Representation of cardinal contour overlaps less with representation of nearby angles in cat visual cortex

Extensive attempts have been made to explain the neurobiological basis of the greater sensitivity of the visual system to vertically or horizontally oriented information than to information presented at oblique angles. However, investigators have largely ignored the overlap of the representation of a given angle with the representation of nearby angles. Recordings based on intrinsic optical signals were obtained in area 17 from 12 adult cats during the presentation of contours in various orientations. A method investigating both amplitude and statistical significance of changes was proposed to evaluate the orientation tuning properties for cell populations in the central area retinotopically corresponding to 0-15 degrees of visual field. Cardinal orientations were found to activate significantly greater areas in the exposed cortical area than the areas activated by oblique orientations. Areas activated by cardinal or oblique contours and those separated from them by 10 degrees were compared. A significantly lower degree of overlap was seen between areas activated by presentation of cardinal contours and areas activated by neighboring orientations compared with those for oblique orientations which overlapped more extensively with neighboring orientations. In addition, areas activated only by cardinal contours were significantly larger than areas activated only by oblique contours. These results demonstrated in cell population level that more cells prefer horizontal or vertical orientations, and these cells are tuned more sharply than oblique selective cells.     

Computational approaches to spatial orientation: from transfer functions to dynamic Bayesian inference

Spatial orientation is the sense of body orientation and self-motion relative to the stationary environment, fundamental to normal waking behavior and control of everyday motor actions including eye movements, postural control, and locomotion. The brain achieves spatial orientation by integrating visual, vestibular, and somatosensory signals. Over the past years, considerable progress has been made toward understanding how these signals are processed by the brain using multiple computational approaches that include frequency domain analysis, the concept of internal models, observer theory, Bayesian theory, and Kalman filtering. Here we put these approaches in context by examining the specific questions that can be addressed by each technique and some of the scientific insights that have resulted. We conclude with a recent application of particle filtering, a probabilistic simulation technique that aims to generate the most likely state estimates by incorporating internal models of sensor dynamics and physical laws and noise associated with sensory processing as well as prior knowledge or experience. In this framework, priors for low angular velocity and linear acceleration can explain the phenomena of velocity storage and frequency segregation, both of which have been modeled previously using arbitrary low-pass filtering. How Kalman and particle filters may be implemented by the brain is an emerging field. Unlike past neurophysiological research that has aimed to characterize mean responses of single neurons, investigations of dynamic Bayesian inference should attempt to characterize population activities that constitute probabilistic representations of sensory and prior information.     

Tilt aftereffect and adaptation-induced changes in orientation tuning in visual cortex

The tilt aftereffect (TAE) is a visual illusion in which prolonged adaptation to an oriented stimulus causes shifts in subsequent perceived orientations. Historically, neural models of the TAE have explained it as the outcome of response suppression of neurons tuned to the adapting orientation. Recent physiological studies of neurons in primary visual cortex (V1) have confirmed that such response suppression exists. However, it was also found that the preferred orientations of neurons shift away from the adapting orientation. Here we show that adding this second factor to a population coding model of V1 improves the correspondence between neurophysiological data and TAE measurements. According to our model, the shifts in preferred orientation have the opposite effect as response suppression, reducing the magnitude of the TAE.     

Weakened feedback abolishes neural oblique effect evoked by pseudo-natural visual stimuli in area 17 of the cat

The psychological oblique effect, a well-known phenomenon that humans and some mammals are more visually sensitive to cardinal (vertical and horizontal) contours than to oblique ones, has commonly been associated with the overrepresentation of cardinal orientations in the visual cortex. In contrast to the oblique effect, however, Essock et al. [E.A. Essock, J.K. DeFord, B.C. Hansen, M.J. Sinai, Oblique stimuli are seen best (not worst!) broad-band stimuli: a horizontal effect, Vision Res. 43 (2003) 1329–1335] reported a psychological ‘horizontal effect’, in which visual stimuli dominated by oblique orientations were best perceived by human subjects when tested with unique natural broad-band stimuli. In this study, using optical imaging and the similar visual stimuli, we found an overrepresentation of cardinal orientations, i.e. the neural oblique effect, but not ‘horizontal effect’, in area 17 of the cat. In addition, the oblique effect was abolished by GABA administration in area 21a due to the preferred orientation shifting (6.0%) and decrease of orientation selectivity strength of neurons (26.9%) in area 17. These results indicate a neuronal basis of the oblique effect when animals watch a more natural scene, whereas no evidence was found for the ‘horizontal effect’.     

