a delayed gain control model.

Visual neurons respond to static images with specific dynamics: neuronal responses sum sub-additively over time, reduce in amplitude with repeated or sustained stimuli (neuronal adaptation), and are slower at low stimulus contrast. Here, we propose a simple model that predicts these seemingly disparate response patterns observed in a diverse set of measurements-intracranial electrodes in patients, fMRI, and macaque single unit spiking. The model takes a time-varying contrast time course of a stimulus as input, and produces predicted neuronal dynamics as output. Model computation consists of linear filtering, expansive exponentiation, and a divisive gain control. The gain control signal relates to but is slower than the linear signal, and this delay is critical in giving rise to predictions matched to the observed dynamics. Our model is simpler than previously proposed related models, and fitting the model to intracranial EEG data uncovers two regularities across human visual field maps: estimated linear filters (temporal receptive fields) systematically differ across and within visual field maps, and later areas exhibit more rapid and substantial gain control. The model is further generalizable to account for dynamics of contrast-dependent spike rates in macaque V1, and amplitudes of fMRI BOLD in human V1.