The effect of aging on the eccentricity dependency of orientation anisotropy of perceptual surround suppression.

The features of perceptual surround suppression vary with eccentricity, such that the suppression strength is increased for horizontally oriented stimuli relative to other orientations near the fovea, but is strongest for radially oriented stimuli more peripherally. Perceptual suppression also varies with age, which has been well-studied for central fixation. However, only limited data are available regarding perceptual suppression in older adults for nonfoveal vision, and none of those studies have taken orientation biases of contrast sensitivity into account. Here, we explored the effects of older age on the eccentricity dependency of orientation biases of perceptual suppression. We found increased perceptual suppression in older adults at both 6° and 15° eccentricities relative to younger adults. A main effect of the horizontal orientation bias was found at 6° and a main effect of the radial orientation bias was found at 15° in both groups. In summary, perceptual surround suppression of contrast is stronger for older adults compared with younger adults at 6° and 15° eccentricities, but retinotopic orientation anisotropies are maintained with age. This study provides new insight into parafoveal visual perception in older adults, which may be particularly important to understand the visual experience of those who depend on nonfoveal vision owing to common age-related eye diseases.

Diversity of Feature Selectivity in Macaque Visual Cortex Arising from a Limited Number of Broadly Tuned Input Channels.

Spike (action potential) responses of most primary visual cortical cells in the macaque are sharply tuned for the orientation of a line or an edge, and neurons preferring similar orientations are clustered together in cortical columns. The preferred stimulus orientation of these columns span the full range of orientations, as observed in recordings of spikes and in classical optical imaging of intrinsic signals. However, when we imaged the putative thalamic input to striate cortical cells that can be seen in imaging of intrinsic signals when they are analyzed on a larger spatial scale, we found that the orientation domain map of the primary visual cortex did not show the same diversity of orientations. This map was dominated by just the one orientation that is most commonly preferred by neurons in the retina and the lateral geniculate nucleus. This supports cortical feature selectivity and columnar architecture being built upon feed-forward signals transmitted from the thalamus in a very limited number of broadly tuned input channels.

Attentional asymmetry between visual hemifields is related to habitual direction of reading and its implications for debate on cause and effects of dyslexia.

A major controversy regarding dyslexia is whether any of the many visual and phonological deficits found to be correlated with reading difficulty cause the impairment or result from the reduced amount of reading done by dyslexics. We studied this question by comparing a visual capacity in the left and right visual hemifields in people habitually reading scripts written right-to-left or left-to-right. Selective visual attention is necessary for efficient visual search and also for the sequential recognition of letters in words. Because such attentional allocation during reading depends on the direction in which one is reading, asymmetries in search efficiency may reflect biases arising from the habitual direction of reading. We studied this by examining search performance in three cohorts: (a) left-to-right readers who read English fluently; (b) right-to-left readers fluent in reading Farsi but not any left-to-right script; and (c) bilingual readers fluent in English and in Farsi, Arabic, or Hebrew. Left-to-right readers showed better search performance in the right hemifield and right-to-left readers in the left hemifield, but bilingual readers showed no such asymmetries. Thus, reading experience biases search performance in the direction of reading, which has implications for the cause and effect relationships between reading and cognitive functions.

Eccentricity dependence of orientation anisotropy of surround suppression of contrast-detection threshold.

Both neurophysiological and psychophysical data provide evidence for orientation biases in nonfoveal vision-specifically, a tendency for a Cartesian horizontal and vertical bias close to fixation, changing to a radial bias with increasing retinal eccentricity. We explore whether the strength of surround suppression of contrast detection also depends on retinotopic location and relative surround configuration (horizontal, vertical, radial, tangential) in parafoveal vision. Three visual-field locations were tested (0°, 225°, and 270°, angle increasing anticlockwise from 0° horizontal axis) at viewing eccentricities of 6° and 15°. Contrast-detection threshold was estimated with and without a surrounding annulus. At 6° eccentricity, horizontally oriented parallel center-surround (C-S) configurations resulted in greater surround suppression compared to vertically oriented parallel center-surround configurations (p = 0.001). At 15° eccentricity, radially oriented parallel center-surround stimuli conferred greater suppression than tangentially oriented stimuli (p = 0.027). Parallel surrounds resulted in greater suppression than orthogonal surrounds at both eccentricities (p < 0.05). At 6° the horizontal center was more susceptible to suppression than a vertical center (p < 0.001) for both parallel and orthogonal surrounds, while at 15° a radial center was more susceptible to suppression (relative to a tangential center), but only if the surround was parallel (p = 0.005). Our data show that orientation anisotropy of surround suppression alters with eccentricity, reflecting a link between suppression strength and visual-field retinotopy.

