Brain mechanisms associated with top-down processes in perception.

Perception arises through an interaction between sensory input and prior knowledge. We propose that at least two brain areas are required for such an interaction: the ''site'' where analysis of afferent signals occurs and the ''source'' which applies the relevant prior knowledge. In the human brain, functional imaging studies have demonstrated that selective attention modifies activity in early visual processing areas specific to the attended feature. Early processing areas are also modified when prior knowledge permits a percept to emerge from an otherwise meaningless stimulus. Sources of this modification have been identified in parietal cortex and in prefrontal cortex. Modification of early processing areas also occurs on the basis of prior knowledge about the predicted sensory effects of the subject''s own actions. Activity associated with mental imagery resembles that associated with response preparation (for motor imagery) and selective attention (for sensory imagery) suggesting that mental imagery reflects the effects of prior knowledge on sensory processing areas in the absence of sensory input. Damage to sensory processing areas can lead to a form of sensory hallucination which seems to arise from the interaction of prior knowledge with random sensory activity. In contrast, hallucinations associated with schizophrenia may arise from a failure of prior knowledge about motor intentions to modify activity in relevant sensory areas. When functioning normally, this mechanism permits us to distinguish our own actions from those of independent agents in the outside world. Failure to make this distinction correctly may account for the strong association between hallucinations and paranoid delusions in schizophrenia; the patient not only hears voices, but attributes (usually hostile) intentions to these voices.     

On the perception of probable things: neural substrates of associative memory, imagery, and perception

Perception is influenced both by the immediate pattern of sensory inputs and by memories acquired through prior experiences with the world. Throughout much of its illustrious history, however, study of the cellular basis of perception has focused on neuronal structures and events that underlie the detection and discrimination of sensory stimuli. Relatively little attention has been paid to the means by which memories interact with incoming sensory signals. Building upon recent neurophysiological/behavioral studies of the cortical substrates of visual associative memory, I propose a specific functional process by which stored information about the world supplements sensory inputs to yield neuronal signals that can account for visual perceptual experience. This perspective represents a significant shift in the way we think about the cellular bases of perception.     

Visual homing using an associative memory

Homing is the process by which an autonomous system guides itself to a particular location on the basis of sensory input. In this paper, a method of visual homing using an associative memory based on a simple pattern classifier is described. Homing is accomplished without the use of an explicit world model by utilizing direct associations between learned visual patterns and system motor commands. The method is analyzed in terms of a pattern space and conditions obtained that allow the system performance to be predicted on the basis of statistical measurements on the environment. Results of experiments utilizing the method to guide a robot-mounted camera in a three-dimensional environment are presented.     

Gain modulation by nicotine in macaque v1

Acetylcholine is a ubiquitous cortical neuromodulator implicated in cognition. In order to understand the potential for acetylcholine to play a role in visual attention, we studied nicotinic acetylcholine receptor (nAChR) localization and function in area V1 of the macaque. We found nAChRs presynaptically at thalamic synapses onto excitatory, but not inhibitory, neurons in the primary thalamorecipient layer 4c. Furthermore, consistent with the release enhancement suggested by this localization, we discovered that nicotine increases responsiveness and lowers contrast threshold in layer 4c neurons. We also found that nAChRs are expressed by GABAergic interneurons in V1 but rarely by pyramidal neurons, and that nicotine suppresses visual responses outside layer 4c. All sensory systems incorporate gain control mechanisms, or processes which dynamically alter input/output relationships. We demonstrate that at the site of thalamic input to visual cortex, the effect of this nAChR-mediated gain is an enhancement of the detection of visual stimuli.     

Knowledge in perception and illusion.

Following Hermann von Helmholtz, who described visual perceptions as unconscious inferences from sensory data and knowledge derived from the past, perceptions are regarded as similar to predictive hypotheses of science, but are psychologically projected into external space and accepted as our most immediate reality. There are increasing discrepancies between perceptions and conceptions with science''s advances, which makes it hard to define ''illusion''. Visual illusions can provide evidence of object knowledge and working rules for vision, but only when the phenomena are explained and classified. A tentative classification is presented, in terms of appearances and kinds of causes. The large contribution of knowledge from the past for vision raises the issue: how do we recognize the present, without confusion from the past. This danger is generally avoided as the present is signalled by real-time sensory inputs-perhaps flagged by qualia of consciousness.     

