Crossmodal enhancement in the LOC for visuohaptic object recognition over development.
ABSTRACT: Research has provided strong evidence of multisensory convergence of visual and haptic information within the visual cortex. These studies implement crossmodal matching paradigms to examine how systems use information from different sensory modalities for object recognition. Developmentally, behavioral evidence of visuohaptic crossmodal processing has suggested that communication within sensory systems develops earlier than across systems; nonetheless, it is unknown how the neural mechanisms driving these behavioral effects develop. To address this gap in knowledge, BOLD functional Magnetic Resonance Imaging (fMRI) was measured during delayed match-to-sample tasks that examined intramodal (visual-to-visual, haptic-to-haptic) and crossmodal (visual-to-haptic, haptic-to-visual) novel object recognition in children aged 7-8.5 years and adults. Tasks were further divided into sample encoding and test matching phases to dissociate the relative contributions of each. Results of crossmodal and intramodal object recognition revealed the network of known visuohaptic multisensory substrates, including the lateral occipital complex (LOC) and the intraparietal sulcus (IPS). Critically, both adults and children showed crossmodal enhancement within the LOC, suggesting a sensitivity to changes in sensory modality during recognition. These groups showed similar regions of activation, although children generally exhibited more widespread activity during sample encoding and weaker BOLD signal change during test matching than adults. Results further provided evidence of a bilateral region in the occipitotemporal cortex that was haptic-preferring in both age groups. This region abutted the bimodal LOtv, and was consistent with a medial to lateral organization that transitioned from a visual to haptic bias within the LOC. These findings converge with existing evidence of visuohaptic processing in the LOC in adults, and extend our knowledge of crossmodal processing in adults and children.
Project description:Functional magnetic resonance imaging (fMRI) studies have provided ample evidence for the involvement of the lateral occipital cortex (LO), fusiform gyrus (FG), and intraparietal sulcus (IPS) in visuo-haptic object integration. Here we applied 30 min of sham (non-effective) or real offline 1 Hz repetitive transcranial magnetic stimulation (rTMS) to perturb neural processing in left LO immediately before subjects performed a visuo-haptic delayed-match-to-sample task during fMRI. In this task, subjects had to match sample (S1) and target (S2) objects presented sequentially within or across vision and/or haptics in both directions (visual-haptic or haptic-visual) and decide whether or not S1 and S2 were the same objects. Real rTMS transiently decreased activity at the site of stimulation and remote regions such as the right LO and bilateral FG during haptic S1 processing. Without affecting behavior, the same stimulation gave rise to relative increases in activation during S2 processing in the right LO, left FG, bilateral IPS, and other regions previously associated with object recognition. Critically, the modality of S2 determined which regions were recruited after rTMS. Relative to sham rTMS, real rTMS induced increased activations during crossmodal congruent matching in the left FG for haptic S2 and the temporal pole for visual S2. In addition, we found stronger activations for incongruent than congruent matching in the right anterior parahippocampus and middle frontal gyrus for crossmodal matching of haptic S2 and in the left FG and bilateral IPS for unimodal matching of visual S2, only after real but not sham rTMS. The results imply that a focal perturbation of the left LO triggers modality-specific interactions between the stimulated left LO and other key regions of object processing possibly to maintain unimpaired object recognition. This suggests that visual and haptic processing engage partially distinct brain networks during visuo-haptic object matching.
Project description:Visuohaptic inputs offer redundant and complementary information regarding an object?s geometrical structure. The integration of these inputs facilitates object recognition in adults. While the ability to recognize objects in the environment both visually and haptically develops early on, the development of the neural mechanisms for integrating visual and haptic object shape information remains unknown. In the present study, we used functional Magnetic Resonance Imaging (fMRI) in three groups of participants, 4 to 5.5 year olds, 7 to 8.5 year olds, and adults. Participants were tested in a block design involving visual exploration of two-dimensional images of common objects and real textures, and haptic exploration of their three-dimensional counterparts. As in previous studies, object preference was defined as a greater BOLD response for objects than textures. The analyses specifically target two sites of known visuohaptic convergence in adults: the lateral occipital tactile-visual region (LOtv) and intraparietal sulcus (IPS). Results indicated that the LOtv is involved in visuohaptic object recognition early on. More importantly, object preference in the LOtv became increasingly visually dominant with development. Despite previous reports that the lateral occipital complex (LOC) is adult-like by 8 years, these findings indicate that at least part of the LOC is not. Whole-brain maps showed overlap between adults and both groups of children in the LOC. However, the overlap did not build incrementally from the younger to the older group, suggesting that visuohaptic object preference does not develop in an additive manner. Taken together, the results show that the development of neural substrates for visuohaptic recognition is protracted compared to substrates that are primarily visual or haptic.