Contrast invariance of orientation tuning in the lateral geniculate nucleus of the feline visual system.

Responses of most neurons in the primary visual cortex of mammals are markedly selective for stimulus orientation and their orientation tuning does not vary with changes in stimulus contrast. The basis of such contrast invariance of orientation tuning has been shown to be the higher variability in the response for low-contrast stimuli. Neurons in the lateral geniculate nucleus (LGN), which provides the major visual input to the cortex, have also been shown to have higher variability in their response to low-contrast stimuli. Parallel studies have also long established mild degrees of orientation selectivity in LGN and retinal cells. In our study, we show that contrast invariance of orientation tuning is already present in the LGN. In addition, we show that the variability of spike responses of LGN neurons increases at lower stimulus contrasts, especially for non-preferred orientations. We suggest that such contrast- and orientation-sensitive variability not only explains the contrast invariance observed in the LGN but can also underlie the contrast-invariant orientation tuning seen at the level of the primary visual cortex.

Functional size of human visual area V1: a neural correlate of top-down attention.

Heavy demands are placed on the brain's attentional capacity when selecting a target item in a cluttered visual scene, or when reading. It is widely accepted that such attentional selection is mediated by top-down signals from higher cortical areas to early visual areas such as the primary visual cortex (V1). Further, it has also been reported that there is considerable variation in the surface area of V1. This variation may impact on either the number or specificity of attentional feedback signals and, thereby, the efficiency of attentional mechanisms. In this study, we investigated whether individual differences between humans performing attention-demanding tasks can be related to the functional area of V1. We found that those with a larger representation in V1 of the central 12° of the visual field as measured using BOLD signals from fMRI were able to perform a serial search task at a faster rate. In line with recent suggestions of the vital role of visuo-spatial attention in reading, the speed of reading showed a strong positive correlation with the speed of visual search, although it showed little correlation with the size of V1. The results support the idea that the functional size of the primary visual cortex is an important determinant of the efficiency of selective spatial attention for simple tasks, and that the attentional processing required for complex tasks like reading are to a large extent determined by other brain areas and inter-areal connections.

Multiple pathways carry signals from short-wavelength-sensitive ('blue') cones to the middle temporal area of the macaque.

We recorded spike activity of single neurones in the middle temporal visual cortical area (MT or V5) of anaesthetised macaque monkeys. We used flashing, stationary spatially circumscribed, cone-isolating and luminance-modulated stimuli of uniform fields to assess the effects of signals originating from the long-, medium- or short- (S) wavelength-sensitive cone classes. Nearly half (41/86) of the tested MT neurones responded reliably to S-cone-isolating stimuli. Response amplitude in the majority of the neurones tested further (19/28) was significantly reduced, though not always completely abolished, during reversible inactivation of visuotopically corresponding regions of the ipsilateral primary visual cortex (striate cortex, area V1). Thus, the present data indicate that signals originating in S-cones reach area MT, either via V1 or via a pathway that does not go through area V1. We did not find a significant difference between the mean latencies of spike responses of MT neurones to signals that bypass V1 and those that do not; the considerable overlap we observed precludes the use of spike-response latency as a criterion to define the routes through which the signals reach MT.

Information processing bottlenecks in macaque posterior parietal cortex: an attentional blink?

When two brief stimuli are presented in rapid succession, our ability to attend and recognize the second stimulus is impaired if our attentional resources are devoted to processing the first. Such inability (termed the "attentional blink" in human studies) arises around 200-500 ms following the onset of the first stimulus. We trained two monkeys on a delayed-match-to-sample task where both the location and orientation of two successively presented grating patches had to be matched. When the delay between the two gratings was varied, monkey's behavioral performance (d') was affected in a way that was analogous to the attentional blink in humans. Furthermore, a subset of neurons in the monkey's lateral intraparietal area, known to be crucial in the control of attention, closely followed the variation in d', even on occasions when d' followed an atypical pattern. Our results provide the first behavioral demonstration of an attentional bottleneck in the macaque of a type similar to the human attentional blink as well as a possible single-neuron correlate of the phenomenon.

Space, color, and direction of movement: how do they affect attention?

