Stimulus dependency of object-evoked responses in human visual cortex: an inverse problem for category specificity

Many studies have linked the processing of different object categories to specific event-related potentials (ERPs) such as the face-specific N170. Despite reports showing that object-related ERPs are influenced by visual stimulus features, there is consensus that these components primarily reflect categorical aspects of the stimuli. Here, we re-investigated this idea by systematically measuring the effects of visual feature manipulations on ERP responses elicited by both structure-from-motion (SFM)-defined and luminance-defined object stimuli. SFM objects elicited a novel component at 200-250 ms (N250) over parietal and posterior temporal sites. We found, however, that the N250 amplitude was unaffected by restructuring SFM stimuli into meaningless objects based on identical visual cues. This suggests that this N250 peak was not uniquely linked to categorical aspects of the objects, but is strongly determined by visual stimulus features. We provide strong support for this hypothesis by parametrically manipulating the depth range of both SFM- and luminance-defined object stimuli and showing that the N250 evoked by SFM stimuli as well as the well-known N170 to static faces were sensitive to this manipulation. Importantly, this effect could not be attributed to compromised object categorization in low depth stimuli, confirming a strong impact of visual stimulus features on object-related ERP signals. As ERP components linked with visual categorical object perception are likely determined by multiple stimulus features, this creates an interesting inverse problem when deriving specific perceptual processes from variations in ERP components.     

Recognition of fragmented images and mechanisms of memory

Analysis of the topography and parameters of event-related potentials (ERPs) recorded during the presentation of incomplete images with different fragmentation aided in study of the role of different cortical zones and the order of their involvement in the recognition process. The role of the frontal cortical areas at different stages of perception of fragmented images was established. The differences in the ERPs induced by recognized and unrecognized stimuli in the frontal and frontal-temporal derivations in the interval 30–83 ms were associated with the appearance of early positivity in response to recognized images and development of early negativity in response to unrecognized stimuli. The N300 component associated with recognition was stronger in these cortical zones during identification of images. A late positive complex appeared in the frontal areas earlier than in other areas. Involvement of the caudal visual areas in the recognition process was reflected by enhancement of the components P100, P250, and N400. Our results suggest that the frontal areas play the main role in the recognition of fragmented images because they are the structures that organize extraction of traces from long-term modality-specific memory using a system of afferent and efferent links and determine the strategy of information analysis necessary for the solution of a given task.     

Do Simultaneously Viewed Objects Influence Scene Recognition Individually or as Groups? Two Perceptual Studies

The ability to quickly categorize visual scenes is critical to daily life, allowing us to identify our whereabouts and to navigate from one place to another. Rapid scene categorization relies heavily on the kinds of objects scenes contain; for instance, studies have shown that recognition is less accurate for scenes to which incongruent objects have been added, an effect usually interpreted as evidence of objects'' general capacity to activate semantic networks for scene categories they are statistically associated with. Essentially all real-world scenes contain multiple objects, however, and it is unclear whether scene recognition draws on the scene associations of individual objects or of object groups. To test the hypothesis that scene recognition is steered, at least in part, by associations between object groups and scene categories, we asked observers to categorize briefly-viewed scenes appearing with object pairs that were semantically consistent or inconsistent with the scenes. In line with previous results, scenes were less accurately recognized when viewed with inconsistent versus consistent pairs. To understand whether this reflected individual or group-level object associations, we compared the impact of pairs composed of mutually related versus unrelated objects; i.e., pairs, which, as groups, had clear associations to particular scene categories versus those that did not. Although related and unrelated object pairs equally reduced scene recognition accuracy, unrelated pairs were consistently less capable of drawing erroneous scene judgments towards scene categories associated with their individual objects. This suggests that scene judgments were influenced by the scene associations of object groups, beyond the influence of individual objects. More generally, the fact that unrelated objects were as capable of degrading categorization accuracy as related objects, while less capable of generating specific alternative judgments, indicates that the process by which objects interfere with scene recognition is separate from the one through which they inform it.     