Am I seeing my hand? Visual appearance and knowledge of controllability both contribute to the visual capture of a person's own body

When confronted with complex visual scenes in daily life, how do we know which visual information represents our own hand? We investigated the cues used to assign visual information to one''s own hand. Wrist tendon vibration elicits an illusory sensation of wrist movement. The intensity of this illusion attenuates when the actual motionless hand is visually presented. Testing what kind of visual stimuli attenuate this illusion will elucidate factors contributing to visual detection of one''s own hand. The illusion was reduced when a stationary object was shown, but only when participants knew it was controllable with their hands. In contrast, the visual image of their own hand attenuated the illusion even when participants knew that it was not controllable. We suggest that long-term knowledge about the appearance of the body and short-term knowledge about controllability of a visual object are combined to robustly extract our own body from a visual scene.     

Mirror agnosia.

Normal people rarely confuse the mirror image of an object with a real object so long as they realize they are looking into a mirror. We report a new neurological sign, ''mirror agnosia'', following right parietal lesions in which this ability is severely compromised. We studied four right hemisphere stroke patients who had left visual field ''neglect''. i.e. they were indifferent to objects in their left visual field even though they were not blind. We then placed a vertical parasagittal mirror on each patients'' right so that they could clearly see the reflection of objects placed in the (neglected) visual field. When shown a candy or pen on their left, the patients kept banging their hand into the mirror or groped behind it attempting to grab the reflection; they did not reach for the real object on the left, even though they were mentally quite lucid and knew they were looking into a mirror. Remarkably, all four patients kept complaining that the object was ''in the mirror'', ''outside my reach'' or ''behind the mirror''. Thus, even the patients'' ability to make simple logical inferences about mirrors has been selectively warped to accommodate the strange new sensory world that they now inhabit. The finding may have implications for understanding how the brain creates representations of mirror reflections.     

The world from a cat’s perspective – statistics of natural videos

The mammalian visual system is one of the most intensively investigated sensory systems. However, our knowledge of the typical input it is operating on is surprisingly limited. To address this issue, we seek to learn about the natural visual environment and the world as seen by a cat. With a CCD camera attached to their head, cats explore several outdoor environments and videos of natural stimuli are recorded from the animals perspective. The statistical analysis of these videos reveals several remarkable properties. First, we find an anisotropy of oriented contours with an enhanced occurrence of horizontal orientations, earlier described in the oblique effect as a predominance of the two cardinal orientations. Second, contrast is not elevated in the center of the images, suggesting different mechanisms of fixation point selection as compared to humans. Third, analyzing a sequence of images we find that the precise position of contours varies faster than their orientation. Finally, collinear contours prevail over parallel shifted contours, matching recent physiological and anatomical results. These findings demonstrate the rich structure of natural visual stimuli and its direct relation to extensively studied anatomical and physiological issues.     

Adaptation in the corticothalamic loop: computational prospects of tuning the senses

The present article discusses computational hypotheses on corticothalamic feedback and modulation of cortical response properties. We have recently proposed that the two phenomena are related, hypothesizing that neuronal velocity preference in the visual cortex is altered by feedback to the lateral geniculate nucleus. We now contrast the common view that response adaptation to stimuli subserves a function of redundancy reduction with the idea that it may enhance cortical representation of objects. Our arguments lead to the concept that the corticothalamic loop is involved in reducing sensory input to behaviourally relevant aspects, a pre-attentive gating.     

Nonlinear visuoauditory integration in the mouse superior colliculus

Sensory information from different modalities is processed in parallel, and then integrated in associative brain areas to improve object identification and the interpretation of sensory experiences. The Superior Colliculus (SC) is a midbrain structure that plays a critical role in integrating visual, auditory, and somatosensory input to assess saliency and promote action. Although the response properties of the individual SC neurons to visuoauditory stimuli have been characterized, little is known about the spatial and temporal dynamics of the integration at the population level. Here we recorded the response properties of SC neurons to spatially restricted visual and auditory stimuli using large-scale electrophysiology. We then created a general, population-level model that explains the spatial, temporal, and intensity requirements of stimuli needed for sensory integration. We found that the mouse SC contains topographically organized visual and auditory neurons that exhibit nonlinear multisensory integration. We show that nonlinear integration depends on properties of auditory but not visual stimuli. We also find that a heuristically derived nonlinear modulation function reveals conditions required for sensory integration that are consistent with previously proposed models of sensory integration such as spatial matching and the principle of inverse effectiveness.     

Music alters visual perception

Background

Visual perception is not a passive process: in order to efficiently process visual input, the brain actively uses previous knowledge (e.g., memory) and expectations about what the world should look like. However, perception is not only influenced by previous knowledge. Especially the perception of emotional stimuli is influenced by the emotional state of the observer. In other words, how we perceive the world does not only depend on what we know of the world, but also by how we feel. In this study, we further investigated the relation between mood and perception.