Paying attention improves performance, but is this improvement regardless of what we attend to? We explored the differences in performance between attending to a location and attending to a feature when perceiving global motion. Attention was first cued to one of four locations that had coherently moving dots, while the remaining three had randomly moving distracter dots. Participants then viewed a colored display, wherein the color of the coherently moving dots was cued instead of location. In the third task, participants identified the location that had a particular cued direction of motion. Most observers reported reductions of motion threshold in all three tasks compared to when no cue was provided. However, the attentional bias generated by location cues was significantly larger than the bias resulting from feature cues of direction or color. This effect is consistent with the idea that attention is largely controlled by a fronto-parietal network where spatial relations are preferentially processed. On the other hand, color could not be used as a cue to focus attention and integrate motion. This finding suggests that color relies heavily on processing by ventral temporal cortical areas, which may have little control over the global motion areas in the dorsal part of the brain.

Dynamic coupling of oscillatory neural activity and its roles in visual attention.

Oscillatory neural activity is believed to have a central role in information processing in the mammalian brain. While early studies often focussed on the function of individual frequency bands, there is emerging appreciation for the role of simultaneous activity in many distinct frequency bands and the interactions between them in high-level cognitive functions. Here, we focus on the role of cross-frequency coupling (CFC) in visual attention. First, we propose a framework that reconciles previous contrasting findings, showing how CFC could have a functional role on both intra- and interareal scales. Second, we outline how CFC between distinct frequency bands could label different submodalities of sensory information. Overall, our scheme provides a novel perspective of how interfrequency interaction contributes to efficient and dynamic processing of information across the brain.

Mechanism underpinning the sharpening of orientation and spatial frequency selectivities in the tree shrew (Tupaia belangeri) primary visual cortex.

Most neurons in the primary visual cortex (V1) of mammals show sharp orientation selectivity and band-pass spatial frequency tuning. Here, we examine whether sharpening of the broad tuning that exists subcortically, namely in the retina and the lateral geniculate nucleus (LGN), underlie the sharper tuning seen for both the above features in tree shrew V1. Since the transition from poor feature selectivity to sharp tuning occurs entirely within V1 in tree shrews, we examined the orientation selectivity and spatial frequency tuning of neurons within individual electrode penetrations. We found that most layer 4 and layer 2/3 neurons in the same cortical column preferred the same stimulus orientation. However, a subset of layer 3c neurons close to the layer 4 border preferred near orthogonal orientations, suggesting that layer 2/3 neurons may inherit the orientation preferences of their layer 4 input neurons and also receive cross-orientation inhibition from layer 3c neurons. We also found that layer 4 neurons showed sharper orientation selectivity at higher spatial frequencies, suggesting that attenuation of low spatial frequency responses by spatially broad inhibition acting on layer 4 inputs to layer 2/3 neurons can enhance both orientation and spatial frequency selectivities. However, in a proportion of layer 2/3 neurons, the sharper tuning of layer 2/3 neurons appeared to arise also or even mainly from inhibition specific to high spatial frequencies acting on the layer 4 inputs to layer 2/3. Overall, our results are consistent with the suggestion that in tree shrews, sharp feature selectivity in layer 2/3 can be established by intracortical mechanisms that sharpen biases observed in layer 4, which are in turn inherited presumably from thalamic afferents.

Role of feedforward geniculate inputs in the generation of orientation selectivity in the cat's primary visual cortex.

Neurones of the mammalian primary visual cortex have the remarkable property of being selective for the orientation of visual contours. It has been controversial whether the selectivity arises from intracortical mechanisms, from the pattern of afferent connectivity from lateral geniculate nucleus (LGN) to cortical cells or from the sharpening of a bias that is already present in the responses of many geniculate cells. To investigate this, we employed a variation of an electrical stimulation protocol in the LGN that has been claimed to suppress intra cortical inputs and isolate the raw geniculocortical input to a striate cortical cell. Such stimulation led to a sharpening of the orientation sensitivity of geniculate cells themselves and some broadening of cortical orientation selectivity. These findings are consistent with the idea that non-specific inhibition of the signals from LGN cells which exhibit an orientation bias can generate the sharp orientation selectivity of primary visual cortical cells. This obviates the need for an excitatory convergence from geniculate cells whose receptive fields are arranged along a row in visual space as in the classical model and provides a framework for orientation sensitivity originating in the retina and getting sharpened through inhibition at higher levels of the visual pathway.

Visual search efficiency and functional visual cortical size in children with and without dyslexia.