Neuropsychological studies of object recognition

It is well established that disorders of visual perception are associated with lesions in the right hemisphere. Performances on tasks as disparate as the identification of objects from unusual views of objects drawn so as to overlap, of fragmented letters, of familiar faces, and of anomalous features in drawings, have been shown to be impaired in patients with focal right posterior lesions. A series of investigations are reviewed, directed towards analysing the basis of these deficits. Explanations in terms of primary visual impairment can be rejected, as can an account in terms of faulty figure-ground organization. It is argued that a wide variety of such perceptual deficits--all of which are concerned with meaningful visual stimuli--can be encompassed by the notion of faulty perceptual categorization at an early post-sensory stage of object recognition. Moreover, there is evidence suggesting that some of these various perceptual deficits can be mutually dissociated. The concept of perceptual categorization is discussed in the wider context of tentative model of object recognition.     

Visual apparent motion and some preferred paths in the rotation group SO(3)

The sequential presentation of two distinct stimulus objects to the visual system will, under certain conditions, induce an apparentmotion effect, called beta motion, in which the first object appears to smoothly transform into the second. This study is concerned with the kinds of paths selected by the visual system in effecting beta motion in which the metric structure of the object is preserved throughout. Two schemes are advanced according to which the visual system might operate. The first concentrates upon the manifold M in which the object appears to transform and the second upon the group G of transformations of M onto itself in which the particular transformation describing this motion lie. Under the identification of M with the 2-sphere S ², each scheme specifies the action-minimizing curves in the rotation group SO(3) for a particular “natural” Riemannian metric. An experiment is described in which a determination is made of the actual paths taken by an object under-going various rigid-motion beta motions. The results obtained indicate that the visual system behaves more in accordance with the second scheme than with the first. A generalization of this result is briefly discussed.     

Object discrimination by pigeons: effects of object color and shape

Can nonhuman animals attend to visual stimuli as whole, coherent objects? We investigated this question by adapting for use with pigeons a task in which human participants must report whether two visual attributes belong to the same object (one-object trial) or to different objects (two-object trial). We trained pigeons to discriminate a pair of differently colored shapes that had two targets either on a single object or on two different objects. Each target equally often appeared on the one-object and two-object stimuli; therefore, a specific target location could not serve as a discriminative cue. The pigeons learned to report whether the two target dots were located on a single object or on two different objects; follow-up tests demonstrated that this ability was not entirely based on memorization of the dot patterns and locations. Additional tests disclosed predominate stimulus control by the color, but not by the shape of the two objects. These findings suggest that human psychophysical methods are readily applicable to the study of object discrimination by nonhuman animals.     

Tracking moving identities: after attending the right location, the identity does not come for free

Although tracking identical moving objects has been studied since the 1980''s, only recently the study into tracking moving objects with distinct identities has started (referred to as Multiple Identity Tracking, MIT). So far, only behavioral studies into MIT have been undertaken. These studies have left a fundamental question regarding MIT unanswered, is MIT a one-stage or a two-stage process? According to the one-stage model, after a location has been attended, the identity is released without effort. However, according to the two-stage model, there are two effortful stages in MIT, attending to a location, and attending to the identity of the object at that location. In the current study we investigated this question by measuring brain activity in response to tracking familiar and unfamiliar targets. Familiarity is known to automate effortful processes, so if attention to identify the object is needed, this should become easier. However, if no such attention is needed, familiarity can only affect other processes (such as memory for the target set). Our results revealed that on unfamiliar trials neural activity was higher in both attentional networks, and visual identification networks. These results suggest that familiarity in MIT automates attentional identification processes, thus suggesting that attentional identification is needed in MIT. This then would imply that MIT is essentially a two-stage process, since after attending the location, the identity does not seem to come for free.     

What are birds looking at? Head movements and eye use in chickens

Using video recordings of hens, Gallus gallus domesticus, as they approached different kinds of objects, I examined how change in object distance is associated with a change from lateral to binocular viewing. The birds tended to view distant objects laterally while they preferentially viewed objects less than 20-30 cm away frontally; this was true whether they were looking at another bird or at an inanimate object. However, as well as switching between lateral and frontal viewing, the hens also swung their heads from side to side with movements so large that the same object appeared to be viewed with completely different parts of the retina, and even with different eyes, in rapid succession. When confronted with a novel object, the hens walked more slowly but continued to show large head movements. This suggests that, unlike mammals, which gaze fixedly at novel objects, hens investigate them by moving the head and looking at them with different, specialized, parts of their eyes. Many aspects of bird behaviour, such as search image formation, vigilance and visual discriminations, may be affected by the way they move the head and eyes. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.     