Project description:High-level visual cortex in humans includes functionally defined regions that preferentially respond to objects, faces and places. It is unknown how these regions develop and whether their development relates to recognition memory. We used functional magnetic resonance imaging to examine the development of several functionally defined regions including object (lateral occipital complex, LOC)-, face ('fusiform face area', FFA; superior temporal sulcus, STS)- and place ('parahippocampal place area', PPA)-selective cortices in children (ages 7-11), adolescents (12-16) and adults. Right FFA and left PPA volumes were substantially larger in adults than in children. This development occurred by expansion of FFA and PPA into surrounding cortex and was correlated with improved recognition memory for faces and places, respectively. In contrast, LOC and STS volumes and object-recognition memory remained constant across ages. Thus, the ventral stream undergoes a prolonged maturation that varies temporally across functional regions, is determined by brain region rather than stimulus category, and is correlated with the development of category-specific recognition memory.
Project description:BACKGROUND: It has been shown that visual geometrical shape categories (rectangle and triangle) are graded structures organized around a prototype as demonstrated by perception and production tasks in adults as well as in children. The visual prototypical shapes are better recognized than other exemplars of the categories. Their existence could emerge from early exposure to these prototypical shapes that are present in our visual environment. The present study examined the role of visual experience in the existence of prototypical shapes by comparing the haptic recognition of geometrical shapes in congenitally blind and blindfolded adolescents. METHODOLOGY/PRINCIPAL FINDINGS: To determine whether the existence of a prototype effect (higher recognition of prototypical shapes than non prototypical shapes) depended on visual experience, congenitally blind and blindfolded sighted adolescents were asked to recognize in the haptic modality three categories of correct shapes (square, rectangle, triangle) varying in orientation (prototypical/canonical orientation vs. non prototypical/canonical orientation rotated by 45°) among a set of other shapes. A haptic prototype effect was found in the blindfolded sighted whereas no difference between prototypical and non prototypical correct shapes was observed in the congenitally blind. A control experiment using a similar visual recognition task confirmed the existence of a visual prototype effect in a group of sighted adolescents. CONCLUSION/SIGNIFICANCE: These findings show that the prototype effect is not intrinsic to the haptic modality but depends on visual experience. This suggests that the occurrence of visual and haptic prototypical shapes in the recognition of geometrical shape seems to depend on visual exposure to these prototypical shapes existing in our environment.
Project description:Visual object-recognition is thought to involve activation of a distributed network of cortical regions, nodes of which include the lateral prefrontal cortex, the so-called lateral occipital complex (LOC), and the hippocampal formation. It has been proposed that long-range oscillatory synchronization is a major mode of coordinating such a distributed network. Here, intracranial recordings were made from three humans as they performed a challenging visual object-recognition task that required them to identify barely recognizable fragmented line-drawings of common objects. Subdural electrodes were placed over the prefrontal cortex and LOC, and depth electrodes were placed within the hippocampal formation. Robust beta-band coherence was evident in all subjects during processing of recognizable fragmented images. Significantly lower coherence was evident during processing of unrecognizable scrambled versions of the same. The results indicate that transient beta-band oscillatory coupling between these three distributed cortical regions may reflect a mechanism for effective communication during visual object processing.
Project description:In this study we investigate previous claims that a region in the left posterior superior temporal sulcus (pSTS) is more activated by audiovisual than unimodal processing. First, we compare audiovisual to visual-visual and auditory-auditory conceptual matching using auditory or visual object names that are paired with pictures of objects or their environmental sounds. Second, we compare congruent and incongruent audiovisual trials when presentation is simultaneous or sequential. Third, we compare audiovisual stimuli that are either verbal (auditory and visual words) or nonverbal (pictures of objects and their associated sounds). The results demonstrate that, when task, attention, and stimuli are controlled, pSTS activation for audiovisual conceptual matching is 1) identical to that observed for intramodal conceptual matching, 2) greater for incongruent than congruent trials when auditory and visual stimuli are simultaneously presented, and 3) identical for verbal and nonverbal stimuli. These results are not consistent with previous claims that pSTS activation reflects the active formation of an integrated audiovisual representation. After a discussion of the stimulus and task factors that modulate activation, we conclude that, when stimulus input, task, and attention are controlled, pSTS is part of a distributed set of regions involved in conceptual matching, irrespective of whether the stimuli are audiovisual, auditory-auditory or visual-visual.