Dyslexia is characterised by poor reading ability. Its aetiology is probably multifactorial, with abnormal visual processing playing an important role. Among adults with normal reading ability, there is a larger representation of central visual field in the primary visual cortex (V1) in those with more efficient visuospatial attention. In this study, we tested the hypothesis that poor reading ability in school-aged children (17 children with dyslexia, 14 control children with normal reading ability) is associated with deficits in visuospatial attention using a visual search task. We corroborated the psychophysical findings with neuroimaging, by measuring the functional size of V1 in response to a central 12° visual stimulus. Consistent with other literature, visual search was impaired and less efficient in the dyslexic children, particularly with more distractor elements in the search array (p = 0.04). We also found atypical interhemispheric asymmetry in functional V1 size in the dyslexia group (p = 0.02). Reading impaired children showed poorer visual search efficiency (p = 0.01), needing more time per unit distractor (higher ms/item). Reading ability was also correlated with V1 size asymmetry (p = 0.03), such that poorer readers showed less left hemisphere bias relative to the right hemisphere. Our findings support the view that dyslexic children have abnormal visuospatial attention and interhemispheric V1 asymmetry, relative to chronological age-matched peers, and that these factors may contribute to inter-individual variation in reading performance in children.

Segregation of short-wavelength-sensitive (S) cone signals in the macaque dorsal lateral geniculate nucleus.

An important problem in the study of the mammalian visual system is whether functionally different retinal ganglion cell types are anatomically segregated further up along the central visual pathway. It was previously demonstrated that, in a New World diurnal monkey (marmoset), the neurones carrying signals from the short-wavelength-sensitive (S) cones [blue-yellow (B/Y)-opponent cells] are predominantly located in the koniocellular layers of the dorsal lateral geniculate nucleus (LGN), whereas the red-green (R/G)-opponent cells carrying signals from the medium- and long-wavelength-sensitive cones are segregated in the parvocellular layers. Here, we used extracellular single-unit recordings followed by histological reconstruction to investigate the distribution of color-selective cells in the LGN of the macaque, an Old World diurnal monkey. Cells were classified using cone-isolating stimuli to identify their cone inputs. Our results indicate that the majority of cells carrying signals from S-cones are located either in the koniocellular layers or in the 'koniocellular bridges' that fully or partially span the parvocellular layers. By contrast, the R/G-opponent cells are located in the parvocellular layers. We conclude that anatomical segregation of B/Y- and R/G-opponent afferent signals for color vision is common to the LGNs of New World and Old World diurnal monkeys.

Visual attention and neural oscillations in reading and dyslexia: Are they possible targets for remediation?

After decades of finding a range of cognitive functions both in visual and phonological domains that correlate with reading performance, there are in recent years attempts to solve the causation versus correlation dilemma in finding a core deficit in developmental dyslexia (DD). Thus, longitudinal studies that aim to predict reading difficulties from studies done in pre-reading years and reading-level matched studies that try to factor out the effect due to lack of reading in DD cohorts, have helped identify two possible candidates to be added to the classical phonological suspect. One is a deficit in visuo-spatial attention that underpins our ability to selectively attend to individual objects in a cluttered world, which is fundamental in being able to identify letters and words in a text such as the one you are reading now. The other is an impairment in synchronised neuronal oscillations that may be crucial in mediating many cortical functions and also communication between brain regions. The latter may be a general deficit affecting many areas of the brain and thus underlie the wide-ranging co-morbidities in DD. However, that neuronal synchrony is a critical mediator in visual attention, brings the two suggestions into one hypothesis of a core deficit that triggers in some young children a great reluctance to read, putting them at a handicap in comparison to other children. This deprives them of the advantage that normal readers have in development of those visual and phonological processes that are needed for reading. This insight into aetiology may help in developing new remediation strategies, specifically aimed at improving visual attention and neuronal synchrony.

An Integrated Neuronal Model of Claustral Function in Timing the Synchrony Between Cortical Areas.

It has been suggested that the function of the claustrum (CL) may be to orchestrate and integrate the activity of the different cortical areas that are involved in a particular function by boosting the synchronized oscillations that occur between these areas. We propose here a model of how this may be done, thanks to the unique synaptic morphology of the CL and its excitatory and inhibitory connections with most cortical areas. Using serial visual search as an example, we describe how the functional anatomy of the claustral connections can potentially execute the sequential activation of the representations of objects that are being processed serially. We also propose that cross-frequency coupling (CFC) between low frequency signals from CL and higher frequency oscillations in the cortical areas will be an efficient means of CL modulating neural activity across multiple brain regions in synchrony. This model is applicable to the wide range of functions one performs, from simple object recognition to reading and writing, listening to or performing music, etc.

Coding of spatial attention priorities and object features in the macaque lateral intraparietal cortex.