Overt visual attention as a causal factor of perceptual awareness

Our everyday conscious experience of the visual world is fundamentally shaped by the interaction of overt visual attention and object awareness. Although the principal impact of both components is undisputed, it is still unclear how they interact. Here we recorded eye-movements preceding and following conscious object recognition, collected during the free inspection of ambiguous and corresponding unambiguous stimuli. Using this paradigm, we demonstrate that fixations recorded prior to object awareness predict the later recognized object identity, and that subjects accumulate more evidence that is consistent with their later percept than for the alternative. The timing of reached awareness was verified by a reaction-time based correction method and also based on changes in pupil dilation. Control experiments, in which we manipulated the initial locus of visual attention, confirm a causal influence of overt attention on the subsequent result of object perception. The current study thus demonstrates that distinct patterns of overt attentional selection precede object awareness and thereby directly builds on recent electrophysiological findings suggesting two distinct neuronal mechanisms underlying the two phenomena. Our results emphasize the crucial importance of overt visual attention in the formation of our conscious experience of the visual world.     

Object recognition and generalisation during habituation in horses

The ability of horses to habituate to frightening stimuli greatly increases safety in the horse–human relationship. A recent experiment suggested, however, that habituation to frightening visual stimuli is relatively stimulus-specific in horses and that shape and colour are important factors for object generalisation (Christensen et al., 2008). In a series of experiments, we aimed to further explore the ability of horses (n = 30, 1 and 2-year-old mares) to recognise and generalise between objects during habituation. TEST horses (n = 15) were habituated to a complex object, composed of five simple objects of varying shape and colour, whereas CONTROL horses (n = 15) were habituated to the test arena, but not to the complex object. In the first experiment, we investigated whether TEST horses subsequently reacted less to i) simple objects that were previously part of the complex object (i.e. testing for object recognition) and ii) a novel object (new shape and colour, i.e. testing for object generalisation), compared to CONTROLS. In the second experiment we investigated whether TEST horses reacted to a change in object order and object location. Behavioural reactions to the object, latency to eat, total eating time and heart rate were recorded. Compared to CONTROLS, TEST horses reacted significantly less towards objects, which were previously part of the complex object (e.g. mean heart rate; P = 0.006), indicating object recognition. In contrast to our expectations, TEST horses also reacted significantly less towards the novel object (e.g. mean heart rate; P = 0.018), suggesting that they were capable of object generalisation. We also found that TEST horses showed an increase in exploratory behaviour when objects within the complex object changed order and location (both P < 0.001), whereas there was no increase in heart rate, indicating that the horses were not frightened by the changes. The results demonstrate that it is possible to increase object generalisation in horses by habituating them to a range of colours and shapes simultaneously. This knowledge greatly affects the way in which horses may be trained to react calmly towards frightening objects.     

Distinct mechanisms mediate visual detection and identification

A core organizing principle for studies of the brain is that distinct neural pathways mediate distinct behavioral tasks [1, 2]. When two related tasks are mediated by a common pathway, studies of one are likely to generalize to the other. Here, we test whether performance on two laboratory tasks that model object detection and identification are mediated by common mechanisms of visual adaptation. Although both tasks rely on the luminance pattern in images, their demands on visual processing are quite different. Object detection requires discriminating image luminance differences associated with the light reflected from adjacent objects. To encode these differences reliably, neurons adapt their limited dynamic range to prevailing viewing conditions [3-6]. Object identification, on the other hand, demands a fixed response to light reflected from an object independent of illumination [7]. We compared performance in discrimination and identification tasks for simulated surfaces. In striking contrast to studies with less structured contexts, we found clear evidence that distinct processes mediate judgments in the two tasks. These results challenge models that account for perceived lightness entirely through the action of image-encoding mechanisms.     

