Expansion of direction space around the cardinal axes revealed by smooth pursuit eye movements

It is well established that perceptual direction discrimination shows an oblique effect; thresholds are higher for motion along diagonal directions than for motion along cardinal directions. Here, we compare simultaneous direction judgments and pursuit responses for the same motion stimuli and find that both pursuit and perceptual thresholds show similar anisotropies. The pursuit oblique effect is robust under a wide range of experimental manipulations, being largely resistant to changes in trajectory (radial versus tangential motion), speed (10 versus 25 deg/s), directional uncertainty (blocked versus randomly interleaved), and cognitive state (tracking alone versus concurrent tracking and perceptual tasks). Our data show that the pursuit oblique effect is caused by an effective expansion of direction space surrounding the cardinal directions and the requisite compression of space for other directions. This expansion suggests that the directions around the cardinal directions are in some way overrepresented in the visual cortical pathways that drive both smooth pursuit and perception.     

Predicting human perceptual decisions by decoding neuronal information profiles

Perception relies on the response of populations of neurons in sensory cortex. How the response profile of a neuronal population gives rise to perception and perceptual discrimination has been conceptualized in various ways. Here we suggest that neuronal population responses represent information about our environment explicitly as Fisher information (FI), which is a local measure of the variance estimate of the sensory input. We show how this sensory information can be read out and combined to infer from the available information profile which stimulus value is perceived during a fine discrimination task. In particular, we propose that the perceived stimulus corresponds to the stimulus value that leads to the same information for each of the alternative directions, and compare the model prediction to standard models considered in the literature (population vector, maximum likelihood, maximum-a-posteriori Bayesian inference). The models are applied to human performance in a motion discrimination task that induces perceptual misjudgements of a target direction of motion by task irrelevant motion in the spatial surround of the target stimulus (motion repulsion). By using the neurophysiological insight that surround motion suppresses neuronal responses to the target motion in the center, all models predicted the pattern of perceptual misjudgements. The variation of discrimination thresholds (error on the perceived value) was also explained through the changes of the total FI content with varying surround motion directions. The proposed FI decoding scheme incorporates recent neurophysiological evidence from macaque visual cortex showing that perceptual decisions do not rely on the most active neurons, but rather on the most informative neuronal responses. We statistically compare the prediction capability of the FI decoding approach and the standard decoding models. Notably, all models reproduced the variation of the perceived stimulus values for different surrounds, but with different neuronal tuning characteristics underlying perception. Compared to the FI approach the prediction power of the standard models was based on neurons with far wider tuning width and stronger surround suppression. Our study demonstrates that perceptual misjudgements can be based on neuronal populations encoding explicitly the available sensory information, and provides testable neurophysiological predictions on neuronal tuning characteristics underlying human perceptual decisions.     

Directional anisotropies reveal a functional segregation of visual motion processing for perception and action

Human exhibits an anisotropy in direction perception: discrimination is superior when motion is around horizontal or vertical rather than diagonal axes. In contrast to the consistent directional anisotropy in perception, we found only small idiosyncratic anisotropies in smooth pursuit eye movements, a motor action requiring accurate discrimination of visual motion direction. Both pursuit and perceptual direction discrimination rely on signals from the middle temporal visual area (MT), yet analysis of multiple measures of MT neuronal responses in the macaque failed to provide evidence of a directional anisotropy. We conclude that MT represents different motion directions uniformly, and subsequent processing creates a directional anisotropy in pathways unique to perception. Our data support the hypothesis that, at least for visual motion, perception and action are guided by inputs from separate sensory streams. The directional anisotropy of perception appears to originate after the two streams have segregated and downstream from area MT.     

The hierarchy of directional interactions in visual motion processing

It is well known that context influences our perception of visual motion direction. For example, spatial and temporal context manipulations can be used to induce two well-known motion illusions: direction repulsion and the direction after-effect (DAE). Both result in inaccurate perception of direction when a moving pattern is either superimposed on (direction repulsion), or presented following adaptation to (DAE), another pattern moving in a different direction. Remarkable similarities in tuning characteristics suggest that common processes underlie the two illusions. What is not clear, however, is whether the processes driving the two illusions are expressions of the same or different neural substrates. Here we report two experiments demonstrating that direction repulsion and the DAE are, in fact, expressions of different neural substrates. Our strategy was to use each of the illusions to create a distorted perceptual representation upon which the mechanisms generating the other illusion could potentially operate. We found that the processes mediating direction repulsion did indeed access the distorted perceptual representation induced by the DAE. Conversely, the DAE was unaffected by direction repulsion. Thus parallels in perceptual phenomenology do not necessarily imply common neural substrates. Our results also demonstrate that the neural processes driving the DAE occur at an earlier stage of motion processing than those underlying direction repulsion.     

