Boundaries in Spatial Navigation and Visual Scene Perception

Time/Room: Friday, May 13, 2016, 12:00 – 2:00 pm, Pavilion
Organizer(s): Soojin Park, Johns Hopkins University and Sang Ah Lee, University of Trento
Presenters: Sang Ah Lee, Joshua B Julian, Nathaniel J. Killian, Tom Hartley, Soojin Park, Katrina Ferrara

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Symposium Description

The ability to navigate in the world using vision is intrinsically tied to the ability to analyze spatial relationship within a scene. For the past few decades, navigation researchers have shown that humans and nonhuman animals alike compute locations by using a spontaneously encoded geometry of the 3D environmental boundary layouts. This finding has been supported by neural evidence showing boundary-specific inputs to hippocampal place-mapping. More recently, researchers in visual scene perception have shown that boundaries not only play an important role in defining geometry for spatial navigation, but also in visual scene perception. How are boundary representations in scene perception related to those in navigation? What are the defining features of boundaries, and what are their neural correlates? The aim of this symposium is to bridge research from various subfields of cognitive science to discuss the specific role of boundaries in the processing of spatial information and to converge on a coherent theoretical framework for studying visual representations of boundaries. To achieve this, we have brought together an interdisciplinary group of speakers to present studies of boundary representations on a broad range of subject populations, from rodents, to primates, to individuals with genetic disorders, using various experimental methods (developmental, behavioral, fMRI, TMS, single-cell and population coding). The theoretical flow of the symposium will start with behavioral studies showing specificity and primacy of boundaries in spatial navigation and memory in both humans and a wide range of nonhuman vertebrates. Then, we will ask whether neural representations of boundary geometry can be derived from visual input, as opposed to active navigation, using primate’s saccadic eye gaze and human scene perception. Lastly, we will present evidence of spatial impairment marked by a dysfunction of boundary-processing mechanisms in Williams Syndrome. We believe that this symposium will be of great interest to VSS attendees for the following reasons: First, these convergent findings from independent research approaches to spatial representations and their neural correlates will make a powerful impact on theories of spatial information processing, from visual perception to hippocampal spatial mapping. Second, a better understanding of boundary geometry can broadly inform any research that involves visuo-spatial representations, such as studies on spatial perspective and saccadic eye movements. Finally, the methodological breadth of this symposium, and its aim to integrate them to a coherent picture will provide a new perspective on the power of multidisciplinary research in visual and cognitive sciences.


Boundaries in space: A comparative approach

Speaker: Sang Ah Lee; Center for Mind/Brain Sciences, University of Trento

Spatial navigation provides a unique window into the evolutionary and developmental origins of complex behaviors and memory, due to its richness in representation and computation, its striking similarities between distantly related species, its neural specificity, and its transformation across human development. Environmental boundaries have been shown to play a crucial role in both neural and behavioral studies of spatial representation. In this talk, I will discuss evidence on boundary coding on three different levels: First, I will share my findings showing the primacy and specificity of visual representations of 3D environmental “boundaries” in early spatial navigation in children. Second, I will argue that the cognitive mechanisms underlying boundary representations are shared and widespread across the phylogenetic tree. Finally, I will bring together insights gathered from behavioral findings to investigate the neural underpinnings of boundary coding. From the firing of neurons in a navigating rat’s brain, to a child’s developing understanding of abstract space, I will argue that boundary representation is a fundamental, evolutionarily ancient ability that serves as a basis for spatial cognition and behavior.

Mechanisms for encoding navigational boundaries in the mammalian brain

Speaker: Joshua B Julian; Department of Psychology, University of Pennsylvania
Authors: Alex T Keinath, Department of Psychology, University of Pennsylvania; Jack Ryan, Department of Psychology, University of Pennsylvania; Roy H Hamilton, Department of Neurology, University of Pennsylvania; Isabel A Muzzio, Department of Biology, University of Texas: San Antonio; Russell A Epstein, Department of Psychology, University of Pennsylvania

Thirty years of research suggests that environmental boundaries exert powerful control over navigational behavior, often to the exclusion of other navigationally-relevant cues, such as objects or visual surface textures. Here we present findings from experiments in mice and humans demonstrating the existence of specialized mechanisms for processing boundaries during navigation. In the first study, we examined the navigational behavior of disoriented mice trained to locate rewards in two chambers with geometrically identical boundaries, distinguishable based on the visual textures along one wall. We observed that although visual textures were used to identify the chambers, those very same cues were not used to disambiguate facing directions within a chamber. Rather, recovery of facing directions relied exclusively on boundary geometry. These results provide evidence for dissociable processes for representing boundaries and other visual cues. In a second line of work, we tested whether the human visual system contains neural regions specialized for processing of boundaries. Specifically, we tested the prediction that the Occipital Place Area (OPA) might play a critical role in boundary-based navigation, by extracting boundary information from visual scenes. To do so, we used transcranial magnetic stimulation (TMS) to interrupt processing in the OPA during a navigation task that required participants to learn object locations relative to boundaries and non-boundary cues. We found that TMS of the OPA impaired learning of locations relative to boundaries, but not relative to landmark objects or large-scale visual textures. Taken together, these results provide evidence for dedicated neural circuitry for representing boundary information.

