Top-down gain control of the auditory space map by gaze control circuitry in the barn owl

High-level circuits in the brain that control the direction of gaze are intimately linked with the control of visual spatial attention. Immediately before an animal directs its gaze towards a stimulus, both psychophysical sensitivity to that visual stimulus and the responsiveness of high-order neurons in the cerebral cortex that represent the stimulus increase dramatically. Equivalent effects on behavioural sensitivity and neuronal responsiveness to visual stimuli result from focal electrical microstimulation of gaze control centres in monkeys. Whether the gaze control system modulates neuronal responsiveness in sensory modalities other than vision is unknown. Here we show that electrical microstimulation applied to gaze control circuitry in the forebrain of barn owls regulates the gain of midbrain auditory responses in an attention-like manner. When the forebrain circuit was activated, midbrain responses to auditory stimuli at the location encoded by the forebrain site were enhanced and spatial selectivity was sharpened. The same stimulation suppressed responses to auditory stimuli represented at other locations in the midbrain map. Such space-specific, top-down regulation of auditory responses by gaze control circuitry in the barn owl suggests that the central nervous system uses a common strategy for dynamically regulating sensory gain that applies across modalities, brain areas and classes of vertebrate species. This approach provides a path for discovering mechanisms that underlie top-down gain control in the central nervous system.     

Hearing visual motion in depth

Auditory spatial perception is strongly affected by visual cues. For example, if auditory and visual stimuli are presented synchronously but from different positions, the auditory event is mislocated towards the locus of the visual stimulus-the ventriloquism effect. This 'visual capture' also occurs in motion perception in which a static auditory stimulus appears to move with the visual moving object. We investigated how the human perceptual system coordinates complementary inputs from auditory and visual senses. Here we show that an auditory aftereffect occurs from adaptation to visual motion in depth. After a few minutes of viewing a square moving in depth, a steady sound was perceived as changing loudness in the opposite direction. Adaptation to a combination of auditory and visual stimuli changing in a compatible direction increased the aftereffect and the effect of visual adaptation almost disappeared when the directions were opposite. On the other hand, listening to a sound changing in intensity did not affect the visual changing-size aftereffect. The results provide psychophysical evidence that, for processing of motion in depth, the auditory system responds to both auditory changing intensity and visual motion in depth.     

Adaptive coding of visual information in neural populations

Our perception of the environment relies on the capacity of neural networks to adapt rapidly to changes in incoming stimuli. It is increasingly being realized that the neural code is adaptive, that is, sensory neurons change their responses and selectivity in a dynamic manner to match the changes in input stimuli. Understanding how rapid exposure, or adaptation, to a stimulus of fixed structure changes information processing by cortical networks is essential for understanding the relationship between sensory coding and behaviour. Physiological investigations of adaptation have contributed greatly to our understanding of how individual sensory neurons change their responses to influence stimulus coding, yet whether and how adaptation affects information coding in neural populations is unknown. Here we examine how brief adaptation (on the timescale of visual fixation) influences the structure of interneuronal correlations and the accuracy of population coding in the macaque (Macaca mulatta) primary visual cortex (V1). We find that brief adaptation to a stimulus of fixed structure reorganizes the distribution of correlations across the entire network by selectively reducing their mean and variability. The post-adaptation changes in neuronal correlations are associated with specific, stimulus-dependent changes in the efficiency of the population code, and are consistent with changes in perceptual performance after adaptation. Our results have implications beyond the predictions of current theories of sensory coding, suggesting that brief adaptation improves the accuracy of population coding to optimize neuronal performance during natural viewing.     

Attentional modulation in visual cortex depends on task timing

Paying attention to a stimulus selectively increases the ability to process it. For example, when subjects attend to a specific region of a visual scene, their sensitivity to changes at that location increases. A large number of studies describe the behavioural consequences and neurophysiological correlates of attending to spatial locations. There has, in contrast, been little study of the allocation of attention over time. Because subjects can anticipate predictable events with great temporal precision, it seems probable that they might dynamically shift their attention when performing a familiar perceptual task whose constraints changed over time. We trained monkeys to respond to a stimulus change where the probability of occurrence changed over time. Recording from area V4 of the visual cortex in these animals, we found that the modulation of neuronal responses changed according to the probability of the change occurring at that instant. Thus, we show that the attentional modulation of sensory neurons reflects a subject's anticipation of the timing of behaviourally relevant events.     