Neural correlates of contrast detection at threshold

Human psychophysical studies have demonstrated that, for stimuli near the threshold of visibility, detection of motion in one direction is unaffected by the superimposition of motion in the opposite direction. To investigate the neural basis for this perceptual phenomenon, we recorded from directionally selective neurons in macaque visual area MT (middle temporal visual area). Contrast thresholds obtained for single gratings moving in a neuron's preferred direction were compared with those obtained for motion presented simultaneously in the neuron's preferred and antipreferred directions. A simple model based on probability summation between neurons tuned to opposite directions could sufficiently account for contrast thresholds revealed psychophysically, suggesting that area MT is likely to provide the neural basis for contrast detection of stimuli modulated in time.     

Effects of Isoflurane Anesthesia on Ensemble Patterns of Ca2+ Activity in Mouse V1: Reduced Direction Selectivity Independent of Increased Correlations in Cellular Activity

Anesthesia affects brain activity at the molecular, neuronal and network level, but it is not well-understood how tuning properties of sensory neurons and network connectivity change under its influence. Using in vivo two-photon calcium imaging we matched neuron identity across episodes of wakefulness and anesthesia in the same mouse and recorded spontaneous and visually evoked activity patterns of neuronal ensembles in these two states. Correlations in spontaneous patterns of calcium activity between pairs of neurons were increased under anesthesia. While orientation selectivity remained unaffected by anesthesia, this treatment reduced direction selectivity, which was attributable to an increased response to the null-direction. As compared to anesthesia, populations of V1 neurons coded more mutual information on opposite stimulus directions during wakefulness, whereas information on stimulus orientation differences was lower. Increases in correlations of calcium activity during visual stimulation were correlated with poorer population coding, which raised the hypothesis that the anesthesia-induced increase in correlations may be causal to degrading directional coding. Visual stimulation under anesthesia, however, decorrelated ongoing activity patterns to a level comparable to wakefulness. Because visual stimulation thus appears to ‘break’ the strength of pairwise correlations normally found in spontaneous activity under anesthesia, the changes in correlational structure cannot explain the awake-anesthesia difference in direction coding. The population-wide decrease in coding for stimulus direction thus occurs independently of anesthesia-induced increments in correlations of spontaneous activity.     

纹外皮层PMLS区反馈投射对初级视皮层神经元反应特性的影响

神经系统中存在大量下行投射,与上行输入一起形成复杂的前馈与反馈回路,调控神经信号的传导和处理,但目前对皮层内反馈投射的功能作用认识还比较薄弱.通过微量注射抑制性神经递质γ-氨基丁酸(γ-aminobutyric acid,GABA),使猫纹外皮层后内侧外上雪氏区(area posteromedial lateral suprasylvian,PMLS)局部可逆性失活,使用胞外记录方法,研究初级视皮层17区神经元反应特性的变化.实验结果显示,PMLS区失活后,17区细胞对运动刺激的反应总体减弱,反应的相对稳定性基本不变,最高发放率/自发之比有所下降.与此同时,细胞的方向选择性指数减小,朝向选择性无显著变化.除少数"双向"反应细胞外,绝大部分细胞的最优方向基本不变.进一步分析发现,细胞对各个方向刺激的反应普遍下降,最优方向上的下降程度最大,是导致方向选择性减弱的主要原因.这些结果表明,PMLS区反馈投射可增强初级视皮层的方向选择性,而对朝向选择性影响有限.这一作用特点体现了PMLS区在皮层中偏重处理运动视觉信息的功能.     

