Segregation and persistence of form in the lateral occipital complex

While the lateral occipital complex (LOC) has been shown to be implicated in object recognition, it is unclear whether this brain area is responsive to low-level stimulus-driven features or high-level representational processes. We used scrambled shape-from-motion displays to disambiguate the presence of contours from figure-ground segregation and to measure the strength of the binding process for shapes without contours. We found persisting brain activation in the LOC for scrambled displays after the motion stopped indicating that this brain area subserves and maintains figure-ground segregation processes, a low-level function in the object processing hierarchy. In our second experiment, we found that the figure-ground segregation process has some form of spatial constancy indicating top-down influences. The persisting activation after the motion stops suggests an intermediate role in object recognition processes for this brain area and might provide further evidence for the idea that the lateral occipital complex subserves mnemonic functions mediating between iconic and short-term memory.     

Altered figure-ground perception in monkeys with an extra-striate lesion

The visual system binds and segments the elements of an image into coherent objects and their surroundings. Recent findings demonstrate that primary visual cortex is involved in this process of figure-ground organization. In the primary visual cortex the late part of a neural response to a stimulus correlates with figure-ground segregation and perception. Such a late onset indicates an involvement of feedback projections from higher visual areas. To investigate the possible role of feedback in figure-ground perception we removed dorsal extra-striate areas of the monkey visual cortex. The findings show that figure-ground perception is reduced when the figure is presented in the lesioned hemifield and perception is normal when the figure appeared in the intact hemifield. In conclusion, our observations show the importance for recurrent processing in visual perception.     

Configural specificity of the lateral occipital cortex

While regions of the lateral occipital cortex (LOC) are known to be selective for objects relative to feature-matched controls, it is not known what set of cues or configurations are used to promote this selectivity. Many theories of perceptual organization have emphasized the figure-ground relationship as being especially important in object-level processing. In the present work we studied the role of perceptual organization in eliciting visual evoked potentials from the object selective LOC. To do this, we used two-region stimuli in which the regions were modulated at different temporal frequencies and were comprised of either symmetric or asymmetric arrangements. The asymmetric arrangement produced an unambiguous figure-ground relationship consistent with a smaller figure region surrounded by a larger background, while four different symmetric arrangements resulted in ambiguous figure-ground relationships but still possessed strong kinetic boundaries between the regions. The surrounded figure-ground arrangement evoked greater activity in the LOC relative to first-tier visual areas (V1-V3). Response selectivity in the LOC, however, was not present for the four different types of symmetric stimuli. These results suggest that kinetic texture boundaries alone are not sufficient to trigger selective processing in the LOC, but that the spatial configuration of a figure that is surrounded by a larger background is both necessary and sufficient to selectively activate the LOC.     

Masking interrupts figure-ground signals in V1

In a backward masking paradigm, a target stimulus is rapidly (<100 msec) followed by a second stimulus. This typically results in a dramatic decrease in the visibility of the target stimulus. It has been shown that masking reduces responses in V1. It is not known, however, which process in V1 is affected by the mask. In the past, we have shown that in V1, modulations of neural activity that are specifically related to figure-ground segregation can be recorded. Here, we recorded from awake macaque monkeys, engaged in a task where they had to detect figures from background in a pattern backward masking paradigm. We show that the V1 figure-ground signals are selectively and fully suppressed at target-mask intervals that psychophysically result in the target being invisible. Initial response transients, signalling the features that make up the scene, are not affected. As figure-ground modulations depend on feedback from extrastriate areas, these results suggest that masking selectively interrupts the recurrent interactions between V1 and higher visual areas.     