Event-related potentials associated with a shift in the strategy of visual perception during recognition of a hierarchical stimulus

Recording of event-related potentials (ERPs) was used to study the brain mechanisms of shifting the strategy of recognition of the global and local levels of a hierarchical image by adult subjects. A shift in the strategy of visual recognition results in substantial changes in ERP parameters in the caudal and frontocentral cortical areas. The activation effect of the switchover from one recognition strategy to another is associated with an increase in the amplitude of early ERP components (C1, P100, and N150) of the caudal cortical areas. Changes in the late ERP components associated with processing of significant information features during the shift in the recognition strategy are observed in the frontal areas within the interval 388–579 ms, with the amplitude of components N300 and N400 increasing.     

Neural Androgen Receptor Deletion Impairs the Temporal Processing of Objects and Hippocampal CA1-Dependent Mechanisms

We studied the role of testosterone, mediated by the androgen receptor (AR), in modulating temporal order memory for visual objects. For this purpose, we used male mice lacking AR specifically in the nervous system. Control and mutant males were gonadectomized at adulthood and supplemented with equivalent amounts of testosterone in order to normalize their hormonal levels. We found that neural AR deletion selectively impaired the processing of temporal information for visual objects, without affecting classical object recognition or anxiety-like behavior and circulating corticosterone levels, which remained similar to those in control males. Thus, mutant males were unable to discriminate between the most recently seen object and previously seen objects, whereas their control littermates showed more interest in exploring previously seen objects. Because the hippocampal CA1 area has been associated with temporal memory for visual objects, we investigated whether neural AR deletion altered the functionality of this region. Electrophysiological analysis showed that neural AR deletion affected basal glutamate synaptic transmission and decreased the magnitude of N-methyl-D-aspartate receptor (NMDAR) activation and high-frequency stimulation-induced long-term potentiation. The impairment of NMDAR function was not due to changes in protein levels of receptor. These results provide the first evidence for the modulation of temporal processing of information for visual objects by androgens, via AR activation, possibly through regulation of NMDAR signaling in the CA1 area in male mice.     

Context effects on the neural correlates of recognition memory: an electrophysiological study

Event-related potentials (ERPs) were recorded during a recognition memory test for previously studied visual objects. Some studied objects were paired with the same context (landscape scenes) as at study, some were superimposed on a different studied context, and some were paired with new contexts. Unstudied objects were paired with either a studied or a new context. Three ERP memory effects were observed: an early effect elicited by all stimuli containing at least one studied component; a second effect elicited only by stimuli in which both object and context had been studied; and a third effect elicited by stimuli containing a studied object. Thus, test stimuli engaged three distinct kinds of memory-related neural activity which differed in their specificity for task-relevant features.     

Size Constancy in Bat Biosonar? Perceptual Interaction of Object Aperture and Distance

Perception and encoding of object size is an important feature of sensory systems. In the visual system object size is encoded by the visual angle (visual aperture) on the retina, but the aperture depends on the distance of the object. As object distance is not unambiguously encoded in the visual system, higher computational mechanisms are needed. This phenomenon is termed “size constancy”. It is assumed to reflect an automatic re-scaling of visual aperture with perceived object distance. Recently, it was found that in echolocating bats, the ‘sonar aperture’, i.e., the range of angles from which sound is reflected from an object back to the bat, is unambiguously perceived and neurally encoded. Moreover, it is well known that object distance is accurately perceived and explicitly encoded in bat sonar. Here, we addressed size constancy in bat biosonar, recruiting virtual-object techniques. Bats of the species Phyllostomus discolor learned to discriminate two simple virtual objects that only differed in sonar aperture. Upon successful discrimination, test trials were randomly interspersed using virtual objects that differed in both aperture and distance. It was tested whether the bats spontaneously assigned absolute width information to these objects by combining distance and aperture. The results showed that while the isolated perceptual cues encoding object width, aperture, and distance were all perceptually well resolved by the bats, the animals did not assign absolute width information to the test objects. This lack of sonar size constancy may result from the bats relying on different modalities to extract size information at different distances. Alternatively, it is conceivable that familiarity with a behaviorally relevant, conspicuous object is required for sonar size constancy, as it has been argued for visual size constancy. Based on the current data, it appears that size constancy is not necessarily an essential feature of sonar perception in bats.     

