Cortical quantity representations of visual numerosity and timing overlap increasingly into superior cortices but remain distinct.

Many sensory brain areas are organized as topographic maps where neural response preferences change gradually across the cortical surface. Within association cortices, 7-Tesla fMRI and neural model-based analyses have also revealed many topographic maps for quantities like numerosity and event timing, often in similar locations. Numerical and temporal quantity estimations also show behavioral similarities and even interactions. For example, the duration of high-numerosity displays is perceived as longer than that of low-numerosity displays. Such interactions are often ascribed to a generalized magnitude system with shared neural responses across quantities. Anterior quantity responses are more closely linked to behavior. Here, we investigate whether common quantity representations hierarchically emerge by asking whether numerosity and timing maps become increasingly closely related in their overlap, response preferences, and topography. While the earliest quantity maps do not overlap, more superior maps overlap increasingly. In these overlapping areas, some intraparietal maps have consistently correlated numerosity and timing preferences, and some maps have consistent angles between the topographic progressions of numerosity and timing preferences. However, neither of these relationships increases hierarchically like the amount of overlap does. Therefore, responses to different quantities are initially derived separately, then progressively brought together, without generally becoming a common representation. Bringing together distinct responses to different quantities may underlie behavioral interactions and allow shared access to comparison and action planning systems.

Visual timing-tuned responses in human association cortices and response dynamics in early visual cortex.

Quantifying the timing (duration and frequency) of brief visual events is vital to human perception, multisensory integration and action planning. Tuned neural responses to visual event timing have been found in association cortices, in areas implicated in these processes. Here we ask how these timing-tuned responses are related to the responses of early visual cortex, which monotonically increase with event duration and frequency. Using 7-Tesla functional magnetic resonance imaging and neural model-based analyses, we find a gradual transition from monotonically increasing to timing-tuned neural responses beginning in the medial temporal area (MT/V5). Therefore, across successive stages of visual processing, timing-tuned response components gradually become dominant over inherent sensory response modulation by event timing. This additional timing-tuned response component is independent of retinotopic location. We propose that this hierarchical emergence of timing-tuned responses from sensory processing areas quantifies sensory event timing while abstracting temporal representations from spatial properties of their inputs.

Auditory timing-tuned neural responses in the human auditory cortices.

Perception of sub-second auditory event timing supports multisensory integration, and speech and music perception and production. Neural populations tuned for the timing (duration and rate) of visual events were recently described in several human extrastriate visual areas. Here we ask whether the brain also contains neural populations tuned for auditory event timing, and whether these are shared with visual timing. Using 7T fMRI, we measured responses to white noise bursts of changing duration and rate. We analyzed these responses using neural response models describing different parametric relationships between event timing and neural response amplitude. This revealed auditory timing-tuned responses in the primary auditory cortex, and auditory association areas of the belt, parabelt and premotor cortex. While these areas also showed tonotopic tuning for auditory pitch, pitch and timing preferences were not consistently correlated. Auditory timing-tuned response functions differed between these areas, though without clear hierarchical integration of responses. The similarity of auditory and visual timing tuned responses, together with the lack of overlap between the areas showing these responses for each modality, suggests modality-specific responses to event timing are computed similarly but from different sensory inputs, and then transformed differently to suit the needs of each modality.

Attention drives human numerosity-selective responses.

Numerosity, the set size of a group of items, helps guide behavior and decisions. Previous studies have shown that neural populations respond selectively to numerosities. How numerosity is extracted from the visual scene is a longstanding debate, often contrasting low-level visual with high-level cognitive processes. Here, we investigate how attention influences numerosity-selective responses. The stimuli consisted of black and white dots within the same display. Participants' attention was focused on either black or white dots, while we systematically changed the numerosity of black, white, and total dots. Using 7 T fMRI, we show that the numerosity-tuned neural populations respond only when attention is focused on their preferred numerosity, irrespective of the unattended or total numerosities. Without attention, responses to preferred numerosity are suppressed. Unlike traditional effects of attention in the visual cortex, where attention enhances already existing responses, these results suggest that attention is required to drive numerosity-selective responses.

Numerosity tuning in human association cortices and local image contrast representations in early visual cortex.