Influence of visual attention upon sound localization]

Previous studies on audio-visual interaction such as the ventriloquism effect have indicated cognitive (or context) factors as well as sensory (or synchronous) factors could make the interaction. In these studies, however, visual attention seems to have been neglected. Thus, it has been still unknown whether the visual attention affects the interaction or not. We investigated the contribution of the attention factors to the audio-visual interaction by comparing the sound localization biases made by attentional factors and those by synchronous factors. Three subjects participated in the localization tasks in horizontal and vertical orientations. As the results, we found small influence of the attentional factors upon the interaction in the horizontal orientation, and no influence in the vertical orientation. On the contrary, the effect of the synchronous factors was larger in the vertical orientation than in the horizontal orientation. We concluded that the visual attention could affect the audio-visual interaction slightly, and that the influences of the attentional factors and the perceptual factors upon the interactions were made in the different processes.     

Perceptual learning as improved probabilistic inference in early sensory areas

Extensive training on simple tasks such as fine orientation discrimination results in large improvements in performance, a form of learning known as perceptual learning. Previous models have argued that perceptual learning is due to either sharpening and amplification of tuning curves in early visual areas or to improved probabilistic inference in later visual areas (at the decision stage). However, early theories are inconsistent with the conclusions of psychophysical experiments manipulating external noise, whereas late theories cannot explain the changes in neural responses that have been reported in cortical areas V1 and V4. Here we show that we can capture both the neurophysiological and behavioral aspects of perceptual learning by altering only the feedforward connectivity in a recurrent network of spiking neurons so as to improve probabilistic inference in early visual areas. The resulting network shows modest changes in tuning curves, in line with neurophysiological reports, along with a marked reduction in the amplitude of pairwise noise correlations.     

Orientation sensitivity of cat LGN neurones with and without inputs from visual cortical areas 17 and 18

Summary Orientation sensitivity was tested, using moving bars as stimuli, in 136 LGN cells in normal cats and 82 LGN cells in cats with areas 17 and 18 lesioned.The responses of most neurones showed some dependence on the orientation of the line stimulus. The orientation bias was more pronounced for long, narrow bars moving at rather slow velocities. Length-response curves revealed less end-inhibition along the optimum orientation than along the nonoptimum orientation. Thirty-two percent of the cells in the normal cats and 50% in the lesioned animals responded best to orientations within 10 ° of the vertical or horizontal. The oblique orientations were represented poorly in the lesioned group. Thus the corticogeniculate feedback may serve to confer a more uniform distribution of orientation preferences on the LGN.It is suggested that the orientation biases of LGN neurones may play a role in building orientation-selective cells in the visual cortex. Further, the preferences for horizontal and vertical orientations in the LGN may explain the preferences for these orientations reported for visual cortical cells.     

Multisensory determinants of orientation perception in Parkinson's disease

Perception of the relative orientation of the self and objects in the environment requires integration of visual and vestibular sensory information, and an internal representation of the body's orientation. Parkinson's disease (PD) patients are more visually dependent than controls, implicating the basal ganglia in using visual orientation cues. We examined the relative roles of visual and non-visual cues to orientation in PD using two different measures: the subjective visual vertical (SVV) and the perceptual upright (PU). We tested twelve PD patients (nine both on- and off-medication), and thirteen age-matched controls. Visual, vestibular and body cues were manipulated using a polarized visual room presented in various orientations while observers were upright or lying right-side-down. Relative to age-matched controls, patients with PD showed more influence of visual cues for the SVV but were more influenced by the direction of gravity for the PU. Increased SVV visual dependence corresponded with equal decreases of the contributions of body sense and gravity. Increased PU gravitational dependence corresponded mainly with a decreased contribution of body sense. Curiously however, both of these effects were significant only when patients were medicated. Increased SVV visual dependence was highest for PD patients with left-side initial motor symptoms. PD patients when on and off medication were more variable than controls when making judgments. Our results suggest that (i) PD patients are not more visually dependent in general, rather increased visual dependence is task specific and varies with initial onset side, (ii) PD patients may rely more on vestibular information for some perceptual tasks which is reflected in relying less on the internal representation of the body, and (iii) these effects are only present when PD patients are taking dopaminergic medication.     

Decoding the visual and subjective contents of the human brain

The potential for human neuroimaging to read out the detailed contents of a person's mental state has yet to be fully explored. We investigated whether the perception of edge orientation, a fundamental visual feature, can be decoded from human brain activity measured with functional magnetic resonance imaging (fMRI). Using statistical algorithms to classify brain states, we found that ensemble fMRI signals in early visual areas could reliably predict on individual trials which of eight stimulus orientations the subject was seeing. Moreover, when subjects had to attend to one of two overlapping orthogonal gratings, feature-based attention strongly biased ensemble activity toward the attended orientation. These results demonstrate that fMRI activity patterns in early visual areas, including primary visual cortex (V1), contain detailed orientation information that can reliably predict subjective perception. Our approach provides a framework for the readout of fine-tuned representations in the human brain and their subjective contents.     