Developing classification in action: I. Human infants

Human infants’ developing manipulatory transformations involved in classifying objects from ages 6 to 24 months were investigated. Infants’ manipulations develop from predominantly serial one-at-a-time acts with one object to predominantly parallel two-at-a-time acts with two objects. This shift is marked by increasingly overt transformational consequences for the objects manipulated. When infants construct parallel transformations they are initially different. With age they are increasingly identical or reciprocal. Also during this age period, as the number of objects manipulated at the same time increases, so does the frequency with which infants coordinate them. At the same time, the kind of objects infants manipulate simultaneously changes. Six-month-olds manipulate different objects when acting on more than one object at a time. By age 12 months, infants switch to manipulating identical objects at the same time, indicating that they are beginning to construct identity classes. Since this development occurs about a half year before human infants develop any substantial naming behavior, the origins of classification cannot depend on this linguistic development     

How Lateral Connections and Spiking Dynamics May Separate Multiple Objects Moving Together

Over successive stages, the ventral visual system of the primate brain develops neurons that respond selectively to particular objects or faces with translation, size and view invariance. The powerful neural representations found in Inferotemporal cortex form a remarkably rapid and robust basis for object recognition which belies the difficulties faced by the system when learning in natural visual environments. A central issue in understanding the process of biological object recognition is how these neurons learn to form separate representations of objects from complex visual scenes composed of multiple objects. We show how a one-layer competitive network comprised of ‘spiking’ neurons is able to learn separate transformation-invariant representations (exemplified by one-dimensional translations) of visual objects that are always seen together moving in lock-step, but separated in space. This is achieved by combining ‘Mexican hat’ functional lateral connectivity with cell firing-rate adaptation to temporally segment input representations of competing stimuli through anti-phase oscillations (perceptual cycles). These spiking dynamics are quickly and reliably generated, enabling selective modification of the feed-forward connections to neurons in the next layer through Spike-Time-Dependent Plasticity (STDP), resulting in separate translation-invariant representations of each stimulus. Variations in key properties of the model are investigated with respect to the network’s ability to develop appropriate input representations and subsequently output representations through STDP. Contrary to earlier rate-coded models of this learning process, this work shows how spiking neural networks may learn about more than one stimulus together without suffering from the ‘superposition catastrophe’. We take these results to suggest that spiking dynamics are key to understanding biological visual object recognition.     

Subcortical discrimination of unperceived objects during binocular rivalry

Rapid identification of behaviorally relevant objects is important for survival. In humans, the neural computations for visually discriminating complex objects involve inferior temporal cortex (IT). However, less detailed but faster form processing may also occur in a phylogenetically older subcortical visual system that terminates in the amygdala. We used binocular rivalry to present stimuli without conscious awareness, thereby eliminating the IT object representation and isolating subcortical visual input to the amygdala. Functional magnetic resonance imaging revealed significant brain activation in the left amygdala but not in object-selective IT in response to unperceived fearful faces compared to unperceived nonface objects. These findings indicate that, for certain behaviorally relevant stimuli, a high-level cortical representation in IT is not required for object discrimination in the amygdala.     

Neural representation of objects in space: a dual coding account.

I present evidence on the nature of object coding in the brain and discuss the implications of this coding for models of visual selective attention. Neuropsychological studies of task-based constraints on: (i) visual neglect; and (ii) reading and counting, reveal the existence of parallel forms of spatial representation for objects: within-object representations, where elements are coded as parts of objects, and between-object representations, where elements are coded as independent objects. Aside from these spatial codes for objects, however, the coding of visual space is limited. We are extremely poor at remembering small spatial displacements across eye movements, indicating (at best) impoverished coding of spatial position per se. Also, effects of element separation on spatial extinction can be eliminated by filling the space with an occluding object, indicating that spatial effects on visual selection are moderated by object coding. Overall, there are separate limits on visual processing reflecting: (i) the competition to code parts within objects; (ii) the small number of independent objects that can be coded in parallel; and (iii) task-based selection of whether within- or between-object codes determine behaviour. Between-object coding may be linked to the dorsal visual system while parallel coding of parts within objects takes place in the ventral system, although there may additionally be some dorsal involvement either when attention must be shifted within objects or when explicit spatial coding of parts is necessary for object identification.