Defining the V5/MT neuronal pool for perceptual decisions in a visual stereo-motion task

In the primate visual cortex, neurons signal differences in the appearance of objects with high precision. However, not all activated neurons contribute directly to perception. We defined the perceptual pool in extrastriate visual area V5/MT for a stereo-motion task, based on trial-by-trial co-variation between perceptual decisions and neuronal firing (choice probability (CP)). Macaque monkeys were trained to discriminate the direction of rotation of a cylinder, using the binocular depth between the moving dots that form its front and rear surfaces. We manipulated the activity of single neurons trial-to-trial by introducing task-irrelevant stimulus changes: dot motion in cylinders was aligned with neuronal preference on only half the trials, so that neurons were strongly activated with high firing rates on some trials and considerably less activated on others. We show that single neurons maintain high neurometric sensitivity for binocular depth in the face of substantial changes in firing rate. CP was correlated with neurometric sensitivity, not level of activation. In contrast, for individual neurons, the correlation between perceptual choice and neuronal activity may be fundamentally different when responding to different stimulus versions. Therefore, neuronal pools supporting sensory discrimination must be structured flexibly and independently for each stimulus configuration to be discriminated.This article is part of the themed issue ‘Vision in our three-dimensional world''.     

Motion Noise Changes Directional Interaction between Transparently Moving Stimuli from Repulsion to Attraction

To interpret visual scenes, visual systems need to segment or integrate multiple moving features into distinct objects or surfaces. Previous studies have found that the perceived direction separation between two transparently moving random-dot stimuli is wider than the actual direction separation. This perceptual “direction repulsion” is useful for segmenting overlapping motion vectors. Here we investigate the effects of motion noise on the directional interaction between overlapping moving stimuli. Human subjects viewed two overlapping random-dot patches moving in different directions and judged the direction separation between the two motion vectors. We found that the perceived direction separation progressively changed from wide to narrow as the level of motion noise in the stimuli was increased, showing a switch from direction repulsion to attraction (i.e. smaller than the veridical direction separation). We also found that direction attraction occurred at a wider range of direction separations than direction repulsion. The normalized effects of both direction repulsion and attraction were the strongest near the direction separation of ∼25° and declined as the direction separation further increased. These results support the idea that motion noise prompts motion integration to overcome stimulus ambiguity. Our findings provide new constraints on neural models of motion transparency and segmentation.     

Stability of cortical responses and the statistics of natural scenes.

The primary visual cortex (V1) of higher mammals contains maps of stimulus features; how these maps influence vision remains unknown. We have examined the functional significance of an asymmetry in the orientation map in cat V1, i.e., the fact that a larger area of V1 is preferentially activated by vertical and horizontal contours than by contours at oblique orientations. Despite the fact that neurons tuned to cardinal and oblique orientations have indistinguishable tuning characteristics, cardinal neurons remain more stable in their response properties after selective perturbation induced by adaptation. Similarly, human observers report different adaptation-induced changes in orientation tuning between cardinal and oblique axes. We suggest that the larger cortical area devoted to cardinal orientations imposes stability on the processing of cardinal contours during visual perception, by retaining invariant cortical responses along cardinal axes.     

A visual pathway links brain structures active during magnetic compass orientation in migratory birds

The magnetic compass of migratory birds has been suggested to be light-dependent. Retinal cryptochrome-expressing neurons and a forebrain region, "Cluster N", show high neuronal activity when night-migratory songbirds perform magnetic compass orientation. By combining neuronal tracing with behavioral experiments leading to sensory-driven gene expression of the neuronal activity marker ZENK during magnetic compass orientation, we demonstrate a functional neuronal connection between the retinal neurons and Cluster N via the visual thalamus. Thus, the two areas of the central nervous system being most active during magnetic compass orientation are part of an ascending visual processing stream, the thalamofugal pathway. Furthermore, Cluster N seems to be a specialized part of the visual wulst. These findings strongly support the hypothesis that migratory birds use their visual system to perceive the reference compass direction of the geomagnetic field and that migratory birds "see" the reference compass direction provided by the geomagnetic field.     

Spatial and Feature-Based Attention in a Layered Cortical Microcircuit Model

Directing attention to the spatial location or the distinguishing feature of a visual object modulates neuronal responses in the visual cortex and the stimulus discriminability of subjects. However, the spatial and feature-based modes of attention differently influence visual processing by changing the tuning properties of neurons. Intriguingly, neurons'' tuning curves are modulated similarly across different visual areas under both these modes of attention. Here, we explored the mechanism underlying the effects of these two modes of visual attention on the orientation selectivity of visual cortical neurons. To do this, we developed a layered microcircuit model. This model describes multiple orientation-specific microcircuits sharing their receptive fields and consisting of layers 2/3, 4, 5, and 6. These microcircuits represent a functional grouping of cortical neurons and mutually interact via lateral inhibition and excitatory connections between groups with similar selectivity. The individual microcircuits receive bottom-up visual stimuli and top-down attention in different layers. A crucial assumption of the model is that feature-based attention activates orientation-specific microcircuits for the relevant feature selectively, whereas spatial attention activates all microcircuits homogeneously, irrespective of their orientation selectivity. Consequently, our model simultaneously accounts for the multiplicative scaling of neuronal responses in spatial attention and the additive modulations of orientation tuning curves in feature-based attention, which have been observed widely in various visual cortical areas. Simulations of the model predict contrasting differences between excitatory and inhibitory neurons in the two modes of attentional modulations. Furthermore, the model replicates the modulation of the psychophysical discriminability of visual stimuli in the presence of external noise. Our layered model with a biologically suggested laminar structure describes the basic circuit mechanism underlying the attention-mode specific modulations of neuronal responses and visual perception.     