Neural response to the visual familiarity of faces

Recognizing personally familiar faces is the result of a spatially distributed process that involves visual perceptual areas and areas that play a role in other cognitive and social functions, such as the anterior paracingulate cortex, the precuneus and the amygdala [M.I. Gobbini, E. Leibenluft, N. Santiago, J.V. Haxby, Social and emotional attachment in the neural representation of faces, Neuroimage 22 (2004) 1628-1635; M.I. Gobbini, J.V. Haxby, Neural systems for recognition of familiar faces, Neuropsychologia, in press; E. Leibenluft, M.I. Gobbini, T. Harrison, J.V. Haxby, Mothers' neural activation in response to pictures of their, and other, children, Biol. Psychiatry 56 (2004) 225-232]. In order to isolate the role of visual familiarity in face recognition, we used fMRI to measure the response to faces characterized by experimentally induced visual familiarity that carried no biographical information or emotional content. The fMRI results showed a stronger response in the precuneus to the visually familiar faces consistent with studies that implicate this region in the retrieval of information from long-term memory and imagery. Moreover, this finding supports the hypothesis of a key role for the precuneus in the acquisition of familiarity with faces [H. Kosaka, M. Omori, T. Iidaka, T. Murata, T. Shimoyama, T. Okada, N. Sadato, Y. Yonekura, Y. Wada, Neural substrates participating in acquisition of facial familiarity: an fMRI study, Neuroimage 20 (2003) 1734-1742]. By contrast, the visually familiar faces evoked a weaker response in the fusiform gyrus, which may reflect the development of a sparser encoding or a reduced attentional load when processing stimuli that are familiar. The visually familiar faces also evoked a weaker response in the amygdala, supporting the proposed role of this structure in mediating the guarded attitude when meeting someone new.     

Normal form from biological motion despite impaired ventral stream function

We explored the extent to which biological motion perception depends on ventral stream integration by studying LG, an unusual case of developmental visual agnosia. LG has significant ventral stream processing deficits but no discernable structural cortical abnormality. LG's intermediate visual areas and object-sensitive regions exhibit abnormal activation during visual object perception, in contrast to area V5/MT+ which responds normally to visual motion (Gilaie-Dotan, Perry, Bonneh, Malach, & Bentin, 2009). Here, in three studies we used point light displays, which require visual integration, in adaptive threshold experiments to examine LG's ability to detect form from biological and non-biological motion cues. LG's ability to detect and discriminate form from biological motion was similar to healthy controls. In contrast, he was significantly deficient in processing form from non-biological motion. Thus, LG can rely on biological motion cues to perceive human forms, but is considerably impaired in extracting form from non-biological motion. Finally, we found that while LG viewed biological motion, activity in a network of brain regions associated with processing biological motion was functionally correlated with his V5/MT+ activity, indicating that normal inputs from V5/MT+ might suffice to activate his action perception system. These results indicate that processing of biologically moving form can dissociate from other form processing in the ventral pathway. Furthermore, the present results indicate that integrative ventral stream processing is necessary for uncompromised processing of non-biological form from motion.     

Effects of attention and arousal on early responses in striate cortex

Humans employ attention to facilitate perception of relevant stimuli. Visual attention can bias the selection of a location in the visual field, a whole visual object or any visual feature of an object. Attention draws on both current behavioral goals and/or the saliency of physical attributes of a stimulus, and it influences activity of different brain regions at different latencies. Attentional effect in the striate and extrastriate cortices has been the subject of intense research interest in many recent studies. The consensus emerging from them places the first attentional effects in extrastriate areas, which in turn modulate activity of V1 at later latencies. In this view attention influences activity in striate cortex some 150 ms after stimulus onset. Here we use magnetoencephalography to compare brain responses to foveally presented identical stimuli under the conditions of passive viewing, when the stimuli are irrelevant to the subject and under an active GO/NOGO task, when the stimuli are cues instructing the subject to make or inhibit movement of his/her left or right index finger. The earliest striate activity was identified 40-45 ms after stimulus onset, and it was identical in passive and active conditions. Later striate response starting at about 70 ms and reaching a peak at about 100 ms showed a strong attentional modulation. Even before the striate cortex, activity of the right inferior parietal lobule was modulated by attention, suggesting this region as a candidate for mediating attentional signals to the striate cortex.     

Figure-ground segregation requires two distinct periods of activity in V1: a transcranial magnetic stimulation study

Discriminating objects from their surroundings by the visual system is known as figure-ground segregation. This process entails two different subprocesses: boundary detection and subsequent surface segregation or 'filling in'. In this study, we used transcranial magnetic stimulation to test the hypothesis that temporally distinct processes in V1 and related early visual areas such as V2 or V3 are causally related to the process of figure-ground segregation. Our results indicate that correct discrimination between two visual stimuli, which relies on figure-ground segregation, requires two separate periods of information processing in the early visual cortex: one around 130-160 ms and the other around 250-280 ms.     