Methods and Findings

We let observers do a difficult stimulus detection task, in which they had to detect schematic happy and sad faces embedded in noise. Mood was manipulated by means of music. We found that observers were more accurate in detecting faces congruent with their mood, corroborating earlier research. However, in trials in which no actual face was presented, observers made a significant number of false alarms. The content of these false alarms, or illusory percepts, was strongly influenced by the observers'' mood.

Conclusions

As illusory percepts are believed to reflect the content of internal representations that are employed by the brain during top-down processing of visual input, we conclude that top-down modulation of visual processing is not purely predictive in nature: mood, in this case manipulated by music, may also directly alter the way we perceive the world.     

Neural coding of natural stimuli: information at sub-millisecond resolution

Sensory information about the outside world is encoded by neurons in sequences of discrete, identical pulses termed action potentials or spikes. There is persistent controversy about the extent to which the precise timing of these spikes is relevant to the function of the brain. We revisit this issue, using the motion-sensitive neurons of the fly visual system as a test case. Our experimental methods allow us to deliver more nearly natural visual stimuli, comparable to those which flies encounter in free, acrobatic flight. New mathematical methods allow us to draw more reliable conclusions about the information content of neural responses even when the set of possible responses is very large. We find that significant amounts of visual information are represented by details of the spike train at millisecond and sub-millisecond precision, even though the sensory input has a correlation time of ~55 ms; different patterns of spike timing represent distinct motion trajectories, and the absolute timing of spikes points to particular features of these trajectories with high precision. Finally, the efficiency of our entropy estimator makes it possible to uncover features of neural coding relevant for natural visual stimuli: first, the system's information transmission rate varies with natural fluctuations in light intensity, resulting from varying cloud cover, such that marginal increases in information rate thus occur even when the individual photoreceptors are counting on the order of one million photons per second. Secondly, we see that the system exploits the relatively slow dynamics of the stimulus to remove coding redundancy and so generate a more efficient neural code.     

The absolute efficiency of perceptual decisions

Our perceptions of the world around us are stable and reliable. Is this because the mechanisms that yield them are crude and insensitive and thus immune to false responses? Or is it because a statistical censor that blocks unreliable messages intervenes between the signals from our sense organs and our knowledge of them? This question can be answered by measuring the efficiency with which statistical information is utilized in perception. It is shown that mirror symmetry can be detected in displays of otherwise random dots with an efficiency of up to 50%; thus the statistical mechanisms are not crude and insensitive, and this aspect of sensory physiology and psychology may deserve more attention.     

The Importance of Lateral Connections in the Parietal Cortex for Generating Motor Plans

Substantial evidence has highlighted the significant role of associative brain areas, such as the posterior parietal cortex (PPC) in transforming multimodal sensory information into motor plans. However, little is known about how different sensory information, which can have different delays or be absent, combines to produce a motor plan, such as executing a reaching movement. To address these issues, we constructed four biologically plausible network architectures to simulate PPC: 1) feedforward from sensory input to the PPC to a motor output area, 2) feedforward with the addition of an efference copy from the motor area, 3) feedforward with the addition of lateral or recurrent connectivity across PPC neurons, and 4) feedforward plus efference copy, and lateral connections. Using an evolutionary strategy, the connectivity of these network architectures was evolved to execute visually guided movements, where the target stimulus provided visual input for the entirety of each trial. The models were then tested on a memory guided motor task, where the visual target disappeared after a short duration. Sensory input to the neural networks had sensory delays consistent with results from monkey studies. We found that lateral connections within the PPC resulted in smoother movements and were necessary for accurate movements in the absence of visual input. The addition of lateral connections resulted in velocity profiles consistent with those observed in human and non-human primate visually guided studies of reaching, and allowed for smooth, rapid, and accurate movements under all conditions. In contrast, Feedforward or Feedback architectures were insufficient to overcome these challenges. Our results suggest that intrinsic lateral connections are critical for executing accurate, smooth motor plans.     