United we sense, divided we fail: context-driven perception of ambiguous visual stimuli

Ambiguous visual stimuli provide the brain with sensory information that contains conflicting evidence for multiple mutually exclusive interpretations. Two distinct aspects of the phenomenological experience associated with viewing ambiguous visual stimuli are the apparent stability of perception whenever one perceptual interpretation is dominant, and the instability of perception that causes perceptual dominance to alternate between perceptual interpretations upon extended viewing. This review summarizes several ways in which contextual information can help the brain resolve visual ambiguities and construct temporarily stable perceptual experiences. Temporal context through prior stimulation or internal brain states brought about by feedback from higher cortical processing levels may alter the response characteristics of specific neurons involved in rivalry resolution. Furthermore, spatial or crossmodal context may strengthen the neuronal representation of one of the possible perceptual interpretations and consequently bias the rivalry process towards it. We suggest that contextual influences on perceptual choices with ambiguous visual stimuli can be highly informative about the neuronal mechanisms of context-driven inference in the general processes of perceptual decision-making.     

Perceptual “Read-Out” of Conjoined Direction and Disparity Maps in Extrastriate Area MT

Cortical neurons are frequently tuned to several stimulus dimensions, and many cortical areas contain intercalated maps of multiple variables. Relatively little is known about how information is “read out” of these multidimensional maps. For example, how does an organism extract information relevant to the task at hand from neurons that are also tuned to other, irrelevant stimulus dimensions? We addressed this question by employing microstimulation techniques to examine the contribution of disparity-tuned neurons in the middle temporal (MT) visual area to performance on a direction discrimination task. Most MT neurons are tuned to both binocular disparity and the direction of stimulus motion, and MT contains topographic maps of both parameters. We assessed the effect of microstimulation on direction judgments after first characterizing the disparity tuning of each stimulation site. Although the disparity of the stimulus was irrelevant to the required task, we found that microstimulation effects were strongly modulated by the disparity tuning of the stimulated neurons. For two of three monkeys, microstimulation of nondisparity-selective sites produced large biases in direction judgments, whereas stimulation of disparity-selective sites had little or no effect. The binocular disparity was optimized for each stimulation site, and our result could not be explained by variations in direction tuning, response strength, or any other tuning property that we examined. When microstimulation of a disparity-tuned site did affect direction judgments, the effects tended to be stronger at the preferred disparity of a stimulation site than at the nonpreferred disparity, indicating that monkeys can selectively monitor direction columns that are best tuned to an appropriate conjunction of parameters. We conclude that the contribution of neurons to behavior can depend strongly upon tuning to stimulus dimensions that appear to be irrelevant to the current task, and we suggest that these findings are best explained in terms of the strategy used by animals to perform the task.     

Specificity of sensorimotor learning and the neural code: Neuronal representations in the primary motor cortex

Human studies show that the learning of a new sensorimotor mapping that requires adaptation to directional errors is local and generalizes poorly to untrained directions. We trained monkeys to learn new visuomotor rotations for only one target in space and recorded neuronal activity in the primary motor cortex before, during and after learning. Similar to humans, the monkeys showed poor transfer of learning to other directions, as observed by behavioral aftereffects for untrained directions. To test for internal representations underlying these changes, we compared two features of neuronal activity before and after learning: changes in firing rates and changes in information content. Specific elevations of firing rate were only observed in a subpopulation of cells in the motor cortex with directional properties corresponding to the locally learned rotation; namely cells only showed plasticity if their preferred direction was near the training one. We applied measures from information theory to probe for learning-related changes in the neuronal code. Single cells conveyed more information about the direction of movement and this specific improvement in encoding was correlated with an increase in the slope of the neurons' tuning curve. Further, the improved information after learning enabled a more accurate reconstruction of movement direction from neuronal populations. Our findings suggest a neural mechanism for the confined generalization of a newly acquired internal model by showing a tight relationship between the locality of learning and the properties of neurons. They also provide direct evidence for improvement in the neural code as a result of learning.     