Neuronal representation of visual borders in the primate entorhinal cortex

Speaker: Nathaniel J. Killian; Department of Neurosurgery, Massachusetts General Hospital-Harvard Medical School
Authors: Elizabeth A Buffalo, Department of Physiology and Biophysics, University of Washington

The entorhinal cortex (EC) is critical to the formation of memories for complex visual relationships. Thus we might expect that EC neurons encode visual scenes within a consistent spatial framework to facilitate associations between items and the places where they are encountered. In particular, encoding of visual borders could provide a means to anchor visual scene information in allocentric coordinates. Studies of the rodent EC have revealed neurons that represent location, heading, and borders when an animal is exploring an environment. Because of interspecies differences in vision and exploratory behavior, we reasoned that the primate EC may represent visual space in a manner analogous to the rodent EC, but without requiring physical visits to particular places or items. We recorded activity of EC neurons in non-human primates (Macaca mulatta) that were head-fixed and freely viewing novel photographs presented in a fixed external reference frame. We identified visual border cells, neurons that had increased firing rate when gaze was close to one or more image borders. Border cells were co-localized with neurons that represented visual space in a grid-like manner and with neurons that encoded the angular direction of saccadic eye movements. As a population, primate EC neurons appear to represent gaze location, gaze movement direction, and scene boundaries. These spatial representations were detected in the presence of changing visual content, suggesting that the EC provides a consistent spatial framework for encoding visual experiences.

Investigating cortical encoding of visual parameters relevant to spatial cognition and environmental geometry in humans.

Speaker: Tom Hartley; Department of Psychology, University of York, UK
Authors: David Watson, Department of Psychology, University of York, UK; Tim Andrews, Department of Psychology, University of York, UK

Studies of firing properties of cells in the rodent hippocampal formation indicate an important role for “boundary cells” in anchoring the allocentric firing fields of place and grid cells. To understand how spatial variables such as the distance to local boundaries might be derived from visual input in humans, we are investigating links between the statistical properties of natural scenes and patterns of neural response in scene selective visual cortex. In our latest work we used a data-driven analysis to select clusters of natural scenes from a large database, solely on the basis of their image properties. Although these visually-defined clusters did not correspond to typical experimenter-defined categories used in earlier work, we found they elicited distinct and reliable patterns of neural response in parahippocampal cortex, and that the relative similarity of the response patterns was better explained in terms of low-level visual properties of the images than by local semantic information. Our results suggest that human parahippocampal cortex encodes visual parameters (including properties relevant to environmental geometry). Our approach opens the way to isolating these parameters and investigating their relationship to spatial variables.

Complementary neural representation of scene boundaries

Speaker: Soojin Park; Department of Cognitive Science, Johns Hopkins University
Authors: Katrina Ferrara, Center for Brain Plasticity and Recovery, Georgetown University

Environmental boundaries play a critical role in defining spatial geometry and restrict our movement within an environment. Developmental research with 4-year-olds shows that children are able to reorient themselves by the geometry of a curb that is only 2 cm high, but fail to do so when the curb boundary is replaced by a flat mat on the floor (Lee & Spelke, 2011). In this talk, we will present evidence that such fine-grained sensitivity to a 3D boundary cue is represented in visual scene processing regions of the brain, parahippocampal place area (PPA) and retrosplenial cortex (RSC). First, we will present univariate and multivoxel pattern data from both regions to suggest that they play complementary roles in the representation of boundary cues. The PPA shows disproportionately strong sensitivity to the presence of a slight vertical boundary, demonstrating a neural signature that corresponds to children’s behavioral sensitivity to slight 3D vertical cues (i.e., the curb boundary). RSC did not display this sensitivity. We will argue that this sensitivity does not simply reflect low-level image differences across conditions. Second, we investigate the nature of boundary representation in RSC by parametrically varying the height of boundaries in the vertical dimension. We find that RSC’s response matches a behavioral categorical decision point for the boundary’s functional affordance (e.g., whether the boundary limits the viewer’s potential navigation or not). Collectively, this research serves to highlight boundary structure as a key component of space that is represented in qualitatively different ways across two scene-selective brain regions.

Neural and behavioral sensitivity to boundary cues in Williams syndrome

Speaker: Katrina Ferrara; Center for Brain Plasticity and Recovery, Georgetown University
Authors: Barbara Landau, Department of Cognitive Science, Johns Hopkins University; Soojin Park, Department of Cognitive Science, Johns Hopkins University

Boundaries are fundamental features that define a scene and contribute to its geometric shape. Our previous research using fMRI demonstrates a distinct sensitivity to the presence of vertical boundaries in scene representation by the parahippocampal place area (PPA) in healthy adults (Ferrara & Park, 2014). In the present research, we show that this sensitivity to boundaries is impaired by genetic deficit. Studying populations with spatial disorders can provide insight to potential brain/behavior links that may be difficult to detect in healthy adults. We couple behavioral and neuroimaging methods to study individuals with Williams syndrome (WS), a disorder characterized by the deletion of 25 genes and severe impairment in a range of spatial functions. When both humans and animals are disoriented in a rectangular space, they are able to reorient themselves by metric information conveyed by the enclosure’s boundaries (e.g., long wall vs. short wall). Using this reorientation process as a measure, we find that individuals with WS are unable to reorient by a small boundary cue, in stark contrast to the behavior of typically developing (TD) children (Lee & Spelke, 2011). Using fMRI, we find a linked neural pattern in that the WS PPA does not detect the presence of a small boundary within a scene. Taken together, these results demonstrate that atypical patterns of reorientation correspond with less fine-grained representation of boundaries at the neural level in WS. This suggests that sensitivity to the geometry of boundaries is one of the core impairments that underlies the WS reorientation deficit.

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