Eye position-dependent activity in the primary visual area as revealed by fMRI

Internal senses of the position of the eye in the orbit may influence the cognitive processes that take into account gaze and limb positioning for movement or guiding actions. Neuroimaging studies have revealed eye position-dependent activity in the extrastriate visual, parietal, and frontal areas, but, at the earliest vision stage, the role of the primary visual area (V1) in these processes remains unclear. Functional MRI (fMRI) was used to investigate the effect of eye position on V1 activity evoked by a quarter-field stimulation using a visual checkerboard. We showed that the amplitude of V1 activity was modulated by the position of the eye, the activity being maximal when both the eye and head positions were aligned. Previous studies gave impetus to the emerging view that V1 activity is a cortical area in which contextual influences take place. The present study suggests that eye position may affect an early stage of visual processing.     

The inversion effect in visual word form processing

Reading is one of the best well-practiced visual tasks for modern people. We investigated how the visual cortex analyzes spatial configuration in written words by studying the inversion effect in Chinese character processing. We measured the psychometric functions and brain activations for upright real-characters and non-characters and their inverted (upside down) versions. In the psychophysical experiment, the real-characters showed an inversion effect at both 1° and 4° eccentricities, while the non-characters showed no inversion effect for all eccentricities tested. In the functional magnetic resonance image (fMRI) experiment, the left fusiform gyrus and a small area in the bilateral lateral occipital regions showed a significant differential activation between upright and inverted real-characters. The bilateral fusiform gyri also show differential activation between upright real- and non-characters. The dorsal lateral occipital regions showed character-selective activation when compared with scrambled lines. The result suggested that the occipitoparietal regions may analyze the local features of an object regardless of its familiarity. Therefore, the lateral occipital regions may play an intermediate role in integrating the local information in an object. Finally, the fusiform gyrus plays a critical role in analyzing global configurations of a visual word form. This is consistent with the notion that the human visual cortex analyzes an object in a hierarchical way.     

Visual topography of area TEO in the macaque.

Previous studies have mapped the visuotopic organization of visual areas from V1 through V4 in the occipital cortex and of area TE in the temporal cortex, but the cortex in between, at the occipito-temporal junction, has remained relatively unexplored. To determine the visuotopic organization of this region, receptive fields were mapped at 1,200 visually responsive sites on 370 penetrations in the ventral occipital and temporal cortex of five macaques. We identified a new visual area, roughly corresponding to cytoarchitectonic area TEO, located between the ventral portion of V4 and area TE. Receptive fields in TEO are intermediate in size between those in V4 and TE and have a coarse visuotopic organization. Collectively, receptive fields in TEO appear to cover nearly the entire contralateral visual field. The foveal and parafoveal representation of TEO is located laterally on the convexity of the inferior temporal gyrus, and the peripheral field is represented medially on the ventral surface of the hemisphere, within and medial to the occipitotemporal sulcus. Beyond the medial border of TEO, within cyteoarchitectonic area TF, is another visually responsive region, which we have termed VTF; this region may also have some crude visual topography. Bands of constant eccentricity in TEO appear to be continuous with those in V2, V3v, and V4. The upper field representation in TEO is located adjacent to that in ventral V4, with a representation of the horizontal meridian forming the boundary between the two areas. The lower field representation in TEO is located just anterior to the upper field but is smaller. In contrast to the orderly representation of eccentricity in TEO, we found little consistent representation of polar angle, other than the separation of upper and lower fields. The results of injecting anatomical tracers in two animals suggest that TEO is an important link in the pathway that relays visual information from V1 to the inferior temporal cortex. TEO is thus likely to play an important role in pattern perception.     