Human early visual cortex response amplitudes monotonically increase with numerosity (object number), regardless of object size and spacing. However, numerosity is typically considered a high-level visual or cognitive feature, while early visual responses follow image contrast in the spatial frequency domain. We find that, at fixed contrast, aggregate Fourier power (at all orientations and spatial frequencies) follows numerosity closely but nonlinearly with little effect of object size, spacing or shape. This would allow straightforward numerosity estimation from spatial frequency domain image representations. Using 7T fMRI, we show monotonic responses originate in primary visual cortex (V1) at the stimulus's retinotopic location. Responses here and in neural network models follow aggregate Fourier power more closely than numerosity. Truly numerosity tuned responses emerge after lateral occipital cortex and are independent of retinotopic location. We propose numerosity's straightforward perception and neural responses may result from the pervasive spatial frequency analyses of early visual processing.

The role of neural tuning in quantity perception.

Perception of quantities, such as numerosity, timing, and size, is essential for behavior and cognition. Accumulating evidence demonstrates neurons processing quantities are tuned, that is, have a preferred quantity amount, not only for numerosity, but also other quantity dimensions and sensory modalities. We argue that quantity-tuned neurons are fundamental to understanding quantity perception. We illustrate how the properties of quantity-tuned neurons can underlie a range of perceptual phenomena. Furthermore, quantity-tuned neurons are organized in distinct but overlapping topographic maps. We suggest that this overlap in tuning provides the neural basis for perceptual interactions between different quantities, without the need for a common neural representational code.

Simultaneous changes in visual acuity, cortical population receptive field size, visual field map size, and retinal thickness in healthy human aging.

Healthy human aging is associated with a deterioration of visual acuity, retinal thinning, visual field map shrinkage and increasing population receptive field sizes. Here we ask how these changes are related to each other in a cross-sectional sample of fifty healthy adults aged 20-80 years. We hypothesized that age-related loss of macular retinal ganglion cells may lead to decreased visual field map sizes, and both may lead to increased pRF sizes in the cortical central visual field representation. We measured our participants' perceptual corrected visual acuity using standard ophthalmological letter charts. We then measured their early visual field map (V1, V2 and V3) functional population receptive field (pRF) sizes and structural surface areas using fMRI, and their retinal structure using high-definition optical coherence tomography. With increasing age visual acuity decreased, pRF sizes increased, visual field maps surface areas (but not whole-brain surface areas) decreased, and retinal thickness decreased. Among these measures, only functional pRF sizes predicted perceptual visual acuity, and Bayesian statistics support a null relationship between visual acuity and cortical or retinal structure. However, pRF sizes were in turn predicted by cortical structure only (visual field map surface areas), which were only predicted by retinal structure (thickness). These results suggest that simultaneous disruptions of neural structure and function throughout the early visual system may underlie the deterioration of perceptual visual acuity in healthy aging.

Topographic numerosity maps cover subitizing and estimation ranges.

Numerosity, the set size of a group of items, helps guide behaviour and decisions. Non-symbolic numerosities are represented by the approximate number system. However, distinct behavioural performance suggests that small numerosities, i.e. subitizing range, are implemented differently in the brain than larger numerosities. Prior work has shown that neural populations selectively responding (i.e. hemodynamic responses) to small numerosities are organized into a network of topographical maps. Here, we investigate how neural populations respond to large numerosities, well into the ANS. Using 7 T fMRI and biologically-inspired analyses, we found a network of neural populations tuned to both small and large numerosities organized within the same topographic maps. These results demonstrate a continuum of numerosity preferences that progressively cover both the subitizing range and beyond within the same numerosity map, suggesting a single neural mechanism. We hypothesize that differences in map properties, such as cortical magnification and tuning width, underlie known differences in behaviour.

Size constancy affects the perception and parietal neural representation of object size.

Humans and animals rely on accurate object size perception to guide behavior. Object size is judged from visual input, but the relationship between an object's retinal size and its real-world size varies with distance. Humans perceive object sizes to be relatively constant when retinal size changes. Such size constancy compensates for the variable relationship between retinal size and real-world size, using the context of recent retinal sizes of the same object to bias perception towards its likely real-world size. We therefore hypothesized that object size perception may be affected by the range of recently viewed object sizes, attracting perceived object sizes towards recently viewed sizes. We demonstrate two systematic biases: a central tendency attracting perceived size towards the average size across all trials, and a serial dependence attracting perceived size towards the size presented on the previous trial. We recently described topographic object size maps in the human parietal cortex. We therefore hypothesized that neural representations of object size here would be attracted towards recently viewed sizes. We used ultra-high-field (7T) functional MRI and population receptive field modeling to compare object size representations measured with small (0.05-1.4°diameter) and large objects sizes (0.1-2.8°). We found that parietal object size preferences and tuning widths follow this presented range, but change less than presented object sizes. Therefore, perception and neural representation of object size are attracted towards recently viewed sizes. This context-dependent object size representation reveals effects on neural response preferences that may underlie context dependence of object size perception.