Circuit Motifs for Contrast-Adaptive Differentiation in Early Sensory Systems: The Role of Presynaptic Inhibition and Short-Term Plasticity

In natural signals, such as the luminance value across of a visual scene, abrupt changes in intensity value are often more relevant to an organism than intensity values at other positions and times. Thus to reduce redundancy, sensory systems are specialized to detect the times and amplitudes of informative abrupt changes in the input stream rather than coding the intensity values at all times. In theory, a system that responds transiently to fast changes is called a differentiator. In principle, several different neural circuit mechanisms exist that are capable of responding transiently to abrupt input changes. However, it is unclear which circuit would be best suited for early sensory systems, where the dynamic range of the natural input signals can be very wide. We here compare the properties of different simple neural circuit motifs for implementing signal differentiation. We found that a circuit motif based on presynaptic inhibition (PI) is unique in a sense that the vesicle resources in the presynaptic site can be stably maintained over a wide range of stimulus intensities, making PI a biophysically plausible mechanism to implement a differentiator with a very wide dynamical range. Moreover, by additionally considering short-term plasticity (STP), differentiation becomes contrast adaptive in the PI-circuit but not in other potential neural circuit motifs. Numerical simulations show that the behavior of the adaptive PI-circuit is consistent with experimental observations suggesting that adaptive presynaptic inhibition might be a good candidate neural mechanism to achieve differentiation in early sensory systems.     

The Effect of Self-Efficacy on Visual Discrimination Sensitivity

Can subjective belief about one''s own perceptual competence change one''s perception? To address this question, we investigated the influence of self-efficacy on sensory discrimination in two low-level visual tasks: contrast and orientation discrimination. We utilised a pre-post manipulation approach whereby two experimental groups (high and low self-efficacy) and a control group made objective perceptual judgments on the contrast or the orientation of the visual stimuli. High and low self-efficacy were induced by the provision of fake social-comparative performance feedback and fictional research findings. Subsequently, the post-manipulation phase was performed to assess changes in visual discrimination thresholds as a function of the self-efficacy manipulations. The results showed that the high self-efficacy group demonstrated greater improvement in visual discrimination sensitivity compared to both the low self-efficacy and control groups. These findings suggest that subjective beliefs about one''s own perceptual competence can affect low-level visual processing.     

The human brain from above: an increase in complexity from environmental stimuli to abstractions

Contrary to common belief, the brain appears to increase the complexity from the perceived object to the idea of it. Topological models predict indeed that: (a) increases in anatomical/functional dimensions and symmetries occur in the transition from the environment to the higher activities of the brain, and (b) informational entropy in the primary sensory areas is lower than in the higher associative ones. To demonstrate this novel hypothesis, we introduce a straightforward approach to measuring island information levels in fMRI neuroimages, via Rényi entropy derived from tessellated fMRI images. This approach facilitates objective detection of entropy and corresponding information levels in zones of fMRI images generally not taken into account. We found that the Rényi entropy is higher in associative cortices than in the visual primary ones. This suggests that the brain lies in dimensions higher than the environment and that it does not concentrate, but rather dilutes messages coming from external inputs.     

A comparison of experience-dependent plasticity in the visual and somatosensory systems

In the visual and somatosensory systems, maturation of neuronal circuits continues for days to weeks after sensory stimulation occurs. Deprivation of sensory input at various stages of development can induce physiological, and often structural, changes that modify the circuitry of these sensory systems. Recent studies also reveal a surprising degree of plasticity in the mature visual and somatosensory pathways. Here, we compare and contrast the effects of sensory experience on the connectivity and function of these pathways and discuss what is known to date concerning the structural, physiological, and molecular mechanisms underlying their plasticity.     

Within- and Cross-Modal Distance Information Disambiguate Visual Size-Change Perception

Perception is fundamentally underconstrained because different combinations of object properties can generate the same sensory information. To disambiguate sensory information into estimates of scene properties, our brains incorporate prior knowledge and additional “auxiliary” (i.e., not directly relevant to desired scene property) sensory information to constrain perceptual interpretations. For example, knowing the distance to an object helps in perceiving its size. The literature contains few demonstrations of the use of prior knowledge and auxiliary information in combined visual and haptic disambiguation and almost no examination of haptic disambiguation of vision beyond “bistable” stimuli. Previous studies have reported humans integrate multiple unambiguous sensations to perceive single, continuous object properties, like size or position. Here we test whether humans use visual and haptic information, individually and jointly, to disambiguate size from distance. We presented participants with a ball moving in depth with a changing diameter. Because no unambiguous distance information is available under monocular viewing, participants rely on prior assumptions about the ball''s distance to disambiguate their -size percept. Presenting auxiliary binocular and/or haptic distance information augments participants'' prior distance assumptions and improves their size judgment accuracy—though binocular cues were trusted more than haptic. Our results suggest both visual and haptic distance information disambiguate size perception, and we interpret these results in the context of probabilistic perceptual reasoning.