Visual properties of neurons in the thalamus and striopallidar complex of the human brain

In parkinsonian patients diagnosed and treated with the aid of long-term intracerebral electrodes, neuronal impulse activity (NIA) was recorded in different nuclei of the thalamus and striopallidar complex during visual testing for orientation sensitivity. Neuronal populations responding only to the presented stimuli with specific angular orientations have been revealed. Orientation-selective neurons have been found with significant responses in NIA observed to the same angular orientations of stimuli during 90 degrees head tilts. It is hypothesized that the visual perception constancy can be maintained with the participation of cerebral nuclei containing such neurons on the basis of convergence of motor, somatosensory and visual information.     

Experience-dependent orientation plasticity in the visual cortex of rats chronically exposed to a single orientation

We used the intrinsic signal optical imaging technique to assess the effect of orientation-restricted visual experience on response properties of the rat visual cortex. We placed young animals wearing goggles fitted with plano-convex cylindrical lenses in a stimulus-enriched environment for 3 weeks. Experienced orientation was over-represented in the visual cortex, which was associated with the under-representation of orthogonal orientation. These findings suggest that chronic exposure to a single orientation can modify orientation preferences even in rats lacking in orderly arrangement of preferred orientations.     

An anisotropy of human tactile sensitivity and its relation to the visual oblique effect

Summary The ability of humans to detect striated stimuli on the distal phalanges was found to be highly anisotropic. Observers were much more sensitive to stripes presented in the proximal-distal orientation than to stripes in any other orientation. This tactile anisotropy was contrasted with the well-known visual anisotropy in which sensitivity is greatest for stripes at the horizontal and vertical orientations. We suggest that both the tactile anisotropy and the visual anisotropy are caused by corresponding anisotropies in the distribution of preferred orientations of orientation-selective neurons with in the respective modalities.     

Predicting the orientation of invisible stimuli from activity in human primary visual cortex

Humans can experience aftereffects from oriented stimuli that are not consciously perceived, suggesting that such stimuli receive cortical processing. Determining the physiological substrate of such effects has proven elusive owing to the low spatial resolution of conventional human neuroimaging techniques compared to the size of orientation columns in visual cortex. Here we show that even at conventional resolutions it is possible to use fMRI to obtain a direct measure of orientation-selective processing in V1. We found that many parts of V1 show subtle but reproducible biases to oriented stimuli, and that we could accumulate this information across the whole of V1 using multivariate pattern recognition. Using this information, we could then successfully predict which one of two oriented stimuli a participant was viewing, even when masking rendered that stimulus invisible. Our findings show that conventional fMRI can be used to reveal feature-selective processing in human cortex, even for invisible stimuli.     

Influence of experience on orientation maps in cat visual cortex.

Experience is known to affect the development of ocular dominance maps in visual cortex, but it has remained controversial whether orientation preference maps are similarly affected by limiting visual experience to a single orientation early in life. Here we used optical imaging based on intrinsic signals to show that the visual cortex of kittens reared in a striped environment responded to all orientations, but devoted up to twice as much surface area to the experienced orientation as the orthogonal one. This effect is due to an instructive role of visual experience whereby some neurons shift their orientation preferences toward the experienced orientation. Thus, although cortical orientation maps are remarkably rigid in the sense that orientations that have never been seen by the animal occupy a large portion of the cortical territory, visual experience can nevertheless alter neuronal responses to oriented contours.     

An oblique effect in human primary visual cortex

Visual perception critically depends on orientation-specific signals that arise early in visual processing. Humans show greater behavioral sensitivity to gratings with horizontal or vertical (0 degrees /90 degrees; 'cardinal') orientations than to other, 'oblique' orientations. Here we used functional magnetic resonance imaging (fMRI) to measure an asymmetry in the responses of human primary visual cortex (V1) to oriented stimuli. We found that neural responses in V1 were larger for cardinal stimuli than for oblique (45 degrees /135 degrees ) stimuli. Thus the fMRI pattern in V1 closely resembled subjects' behavioral judgments; responses in V1 were greater for those orientations that yielded better perceptual performance.     