A new perceptual illusion reveals mechanisms of sensory decoding

Perceptual illusions are usually thought to arise from the way sensory signals are encoded by the brain, and indeed are often used to infer the mechanisms of sensory encoding. But perceptual illusions might also result from the way the brain decodes sensory information, reflecting the strategies that optimize performance in particular tasks. In a fine discrimination task, the most accurate information comes from neurons tuned away from the discrimination boundary, and observers seem to use signals from these 'displaced' neurons to optimize their performance. We wondered whether using signals from these neurons might also bias perception. In a fine direction discrimination task using moving random-dot stimuli, we found that observers' perception of the direction of motion is indeed biased away from the boundary. This misperception can be accurately described by a decoding model that preferentially weights signals from neurons whose responses best discriminate those directions. In a coarse discrimination task, to which a different decoding rule applies, the same stimulus is not misperceived, suggesting that the illusion is a direct consequence of the decoding strategy that observers use to make fine perceptual judgments. The subjective experience of motion is therefore not mediated directly by the responses of sensory neurons, but is only developed after the responses of these neurons are decoded.     

Cortical remodelling induced by activity of ventral tegmental dopamine neurons.

Representations of sensory stimuli in the cerebral cortex can undergo progressive remodelling according to the behavioural importance of the stimuli. The cortex receives widespread projections from dopamine neurons in the ventral tegmental area (VTA), which are activated by new stimuli or unpredicted rewards, and are believed to provide a reinforcement signal for such learning-related cortical reorganization. In the primary auditory cortex (AI) dopamine release has been observed during auditory learning that remodels the sound-frequency representations. Furthermore, dopamine modulates long-term potentiation, a putative cellular mechanism underlying plasticity. Here we show that stimulating the VTA together with an auditory stimulus of a particular tone increases the cortical area and selectivity of the neural responses to that sound stimulus in AI. Conversely, the AI representations of nearby sound frequencies are selectively decreased. Strong, sharply tuned responses to the paired tones also emerge in a second cortical area, whereas the same stimuli evoke only poor or non-selective responses in this second cortical field in naive animals. In addition, we found that strong long-range coherence of neuronal discharge emerges between AI and this secondary auditory cortical area.     

Object-based attention determines dominance in binocular rivalry

A question of long-standing interest to philosophers, psychologists and neuroscientists is how the brain selects which signals enter consciousness. Binocular rivalry and attention both involve selection of visual stimuli, but affect perception quite differently. During binocular rivalry, awareness alternates between two different stimuli presented to the two eyes. In contrast, attending to one of two different stimuli impairs discrimination of the ignored stimulus, but without causing it to disappear from consciousness. Here we show that despite this difference, attention and rivalry rely on shared object-based selection mechanisms. We cued attention to one of two superimposed transparent surfaces and then deleted the image of one surface from each eye, resulting in rivalry. Observers usually reported seeing only the cued surface. They were also less accurate in judging unpredictable changes in the features of the uncued surface. Our design ensured that selection of the cued surface could not have resulted from spatial, ocular or feature-based mechanisms. Rather, attention was drawn to one surface, and this caused the other surface to be perceptually suppressed during rivalry. These results raise the question of how object representations compete during these two forms of perceptual selection, even as the features of those objects change unpredictably over time.     

Selective gating of visual signals by microstimulation of frontal cortex

Several decades of psychophysical and neurophysiological studies have established that visual signals are enhanced at the locus of attention. What remains a mystery is the mechanism that initiates biases in the strength of visual representations. Recent evidence argues that, during spatial attention, these biases reflect nascent saccadic eye movement commands. We examined the functional interaction of saccade preparation and visual coding by electrically stimulating sites within the frontal eye fields (FEF) and measuring its effect on the activity of neurons in extrastriate visual cortex. Here we show that visual responses in area V4 could be enhanced after brief stimulation of retinotopically corresponding sites within the FEF using currents below that needed to evoke saccades. The magnitude of the enhancement depended on the effectiveness of receptive field stimuli as well as on the presence of competing stimuli outside the receptive field. Stimulation of non-corresponding FEF representations could suppress V4 responses. The results suggest that the gain of visual signals is modified according to the strength of spatially corresponding eye movement commands.     

Tracking an object through feature space

Visual attention allows an observer to select certain visual information for specialized processing. Selection is readily apparent in 'tracking' tasks where even with the eyes fixed, observers can track a target as it moves among identical distractor items. In such a case, a target is distinguished by its spatial trajectory. Here we show that one can keep track of a stationary item solely on the basis of its changing appearance--specified by its trajectory along colour, orientation, and spatial frequency dimensions--even when a distractor shares the same spatial location. This ability to track through feature space bears directly on competing theories of attention, that is, on whether attention can select locations in space, features such as colour or shape, or particular visual objects composed of constellations of visual features. Our results affirm, consistent with a growing body of psychophysical and neurophysiological evidence, that attention can indeed select specific visual objects. Furthermore, feature-space tracking extends the definition of visual object to include not only items with well defined spatio-temporal trajectories, but also those with well defined featuro-temporal trajectories.     