Figure-ground representation and its decay in primary visual cortex

We used fMRI to study figure-ground representation and its decay in primary visual cortex (V1). Human observers viewed a motion-defined figure that gradually became camouflaged by a cluttered background after it stopped moving. V1 showed positive fMRI responses corresponding to the moving figure and negative fMRI responses corresponding to the static background. This positive-negative delineation of V1 "figure" and "background" fMRI responses defined a retinotopically organized figure-ground representation that persisted after the figure stopped moving but eventually decayed. The temporal dynamics of V1 "figure" and "background" fMRI responses differed substantially. Positive "figure" responses continued to increase for several seconds after the figure stopped moving and remained elevated after the figure had disappeared. We propose that the sustained positive V1 "figure" fMRI responses reflected both persistent figure-ground representation and sustained attention to the location of the figure after its disappearance, as did subjects' reports of persistence. The decreasing "background" fMRI responses were relatively shorter-lived and less biased by spatial attention. Our results show that the transition from a vivid figure-ground percept to its disappearance corresponds to the concurrent decay of figure enhancement and background suppression in V1, both of which play a role in form-based perceptual memory.     

Decision-related activity in the macaque dorsal visual pathway.

Brain areas at higher levels of cortical organization are thought to be more involved in decision processes than are earlier, i.e. lower, sensory areas. Hence, neuronal activity correlated with decisions should vary with an area's position in the cortical hierarchy. To test this proposal, we investigated whether a change in neuronal activity during error trials depends in a systematic way on cortical hierarchical position. While macaque monkeys discriminated the direction of moving visual stimuli, the activity of direction-selective neurons was recorded in four extrastriate visual areas: V3A, the middle temporal area, the middle superior temporal area and the posterior part of the superior temporal polysensory area. Neuronal activity was significantly reduced in all areas when the monkeys made errors in judging the direction of stimuli moving in the preferred direction with low and intermediate luminance contrast. The amount of activity reduction was approximately 50% in all of the visual areas. Thus, the activity on error trials is reduced in early visual processing, independent of the hierarchy in the dorsal visual pathway. The activity reduction depended on stimulus contrast and the direction of the decision relative to the stimulus motion. It was profound and significant in all areas at low stimulus contrast. However, it was nonsignificant at high stimulus contrast. Our data suggest that activity reduction on error trials is due to lack of attention in association with stimulus expectation.     

Children with autism spectrum disorder spontaneously use scene knowledge to modulate visual object processing

Several studies have investigated contextual influences on visual object processing in individuals with autism spectrum disorder (ASD) and failed to find reduced context effects. However, these studies did not properly account for local inter-object effects and/or the influence of post-perceptual processes, leaving it unclear whether individuals with ASD display equally large global top-down effects of context, or whether they rely on a more local mechanism producing the same result. In this study, an eye-movement paradigm was used to investigate implicitly induced context effects on visual object processing in children with ASD compared to matched controls. To find out whether the context effects in the ASD group were, to the same extent, due to early top-down influences on object recognition, we also examined the interaction between context effects and the ease of object recognition. Both groups displayed equally large context effects and congruent contextual information facilitated object recognition to the same extent in both groups. This indicates that the context effects in the ASD group did not result from the operation of a more local, less top-down mechanism. These findings contradict predictions based on the weak central coherence account. However, a good alternative to explain all inconsistencies is currently lacking.     

Repetition priming effects dissociate between miniature eye movements and induced gamma‐band responses in the human electroencephalogram

The role of induced gamma‐band responses (iGBRs) in the human electroencephalogram (EEG) is a controversial topic. On the one hand, iGBRs have been associated with neuronal activity reflecting the (re‐)activation of cortical object representations. On the other hand, it was shown that miniature saccades (MSs) lead to high‐frequency artifacts in the EEG that can mimic cortical iGBRs. We recorded EEG and eye movements simultaneously while participants were engaged in a combined repetition priming and object recognition experiment. MS rates were mainly modulated by object familiarity in a time window from 100 to 300 ms after stimulus onset. In contrast, artifact‐corrected iGBRs were sensitive to object repetition and object familiarity in a prolonged time window. EEG source analyses revealed that stimulus repetitions modulated iGBRs in temporal and occipital cortex regions while familiarity was associated with activity in parieto‐occipital regions. These results are in line with neuroimaging studies employing functional magnetic resonance imaging or magnetoencephalography. We conclude that MSs reflect early mechanisms of visual perception while iGBRs mirror the activation of cortical networks representing a perceived object.     