Adaptation to visual numerosity changes neural numerosity selectivity.

Perceiving numerosity, i.e. the set size of a group of items, is an evolutionarily preserved ability found in humans and animals. A useful method to infer the neural underpinnings of a given perceptual property is sensory adaptation. Like other primary perceptual attributes, numerosity is susceptible to adaptation. Recently, we have shown numerosity-selective neural populations with a topographic organization in the human brain. Here, we investigated whether numerosity adaptation can affect the numerosity selectivity of these populations using ultra-high field (7 Tesla) functional magnetic resonance imaging (fMRI). Participants viewed stimuli of changing numerosity (1 to 7 dots), which allowed the mapping of numerosity selectivity. We interleaved a low or high numerosity adapter stimulus with these mapping stimuli, repeatedly presenting 1 or 20 dots respectively to adapt the numerosity-selective neural populations. We analyzed the responses using custom-build population receptive field neural models of numerosity encoding and compared estimated numerosity preferences between adaptation conditions. We replicated our previous studies where we found several topographic maps of numerosity-selective responses. We found that overall, numerosity adaptation altered the preferred numerosities within the numerosity maps, resulting in predominantly attractive biases towards the numerosity of the adapter. The differential biases could be explained by the difference between the unadapted preferred numerosity and the numerosity of the adapter, with attractive biases being observed with higher difference. The results could link perceptual numerosity adaptation effects to changes in neural numerosity selectivity.

Topographic maps representing haptic numerosity reveals distinct sensory representations in supramodal networks.

Dedicated maps for cognitive quantities such as timing, size and numerosity support the view that topography is a general principle of brain organization. To date, however, all of these maps were driven by the visual system. Here, we ask whether there are supramodal topographic maps representing cognitive dimensions irrespective of the stimulated sensory modality. We measured haptically and visually driven numerosity-selective neural responses using model-based analyses and ultra-high field (7T) fMRI. We found topographically organized neural populations tuned to haptic numerosity. The responses to visual or haptic numerosity shared a similar cortical network. However, the maps of the two modalities only partially overlap. Thus, although both visual and haptic numerosities are processed in a similar supramodal functional network, the underlying neural populations may be related, but distinct. Therefore, we hypothesize that overlap between modality-specific maps facilitates cross-modal interactions and supramodal representation of cognitive quantities.

Propagation of BOLD Activity Reveals Task-dependent Directed Interactions Across Human Visual Cortex.

It has recently been shown that large-scale propagation of blood-oxygen-level-dependent (BOLD) activity is constrained by anatomical connections and reflects transitions between behavioral states. It remains to be seen, however, if the propagation of BOLD activity can also relate to the brain's anatomical structure at a more local scale. Here, we hypothesized that BOLD propagation reflects structured neuronal activity across early visual field maps. To explore this hypothesis, we characterize the propagation of BOLD activity across V1, V2, and V3 using a modeling approach that aims to disentangle the contributions of local activity and directed interactions in shaping BOLD propagation. It does so by estimating the effective connectivity (EC) and the excitability of a noise-diffusion network to reproduce the spatiotemporal covariance structure of the data. We apply our approach to 7T fMRI recordings acquired during resting state (RS) and visual field mapping (VFM). Our results reveal different EC interactions and changes in cortical excitability in RS and VFM, and point to a reconfiguration of feedforward and feedback interactions across the visual system. We conclude that the propagation of BOLD activity has functional relevance, as it reveals directed interactions and changes in cortical excitability in a task-dependent manner.

A Network of Topographic Maps in Human Association Cortex Hierarchically Transforms Visual Timing-Selective Responses.