Attention to stimulus features shifts spectral tuning of V4 neurons during natural vision

Previous neurophysiological studies suggest that attention can alter the baseline or gain of neurons in extrastriate visual areas but that it cannot change tuning. This suggests that neurons in visual cortex function as labeled lines whose meaning does not depend on task demands. To test this common assumption, we used a system identification approach to measure spatial frequency and orientation tuning in area V4 during two attentionally demanding visual search tasks, one that required fixation and one that allowed free viewing during search. We found that spatial attention modulates response baseline and gain but does not alter tuning, consistent with previous reports. In contrast, feature-based attention often shifts neuronal tuning. These tuning shifts are inconsistent with the labeled-line model and tend to enhance responses to stimulus features that distinguish the search target. Our data suggest that V4 neurons behave as matched filters that are dynamically tuned to optimize visual search.     

Perisaccadic mislocalization orthogonal to saccade direction

Saccadic eye movements transiently distort perceptual space. Visual objects flashed shortly before or during a saccade are mislocalized along the saccade direction, resembling a compression of space around the saccade target. These mislocalizations reflect transient errors of processes that construct spatial stability across eye movements. They may arise from errors of reference signals associated with saccade direction and amplitude or from visual or visuomotor remapping processes focused on the saccade target's position. The second case would predict apparent position shifts toward the target also in directions orthogonal to the saccade. We report that such orthogonal mislocalization indeed occurs. Surprisingly, however, the orthogonal mislocalization is restricted to only part of the visual field. This part comprises distant positions in saccade direction but does not depend on the target's position. Our findings can be explained by a combination of directional and positional reference signals that varies in time course across the visual field.     

Feature-based attention increases the selectivity of population responses in primate visual cortex

BACKGROUND: Attending to the spatial location or to nonspatial features of visual stimuli can modulate neuronal responses in primate visual cortex. The modulation by spatial attention changes the gain of sensory neurons and strengthens the representation of attended locations without changing neuronal selectivities such as directionality, i.e., the ratio of responses to preferred and anti-preferred directions of motion. Whether feature-based attention acts in a similar manner is unknown. RESULTS: To clarify this issue, we recorded the responses of 135 direction-selective neurons in the middle temporal area (MT) of two macaques to an unattended moving random dot pattern (the distractor) positioned inside a neuron's receptive field while the animals attended to a second moving pattern positioned in the opposite hemifield. Responses to different directions of the distractor were modulated by the same factor (approximately 12%) as long as the attended direction remained unchanged. On the other hand, systematically changing the attended direction from a neuron's preferred to its anti-preferred direction caused a systematic change of the attentional modulation from an enhancement to a suppression, increasing directionality by about 20%. CONCLUSIONS: The results show that (1) feature-based attention exerts a multiplicative modulation upon neuronal responses and that the strength of this modulation depends on the similarity between the attended feature and the cell's preferred feature, in line with the feature-similarity gain model, and (2) at the level of the neuronal population, feature-based attention increases the selectivity for attended features by increasing the responses of neurons preferring this feature value while decreasing responses of neurons tuned to the opposite feature value.     

Stimulus timing-dependent plasticity in high-level vision

Humans are able to efficiently learn and remember complex visual patterns after only a few seconds of exposure [1]. At a cellular level, such learning is thought to involve changes in synaptic efficacy, which have been linked to the precise timing of action potentials relative to synaptic inputs [2-4]. Previous experiments have tapped into the timing of neural spiking events by using repeated asynchronous presentation of visual stimuli to induce changes in both the tuning properties of visual neurons and the perception of simple stimulus attributes [5, 6]. Here we used a similar approach to investigate potential mechanisms underlying the perceptual learning of face identity, a high-level stimulus property based on the spatial configuration of local features. Periods of stimulus pairing induced a systematic bias in face-identity perception in a manner consistent with the predictions of spike timing-dependent plasticity. The perceptual shifts induced for face identity were tolerant to a 2-fold change in stimulus size, suggesting that they reflected neuronal changes in nonretinotopic areas, and were more than twice as strong as the perceptual shifts induced for low-level visual features. These results support the idea that spike timing-dependent plasticity can rapidly adjust the neural encoding of high-level stimulus attributes [7-11].