Project description:It is well known that motion facilitates the visual perception of solid object shape, particularly when surface texture or other identifiable features (e.g., corners) are present. Conventional models of structure-from-motion require the presence of texture or identifiable object features in order to recover 3-D structure. Is the facilitation in 3-D shape perception similar in magnitude when surface texture is absent? On any given trial in the current experiments, participants were presented with a single randomly-selected solid object (bell pepper or randomly-shaped "glaven") for 12 seconds and were required to indicate which of 12 (for bell peppers) or 8 (for glavens) simultaneously visible objects possessed the same shape. The initial single object's shape was defined either by boundary contours alone (i.e., presented as a silhouette), specular highlights alone, specular highlights combined with boundary contours, or texture. In addition, there was a haptic condition: in this condition, the participants haptically explored with both hands (but could not see) the initial single object for 12 seconds; they then performed the same shape-matching task used in the visual conditions. For both the visual and haptic conditions, motion (rotation in depth or active object manipulation) was present in half of the trials and was not present for the remaining trials. The effect of motion was quantitatively similar for all of the visual and haptic conditions-e.g., the participants' performance in Experiment 1 was 93.5 percent higher in the motion or active haptic manipulation conditions (when compared to the static conditions). The current results demonstrate that deforming specular highlights or boundary contours facilitate 3-D shape perception as much as the motion of objects that possess texture. The current results also indicate that the improvement with motion that occurs for haptics is similar in magnitude to that which occurs for vision.
Project description:Abstract The lateral occipital complex (LOC) is a set of areas in the human occipito-temporal cortex responding to objects as opposed to low-level control stimuli. Conventional functional magnetic resonance imaging (fMRI) analysis methods based on regional averages could not detect signals discriminative of different types of objects in this region. Here, we examined fMRI signals using multivariate pattern recognition (support vector classification) to systematically explore the nature of object-related information available in fine-grained activity patterns in the LOC. Distributed fMRI signals from the LOC allowed for above-chance discrimination not only of the category but also of within-category exemplars of everyday man-made objects, and such exemplar-specific information generalized across changes in stimulus size and viewpoint, particularly in posterior subregions. Object identity could also be predicted from responses of the early visual cortex, even significantly across the changes in size and viewpoint used here. However, a dissociation was observed between these two regions of interest in the degree of discrimination for objects relative to size: In the early visual cortex, two different sizes of the same object were even better discriminated than two different objects (in accordance with measures of pixelwise stimulus similarity), whereas the opposite was true in the LOC. These findings provide the first evidence that direct evoked fMRI activity patterns in the LOC can be different for individual object exemplars (within a single category). We propose that pattern recognition methods as used here may provide an alternative approach to study mechanisms of neuronal representation based on aspects of the fMRI response independent of those assessed in adaptation paradigms.
Project description:A single experiment evaluated the haptic-visual cross-modal matching of solid object shape. One set of randomly shaped artificial objects was used (sinusoidally modulated spheres, SMS) as well as two sets of naturally shaped objects (bell peppers, Capsicum annuum and sweet potatoes, Ipomoea batatas). A total of 66 adults participated in the study. The participants' task was to haptically explore a single object on any particular trial and subsequently indicate which of 12 simultaneously visible objects possessed the same shape. The participants' performance for the natural objects was 60.9 and 78.7 percent correct for the bell peppers and sweet potatoes, respectively. The analogous performance for the SMS objects, while better than chance, was far worse (18.6 percent correct). All of these types of stimulus objects possess a rich geometrical structure (e.g., they all possess multiple elliptic, hyperbolic, and parabolic surface regions). Nevertheless, these three types of stimulus objects are perceived differently: Individual members of sweet potatoes and bell peppers are largely identifiable to human participants, while the individual SMS objects are not. Analyses of differential geometry indicate that these natural objects (e.g., bell peppers and sweet potatoes) possess heterogeneous spatial configurations of distinctly curved surface regions, and this heterogeneity is lacking in SMS objects. The current results therefore suggest that increases in surface structure heterogeneity facilitate human object recognition.
Project description:Although visual cortical engagement in haptic shape perception is well established, its relationship with visual imagery remains controversial. We addressed this using functional magnetic resonance imaging during separate visual object imagery and haptic shape perception tasks. Two experiments were conducted. In the first experiment, the haptic shape task employed unfamiliar, meaningless objects, whereas familiar objects were used in the second experiment. The activations evoked by visual object imagery overlapped more extensively, and their magnitudes were more correlated, with those evoked during haptic shape perception of familiar, compared to unfamiliar, objects. In the companion paper (Deshpande et al., this issue), we used task-specific functional and effective connectivity analyses to provide convergent evidence: these analyses showed that the neural networks underlying visual imagery were similar to those underlying haptic shape perception of familiar, but not unfamiliar, objects. We conclude that visual object imagery is more closely linked to haptic shape perception when objects are familiar, compared to when they are unfamiliar.