Accurately timing sub-second sensory events is crucial when perceiving our dynamic world. This ability allows complex human behaviors that require timing-dependent multisensory integration and action planning. Such behaviors include perception and performance of speech, music, driving, and many sports. How are responses to sensory event timing processed for multisensory integration and action planning? We measured responses to viewing systematically changing visual event timing using ultra-high-field fMRI. We analyzed these responses with neural population response models selective for event duration and frequency, following behavioral, computational, and macaque action planning results and comparisons to alternative models. We found systematic local changes in timing preferences (recently described in supplementary motor area) in an extensive network of topographic timing maps, mirroring sensory cortices and other quantity processing networks. These timing maps were partially left lateralized and widely spread, from occipital visual areas through parietal multisensory areas to frontal action planning areas. Responses to event duration and frequency were closely linked. As in sensory cortical maps, response precision varied systematically with timing preferences, and timing selectivity systematically varied between maps. Progressing from posterior to anterior maps, responses to multiple events were increasingly integrated, response selectivity narrowed, and responses focused increasingly on the middle of the presented timing range. These timing maps largely overlap with numerosity and visual field map networks. In both visual timing map and visual field map networks, selective responses and topographic map organization may facilitate hierarchical transformations by allowing neural populations to interact over minimal distances.

Temporal Characteristics of Priming of Attention Shifts Are Mirrored by BOLD Response Patterns in the Frontoparietal Attention Network.

Priming of attention shifts involves the reduction in search RTs that occurs when target location or target features repeat. We used functional magnetic resonance imaging to investigate the neural basis of such attentional priming, specifically focusing on its temporal characteristics over trial sequences. We first replicated earlier findings by showing that repetition of target color and of target location from the immediately preceding trial both result in reduced blood oxygen level-dependent (BOLD) signals in a cortical network that encompasses occipital, parietal, and frontal cortices: lag-1 repetition suppression. While such lag-1 suppression can have a number of explanations, behaviorally, the influence of attentional priming extends further, with the influence of past search trials gradually decaying across multiple subsequent trials. Our results reveal that the same regions within the frontoparietal network that show lag-1 suppression, also show longer term BOLD reductions that diminish over the course of several trial presentations, keeping pace with the decaying behavioral influence of past target properties across trials. This distinct parallel between the across-trial patterns of cortical BOLD and search RT reductions, provides strong evidence that these cortical areas play a key role in attentional priming.

Optical Properties Influence Visual Cortical Functional Resolution After Cataract Surgery and Both Dissociate From Subjectively Perceived Quality of Vision.

Purpose: To investigate the relation between optical properties, population receptive fields (pRFs), visual function, and subjectively perceived quality of vision after cataract surgery. Methods: The study includes 30 patients who had recently undergone bilateral sequential cataract surgery. We used functional magnetic resonance imaging and pRF modelling methods to assess pRF sizes across visual cortical regions (V1-V3). Subjects also performed a complete ophthalmologic and psychophysical examination and answered a quality of vision questionnaire. Results: Subjects with worse optical properties had, as predicted, larger pRF sizes. In addition, analysis in the primary visual cortex revealed significantly larger mean pRF sizes for operated subjects with worse contrast sensitivity (P = 0.038). In contrast, patients who scored high in the subjective "bothersome" dimension induced by dysphotic symptoms had surprisingly lower pRF size fitting interception (P = 0.012) and pRF size fitting slopes (P = 0.020), suggesting a dissociation between objective quality of vision and subjective appraisal. Conclusions: Optical properties of the eye influence pRF size. In particular, visual aberrations have a negative impact on visual cortical processing. A novel dissociation between subjective reports of quality of vision and pRF sizes was further identified. This suggests that patients with better cortical resolution may have a negative subjective response possibly because of improved perception of dysphotic phenomena. pRF properties represent a valuable quantitative measure to objectively evaluate quality of vision but do not necessarily predict subjective complaints.

Data describing the accuracy of non-numerical visual features in predicting fMRI responses to numerosity.

Here we took several stimulus configurations that have the same numerosity progression but vary considerably in their non-numerical visual features. We collected responses to these stimuli using ultra-high-field (7T) fMRI in a posterior parietal area that responds to changes in these stimuli. We first quantify the relationships between numerosity and several non-numerical visual features in each stimulus configuration. We then use population receptive field (pRF) modeling to quantify how well responses to each of these visual features predicts the observed responses to each stimulus configuration, and observed responses to all stimulus configurations together. We compare the predictive accuracy of responses to numerosity and to non-numerical visual features in explaining the observed responses. This provides the details of the analysis outcomes summarized in an accompanying article (10.1016/j.neuroimage.2017.02.012, NIMG-16-1350).

Radial asymmetries in population receptive field size and cortical magnification factor in early visual cortex.