Orientation tuning of input conductance, excitation, and inhibition in cat primary visual cortex

The input conductance of cells in the cat primary visual cortex (V1) has been shown recently to grow substantially during visual stimulation. Because increasing conductance can have a divisive effect on the synaptic input, theoretical proposals have ascribed to it specific functions. According to the veto model, conductance increases would serve to sharpen orientation tuning by increasing most at off-optimal orientations. According to the normalization model, conductance increases would control the cell's gain, by being independent of stimulus orientation and by growing with stimulus contrast. We set out to test these proposals and to determine the visual properties and possible synaptic origin of the conductance increases. We recorded the membrane potential of cat V1 cells while injecting steady currents and presenting drifting grating patterns of varying contrast and orientation. Input conductance grew with stimulus contrast by 20-300%, generally more in simple cells (40-300%) than in complex cells (20-120%), and in simple cells was strongly modulated in time. Conductance was invariably maximal for stimuli of the preferred orientation. Thus conductance changes contribute to a gain control mechanism, but the strength of this gain control does not depend uniquely on contrast. By assuming that the conductance changes are entirely synaptic, we further derived the excitatory and inhibitory synaptic conductances underlying the visual responses. In simple cells, these conductances were often arranged in push-pull: excitation increased when inhibition decreased and vice versa. Excitation and inhibition had similar preferred orientations and did not appear to differ in tuning width, suggesting that the intracortical synaptic inputs to simple cells of cat V1 originate from cells with similar orientation tuning. This finding is at odds with models where orientation tuning in simple cells is achieved by inhibition at off-optimal orientations or sharpened by inhibition that is more broadly tuned than excitation.     

The effect of altered gravity states on the perception of orientation

We measured the effect of the orientation of the visual background on the perceptual upright (PU) under different levels of gravity. Brief periods of micro- and hypergravity conditions were created using two series of parabolic flights. Control measures were taken in the laboratory under normal gravity with subjects upright, right side down and supine. Participants viewed a polarized, natural scene presented at various orientations on a laptop viewed through a hood which occluded all other visual cues. Superimposed on the screen was a character the identity of which depended on its orientation. The orientations at which the character was maximally ambiguous were measured and the perceptual upright was defined as half way between these orientations. The visual background affected the orientation of the PU less when in microgravity than when upright in normal gravity and more when supine than when upright in normal gravity. A weighted vector sum model was used to quantify the relative influence of the orientations of gravity, vision and the body in determining the perceptual upright.

Stereoscopic occlusion junctions.

Portions of surfaces in a binocularly viewed scene may be 'half occluded', that is, visible in only one eye. The human visual system uses zones of half occlusion to help segment the visual scene and infer figure-ground relationships at object boundaries. We developed a quantitative model of the depth-discontinuity cue provided by half occlusion. Half occlusions are revealed by two-dimensional interocular displacements of binocularly viewed occlusion junctions, such as T junctions. We derived a formula relating this two-dimensional displacement, or 'pseudodisparity', to binocular disparities and orientations of occluding and occluded contours. In human psychophysical experiments, perceived depth and contour orientation quantitatively depended on pseudodisparity, as predicted by our model, implying that the visual system senses quantitative variations in interocular junction position to reconstruct occlusion geometry.     

Mapping of stimulus energy in primary visual cortex

A recent optical imaging study of primary visual cortex (V1) by Basole, White, and Fitzpatrick demonstrated that maps of preferred orientation depend on the choice of stimuli used to measure them. These authors measured population responses expressed as a function of the optimal orientation of long drifting bars. They then varied bar length, direction, and speed and found that stimuli of a same orientation can elicit different population responses and stimuli with different orientation can elicit similar population responses. We asked whether these results can be explained from known properties of V1 receptive fields. We implemented an "energy model" where a receptive field integrates stimulus energy over a region of three-dimensional frequency space. The population of receptive fields defines a volume of visibility, which covers all orientations and a plausible range of spatial and temporal frequencies. This energy model correctly predicts the population response to bars of different length, direction, and speed and explains the observations made with optical imaging. The model also readily explains a related phenomenon, the appearance of motion streaks for fast-moving dots. We conclude that the energy model can be applied to activation maps of V1 and predicts phenomena that may otherwise appear to be surprising. These results indicate that maps obtained with optical imaging reflect the layout of neurons selective for stimulus energy, not for isolated stimulus features such as orientation, direction, and speed.     

Mechanisms of visual motion detection

Visual motion is processed by neurons in primary visual cortex that are sensitive to spatial orientation and speed. Many models of local velocity computation are based on a second stage that pools the outputs of first-stage neurons selective for different orientations, but the nature of this pooling remains controversial. In a human psychophysical detection experiment, we found near-perfect summation of image energy when it was distributed uniformly across all orientations, but poor summation when it was concentrated in specific orientation bands. The data are consistent with a model that integrates uniformly over all orientations, even when this strategy is sub-optimal.