基于工作记忆内容的注意导向的影响因素

工作记忆内容对视觉搜索中注意选择的影响到底如何,与工作记忆内容匹配的项目是否总是会自动捕获注意,至今仍存在争议。本研究针对前人研究中存在的差异和不足,统一采用"记忆-搜索"双任务范式来探讨搜索任务难度、搜索项目刺激强度以及记忆任务呈现时间对基于工作记忆内容的注意导向的影响。结果发现:当采用困难搜索任务时,干扰条件下被试反应时与中性条件下反应时无显著差异,说明难度会影响工作记忆内容对注意选择的自动导向效应,但这种影响只有在搜索任务难度足够大的情况下才能体现出来。而在本研究中并未发现刺激强度和记忆任务呈现时间这两个因素对基于工作记忆内容的注意导向的影响,即无论刺激强度高低,或记忆任务呈现时间长或短,与工作记忆内容匹配的搜索项目还是会"自动捕获注意",导致干扰条件下被试反应时显著慢于中性条件。     

Experience-dependent representation of visual categories in parietal cortex

Categorization is a process by which the brain assigns meaning to sensory stimuli. Through experience, we learn to group stimuli into categories, such as 'chair', 'table' and 'vehicle', which are critical for rapidly and appropriately selecting behavioural responses. Although much is known about the neural representation of simple visual stimulus features (for example, orientation, direction and colour), relatively little is known about how the brain learns and encodes the meaning of stimuli. We trained monkeys to classify 360 degrees of visual motion directions into two discrete categories, and compared neuronal activity in the lateral intraparietal (LIP) and middle temporal (MT) areas, two interconnected brain regions known to be involved in visual motion processing. Here we show that neurons in LIP--an area known to be centrally involved in visuo-spatial attention, motor planning and decision-making-robustly reflect the category of motion direction as a result of learning. The activity of LIP neurons encoded directions of motion according to their category membership, and that encoding shifted after the monkeys were retrained to group the same stimuli into two new categories. In contrast, neurons in area MT were strongly direction selective but carried little, if any, explicit category information. This indicates that LIP might be an important nexus for the transformation of visual direction selectivity to more abstract representations that encode the behavioural relevance, or meaning, of stimuli.     

Multimodal Brain-Computer Interfaces

A critical parameter of brain-computer interfaces(BCIs) is the number of dimensions a user can control independently.One way to increment this number without increasing the mental effort required to operate the system is to stimulate several sensory modalities simultaneously,and to distinguish brain activity patterns when the user focuses attention to different elements of this multisensory input.In this article we show how shifting attention between simultaneously presented tactile and visual stimuli affects the electrical brain activity of human subjects,and that this signal can be used to augment the control information from the two uni-modal BCI subsystems.     

Cortical microstimulation influences perceptual judgements of motion direction

Neurons in the visual cortex respond selectively to perceptually salient features of the visual scene, such as the direction and speed of moving objects, the orientation of local contours, or the colour or relative depth of a visual pattern. It is commonly assumed that the brain constructs its percept of the visual scene from information encoded in the selective responses of such neurons. We have now tested this hypothesis directly by measuring the effect on psychophysical performance of modifying the firing rates of physiologically characterized neurons. We required rhesus monkeys to report the direction of motion in a visual display while we electrically stimulated clusters of directionally selective neurons in the middle temporal visual area (MT, or V5), an extrastriate area that plays a prominent role in the analysis of visual motion information. Microstimulation biased the animals' judgements towards the direction of motion encoded by the stimulated neurons. This result indicates that physiological properties measured at the neuronal level can be causally related to a specific aspect of perceptual performance.     

Motion-induced blindness in normal observers.

Cases in which salient visual stimuli do not register consciously are known to occur in special conditions, such as the presentation of dissimilar stimuli to the two eyes or when images are stabilized on the retina. Here, we report a striking phenomenon of 'visual disappearance' observed with normal-sighted observers under natural conditions. When a global moving pattern is superimposed on high-contrast stationary or slowly moving stimuli, the latter disappear and reappear alternately for periods of several seconds. We show that this motion-induced blindness (MIB) phenomenon is unlikely to reflect retinal suppression, sensory masking or adaptation. The phenomenology observed includes perceptual grouping effects, object rivalry and visual field anisotropy. This is very similar to that found in other types of visual disappearance, as well as in clinical cases of attention deficits, in which partial invisibility might occur despite the primary visual areas being intact. Disappearance might reflect a disruption of attentional processing, which shifts the system into a winner-takes-all mode, uncovering the dynamics of competition between object representations within the human visual system.     