Primate posterior parietal cortex (PPC) is known to be involved in controlling spatial attention. Neurons in one part of the PPC, the lateral intraparietal area (LIP), show enhanced responses to objects at attended locations. Although many are selective for object features, such as the orientation of a visual stimulus, it is not clear how LIP circuits integrate feature-selective information when providing attentional feedback about behaviorally relevant locations to the visual cortex. We studied the relationship between object feature and spatial attention properties of LIP cells in two macaques by measuring the cells' orientation selectivity and the degree of attentional enhancement while performing a delayed match-to-sample task. Monkeys had to match both the location and orientation of two visual gratings presented separately in time. We found a wide range in orientation selectivity and degree of attentional enhancement among LIP neurons. However, cells with significant attentional enhancement had much less orientation selectivity in their response than cells which showed no significant modulation by attention. Additionally, orientation-selective cells showed working memory activity for their preferred orientation, whereas cells showing attentional enhancement also synchronized with local neuronal activity. These results are consistent with models of selective attention incorporating two stages, where an initial feature-selective process guides a second stage of focal spatial attention. We suggest that LIP contributes to both stages, where the first stage involves orientation-selective LIP cells that support working memory of the relevant feature, and the second stage involves attention-enhanced LIP cells that synchronize to provide feedback on spatial priorities.

The Effect of Aging and Attention on Visual Crowding and Surround Suppression of Perceived Contrast Threshold.

Purpose: The purpose of this study was to study how, in midperipheral vision, aging affects visual processes that interfere with target detection (crowding and surround suppression) and to determine whether the performance on such tasks are related to visuospatial attention as measured by visual search. Methods: We investigated the effect of aging on crowding and suppression in detection of a target in peripheral vision, using different types of flanking stimuli. Both thresholds were also obtained while varying the position of the flanker (placed inside or outside of target, relative to fixation). Crowding thresholds were also estimated with spatial uncertainty (jitter). Additionally, we included a visual search task comprising Gabor stimuli to investigate whether performance is related to top-down attention. Twenty young adults (age, 18-32 years; mean age, 26.1 years; 10 males) and 19 older adults (age, 60-74 years; mean age, 70.3 years; 10 males) participated in the study. Results: Older adults showed more surround suppression than the young (F[1,37] = 4.21; P < 0.05), but crowding was unaffected by age. In the younger group, the position of the flanker influenced the strength of crowding, but not the strength of suppression (F[1,39] = 4.11; P < 0.05). Crowding was not affected by spatial jitter of the stimuli. Neither crowding nor surround suppression was predicted by attentional efficiency measured in the visual search task. There was also no significant correlation between crowding and surround suppression. Conclusions: We show that aging does not affect visual crowding but does increase surround suppression of contrast, suggesting that crowding and surround suppression may be distinct visual phenomena. Furthermore, strengths of crowding and surround suppression did not correlate with each other nor could they be predicted by efficiency of visual search.

Irregularity in neocortical spike trains: influence of measurement factors and another method of estimation.

Irregularity in the interspike interval is a common phenomenon especially in the neocortex. A measure of this random variation in the spacing between neuronal spikes is usually obtained with the coefficient of variation CV (standard deviation/mean interspike interval). In excitable cells, the standard deviation in the interspike interval can be large and the mean firing rate often fluctuates. As a result, there can be substantial variability in the value of the CV computed for the same spike train using only slightly different samples as we show. Moreover, these CV values can be comparatively meaningless unless certain conditions are met. In doing so some researchers have selectively sampled data over a stable mean while others have used a wide range of trial times or subsets thereof (capture window) to compute the CV. This has made interpretation of the raw CV cumbersome. We demonstrate that the CV has a triple sensitivity, namely, for the size of the capture window, the spike count and the refractory period. We assuage these difficulties by introducing a modified term, the coefficient of variation proportion of maximum (CVpm) that offers transportability across different experimental conditions by compensating for the triplet.

Origins of feature selectivities and maps in the mammalian primary visual cortex.

A common feature of the mammalian striate cortex is the arrangement of 'orientation domains' containing neurons preferring similar stimulus orientations. They are arranged as spokes of a pinwheel that converge at singularities known as 'pinwheel centers'. We propose that a cortical network of feedforward and intracortical lateral connections elaborates a full set of optimum orientations from geniculate inputs that show a bias to stimulus orientation and form a set of two or a small number of 'Cartesian' coordinates. Because each geniculate afferent carries signals only from one eye and its receptive field (RF) is either ON or OFF center, the network constructs also ocular dominance columns and a quasi-segregation of ON and OFF responses across the horizontal extent of the striate cortex.