Material Specificity Drives Medial Temporal Lobe Familiarity But Not Hippocampal Recollection

The specific role of the perirhinal (PRC), entorhinal (ERC) and parahippocampal cortices (PHC) in supporting familiarity‐based recognition remains unknown. An fMRI study explored whether these medial temporal lobe (MTL) structures responded in the same way or differentially to familiarity as a function of stimulus type at recognition. A secondary aim was to explore whether the hippocampus responds in the same way to equally strong familiarity and recollection and whether this is influenced by the kind of stimulus involved. Univariate and multivariate analyses revealed that familiarity responses in the PRC, ERC, PHC and the amygdala are material‐specific. Specifically, the PRC and ERC selectively responded to object familiarity, while the PHC responded to both object and scene familiarity. The amygdala only responded to familiarity memory for faces. The hippocampus did not respond to stimulus familiarity for any of the three types of stimuli, but it did respond to recollection for all three types of stimuli. This was true even when recollection was contrasted to equally accurate familiarity. Overall, the findings suggest that the role of the MTL neocortices and the amygdala in familiarity‐based recognition depends on the kind of stimulus in memory, whereas the role of the hippocampus in recollection is independent of the type of cuing stimulus. © 2016 The Authors Hippocampus Published by Wiley Periodicals, Inc.     

Configural and analytical processing of familiar and unfamiliar objects

Configural processing could develop for non-face visual objects as one becomes familiar with those objects through repeated exposure. To explore the role of familiarity in object recognition, we studied the effect of adaptation to a visual object (adapting stimulus) on the identification performance of other objects (test stimulus) while adapting and test stimuli were exactly the same, shared parts or were completely different. We used a subset of English alphabets (p, q, d and b) as familiar objects and an unfamiliar set of symbols constructed from same parts but with different configurations. Adaptation to a member of each set led to a lower identification performance for that object in a crowding paradigm. Adaptation to each member of the unfamiliar set resulted in decreased identification performance for the same object and those members of the set that shared parts with the adapting stimulus. But no such transfer of adaptation was observed for the familiar set. Our results support the notion that processing of object parts plays an important role in the recognition of unfamiliar objects while recognition of familiar objects is mainly based on configural processing mechanisms.     

Electromagnetic correlates of recognition memory processes.

Recognition memory is critically dependent on a hierarchically organized network of brain areas including the visual ventral stream, medial temporal lobe structures, frontal and parietal cortices. In recent years, cognitive theories of recognition memory have been helpful to further our understanding of the functional organization of this network. A prominent, although not unchallenged, set of theories proposes that recognition memory is not a unitary phenomenon, but can be based on the recollection of contextual information about events or on familiarity in the absence of recollection. A number of hemodynamic and electromagnetic studies have been undertaken to relate recollection and familiarity to neuronal substrates both in healthy subjects as well as in patients with brain lesions. Today, it is evident that both event-related potential and event-related field (ERP/ERF) data as well as data of oscillatory brain activity (e.g., theta oscillations) are necessary to fully understand the neural dynamics of recollection and familiarity and their relationship to functional anatomy. Ultimately, such data are required from patients with isolated brain injuries to designated components of the networks (such as the hippocampus) to obtain converging evidence for functional relationships between recollection and familiarity and respective neuroanatomic substrates. The complexity of this task is highlighted by findings indicating that recognition memory can already be affected by preparatory processes prior to stimulus onset.     

Behavioral and neuropsychological foundations of olfactory fear conditioning

Pavlovian fear conditioning procedures have been a fruitful means of exploring the neural substrates of associative learning. There is now substantial evidence suggesting that many aspects of conditioned fear depend critically upon the integrity of the amygdala and the perirhinal cortex. Recent studies in our laboratory examining the contributions of these areas to olfactory and contextual fear conditioning are reviewed; collectively the results of these studies suggest that the amygdala participates critically in the acquisition and expression of fear conditioned to both an olfactory conditioned stimulus (CS) and to the training context, while the perirhinal cortex contributes to olfactory, but not contextual, fear conditioning. Moreover, it appears that perirhinal cortex may play a prominent role in recognition of the CS following conditioning. These results are discussed in light of the extent to which they replicate and extend previous research examining the contributions of these areas to fear conditioned to auditory and visual CSs.