Bottlenose dolphins perceive object features through echolocation

How organisms (including people) recognize distant objects is a fundamental question. The correspondence between object characteristics (distal stimuli), like visual shape, and sensory characteristics (proximal stimuli), like retinal projection, is ambiguous. The view that sensory systems are 'designed' to 'pick up' ecologically useful information is vague about how such mechanisms might work. In echolocating dolphins, which are studied as models for object recognition sonar systems, the correspondence between echo characteristics and object characteristics is less clear. Many cognitive scientists assume that object characteristics are extracted from proximal stimuli, but evidence for this remains ambiguous. For example, a dolphin may store 'sound templates' in its brain and identify whole objects by listening for a particular sound. Alternatively, a dolphin's brain may contain algorithms, derived through natural endowments or experience or both, which allow it to identify object characteristics based on sounds. The standard method used to address this question in many species is indirect and has led to equivocal results with dolphins. Here we outline an appropriate method and test it to show that dolphins extract object characteristics directly from echoes.     

Neural mechanisms of perceptual grouping in human visual cortex

The current work examined neural substrates of perceptual grouping in human visual cortex using event-related potential (ERP) recording. Stimulus arrays consisted of local elements that were either evenly spaced (uniform stimuli) or grouped into columns or rows by proximity or color similarity (grouping stimuli). High-density ERPs were recorded while subjects identified orientations of perceptual groups in stimulus arrays that were presented randomly in one of the four quadrants of the visual field.Both uniform and grouping stimulus arrays elicited an early ERP component (C1), which peaked at about 70ms after stimulus onset and changed its polarity as a function of stimulated elevations. Dipole modeling based on realistichead boundary-element models revealed generators of the C1 component in the calcarine cortex. The C1 was modulated by perceptual grouping of local elements based on proximity, and this grouping effect was stronger in the upper than in the lower visual field. The findings provide ERP evidence for the engagement of human primary visual cortex in the early stage of perceptual grouping.     

Sustained division of the attentional spotlight

By voluntarily directing attention to a specific region of a visual scene, we can improve our perception of stimuli at that location. This ability to focus attention upon specific zones of the visual field has been described metaphorically as a moveable spotlight or zoom lens that facilitates the processing of stimuli within its 'beam'. A long-standing controversy has centred on the question of whether the spotlight of spatial attention has a unitary beam or whether it can be divided flexibly to disparate locations. Evidence supporting the unitary spotlight view has come from numerous behavioural and electrophysiological studies. Recent experiments, however, indicate that the spotlight of spatial attention may be divided between non-contiguous zones of the visual field for very brief stimulus exposures (&<100 ms). Here we use an electrophysiological measure of attentional allocation (the steady-state visual evoked potential) to show that the spotlight may be divided between spatially separated locations (excluding interposed locations) over more extended time periods. This spotlight division appears to be accomplished at an early stage of visual-cortical processing.     

Neuronal correlates of a perceptual decision

The relationship between neuronal activity and psychophysical judgement has long been of interest to students of sensory processing. Previous analyses of this problem have compared the performance of human or animal observers in detection or discrimination tasks with the signals carried by individual neurons, but have been hampered because neuronal and perceptual data were not obtained at the same time and under the same conditions. We have now measured the performance of monkeys and of visual cortical neurons while the animals performed a psychophysical task well matched to the properties of the neurons under study. Here we report that the reliability and sensitivity of most neurons on this task equalled or exceeded that of the monkeys. We therefore suggest that under our conditions, psychophysical judgements could be based on the activity of a relatively small number of neurons.     

Context-enabled learning in the human visual system

Training was found to improve the performance of humans on a variety of visual perceptual tasks. However, the ability to detect small changes in the contrast of simple visual stimuli could not be improved by repetition. Here we show that the performance of this basic task could be modified after the discrimination of the stimulus contrast was practised in the presence of similar laterally placed stimuli, suggesting a change in the local neuronal circuit involved in the task. On the basis of a combination of hebbian and anti-hebbian synaptic learning rules compatible with our results, we propose a mechanism of plasticity in the visual cortex that is enabled by a change in the context.     

A neuronal mechanism for sensory gating during locomotion in a vertebrate

The response of the foot to touch during walking depends on whether it is in the air or on the ground. In most animals, reflex responses to external stimuli are similarly adapted to their timing in the locomotor cycle, but there is only fragmentary information about the neural mechanisms involved. In arthropods, reflex modulation can occur in the sensory receptors themselves and in neurons that discharge during locomotion. By recording with dye-filled microelectrodes from neurons in the spinal cord of frog embryos, we describe reflex modulation at the level of sensory interneurons. Sensory inputs from skin receptors excite a specific class of spinal sensory interneuron whose activity leads to reflex bending of the body away from the stimulus. During swimming, these inputs are gated by rhythmic postsynaptic inhibition, so that sensory drive reaches motor neurons only at phases in the locomotor cycle when the resulting contraction would likewise turn the embryo away from the stimulated side. Such gating of sensory pathways could be a general feature of all locomotor systems where responses to sensory stimuli need to be adapted to the phase of locomotion.