Human visual cortex does not represent the whole visual field with the same detail. Changes in receptive field size, population receptive field (pRF) size and cortical magnification factor (CMF) with eccentricity are well established, and associated with changes in visual acuity with eccentricity. Visual acuity also changes across polar angle. However, it remains unclear how RF size, pRF size and CMF change across polar angle. Here, we examine differences in pRF size and CMF across polar angle in V1, V2 and V3 using pRF modeling of human fMRI data. In these visual field maps, we find smaller pRFs and larger CMFs in horizontal (left and right) than vertical (upper and lower) visual field quadrants. Differences increase with eccentricity, approximately in proportion to average pRF size and CMF. Similarly, we find larger CMFs in the lower than upper quadrant, and again differences increase with eccentricity. However, pRF size differences between lower and upper quadrants change direction with eccentricity. Finally, we find slightly smaller pRFs in the left than right quadrants of V2 and V3, though this difference is very small, and we find no differences in V1 and no differences in CMF. Moreover, differences in pRF size and CMF vary gradually with polar angle and are not limited to the meridians or visual field map discontinuities. PRF size and CMF differences do not consistently follow patterns of cortical curvature, despite the link between cortical curvature and polar angle in V1. Thus, the early human visual cortex has a radially asymmetric representation of the visual field. These asymmetries may underlie consistent reports of asymmetries in perceptual abilities.

Phase-synchronization-based parcellation of resting state fMRI signals reveals topographically organized clusters in early visual cortex.

Resting-state fMRI is widely used to study brain function and connectivity. However, interpreting patterns of resting state (RS) fMRI activity remains challenging as they may arise from different neuronal mechanisms than those triggered by exogenous events. Currently, this limits the use of RS-fMRI for understanding cortical function in health and disease. Here, we examine the phase synchronization (PS) properties of blood-oxygen level dependent (BOLD) signals obtained during visual field mapping (VFM) and RS with 7T fMRI. This data-driven approach exploits spatiotemporal covariations in the phase of BOLD recordings to establish the presence of clusters of synchronized activity. We find that, in both VFM and RS data, selecting the most synchronized neighboring recording sites identifies spatially localized PS clusters that follow the topographic organization of the visual cortex. However, in activity obtained during VFM, PS is spatially more extensive than in RS activity, likely reflecting stimulus-driven interactions between local responses. Nevertheless, the similarity of the PS clusters obtained for RS and stimulus-driven fMRI suggest that they share a common neuroanatomical origin. Our finding justifies and facilitates direct comparison of RS and stimulus-evoked activity.

Image identification from brain activity using the population receptive field model.

A goal of computational models is not only to explain experimental data but also to make new predictions. A current focus of computational neuroimaging is to predict features of the presented stimulus from measured brain signals. These computational neuroimaging approaches may be agnostic about the underlying neural processes or may be biologically inspired. Here, we use the biologically inspired population receptive field (pRF) approach to identify presented images from fMRI recordings of the visual cortex, using an explicit model of the underlying neural response selectivity. The advantage of the pRF-model is its simplicity: it is defined by a handful of parameters, which can be estimated from fMRI data that was collected within half an hour. Using 7T MRI, we measured responses elicited by different visual stimuli: (i) conventional pRF mapping stimuli, (ii) semi-random synthetic images and (iii) natural images. The pRF mapping stimuli were used to estimate the pRF-properties of each cortical location in early visual cortex. Next, we used these pRFs to identify which synthetic or natural images was presented to the subject from the fMRI responses. We show that image identification using V1 responses is far above chance, both for the synthetic and natural images. Thus, we can identify visual images, including natural images, using the most fundamental low-parameter pRF model estimated from conventional pRF mapping stimuli. This allows broader application of image identification.

Comparing Parietal Quantity-Processing Mechanisms between Humans and Macaques.

Quantity processing studies typically assume functional homology between regions within macaque and human intraparietal sulcus (IPS), where apparently similar locations respond to broadly similar tasks. However, macaque single cell neurophysiology is difficult to compare to human functional magnetic resonance imaging (fMRI); particularly in multivoxel pattern analysis and adaptation paradigms, or where different tasks are used. fMRI approaches incorporating neural tuning models allow closer comparison, revealing human numerosity-selective responses only outside the IPS. Extensive functional similarities support this novel homology of physical quantity processing. Human IPS instead houses a network responding to comparisons of physical quantities, symbolic numbers, and other stimulus features. This network likely reflects interactions between physical quantity processing, spatial processing, and (in humans) linguistic processing.