To interact rapidly and effectively with the environment, the mammalian brain needs a representat... more To interact rapidly and effectively with the environment, the mammalian brain needs a representation of the spatial layout of the external world (or a “cognitive map”). A person might need to know where she is standing to find her way home, for instance, or might need to know where she is looking to reach for her out-of-sight keys. For many behaviors, however, simply possessing a map is not enough; in order for a map to be useful in a dynamic world, it must be anchored to stable environmental cues. The goal of the present research is to address this spatial anchoring problem in two different domains: navigation and vision. In the first part of the thesis, which comprises Chapters 1-3, we examine how navigators use perceptual information to re-anchor their cognitive map after becoming lost, a process known as spatial reorientation. Using a novel behavioral paradigm with rodents, in Chapter 2 we show that the cognitive map is reoriented by dissociable inputs for identifying where one ...
To guide spatial behavior, the brain must retrieve memories that are appropriately associated wit... more To guide spatial behavior, the brain must retrieve memories that are appropriately associated with different navigational contexts. Contextual memory might be mediated by cell ensembles in the hippocampal formation that alter their responses to changes in context, processes known as remapping and realignment in the hippocampus and entorhinal cortex, respectively. However, whether remapping and realignment guide context-dependent spatial behavior is unclear. To address this issue, human participants learned object-location associations within two distinct virtual reality environments and subsequently had their memory tested during functional MRI (fMRI) scanning. Entorhinal grid-like representations showed realignment between the two contexts, and coincident changes in fMRI activity patterns consistent with remapping were observed in the hippocampus. Critically, in a third ambiguous context, trial-by-trial remapping and realignment in the hippocampal-entorhinal network predicted conte...
The ability to recover one's bearings when lost is a skill that is fundamental for spatial naviga... more The ability to recover one's bearings when lost is a skill that is fundamental for spatial navigation. We review the cognitive and neural mechanisms that underlie this ability, with the aim of linking together previously disparate findings from animal behavior, human psychology, electrophysiology, and cognitive neuroscience. Behavioral work suggests that reorientation involves two key abilities: first, the recovery of a spatial reference frame (a cognitive map) that is appropriate to the current environment; and second, the determination of one's heading and location relative to that reference frame. Electrophysiological recording studies, primarily in rodents, have revealed potential correlates of these operations in place, grid, border/boundary, and headdirection cells in the hippocampal formation. Cognitive neuroscience studies, primarily in humans, suggest that the perceptual inputs necessary for these operations are processed by neocortical regions such as the retrosplenial complex, occipital place area and parahippocampal place area, with the retrosplenial complex mediating spatial transformations between the local environment and the recovered spatial reference frame, the occipital place area supporting perception of local boundaries, and the parahippocampal place area processing visual information that is essential for identification of the local spatial context. By combining results across these various literatures, we converge on a unified account of reorientation that bridges the cognitive and neural domains.
Cerebral cortex (New York, N.Y. : 1991), Jun 1, 2016
A salient aspect of objects is their real-world size. Large objects tend to be fixed in the world... more A salient aspect of objects is their real-world size. Large objects tend to be fixed in the world and can act as navigational barriers and landmarks, whereas small objects tend to be moveable and manipulable. Previous work has identified regions of visual cortex that respond differentially to large versus small objects, but the role of size in organizing representations of object categories has not been fully explored. To address this issue, we scanned subjects while they viewed large and small objects drawn from 20 categories, with retinotopic extent equated across size classes. Univariate analyses replicated previous results showing a greater response to large than small objects in scene-responsive regions and the converse effect in the left occipitotemporal sulcus. Critically, multivariate analyses revealed organization-by-size both within and across functional regions, as evidenced by activation patterns that were more similar for object categories of the same size than for obje...
Highlights d TMS to the OPA impairs accuracy of navigation to locations in a virtual arena d This... more Highlights d TMS to the OPA impairs accuracy of navigation to locations in a virtual arena d This impairment is observed for locations defined by distance to a bounding wall d This impairment is not found for locations defined by landmarks or visual markings d Results causally implicate OPA in the perception of environmental boundaries
Proceedings of the National Academy of Sciences of the United States of America, Jan 19, 2015
A lost navigator must identify its current location and recover its facing direction to restore i... more A lost navigator must identify its current location and recover its facing direction to restore its bearings. We tested the idea that these two tasks-place recognition and heading retrieval-might be mediated by distinct cognitive systems in mice. Previous work has shown that numerous species, including young children and rodents, use the geometric shape of local space to regain their sense of direction after disorientation, often ignoring nongeometric cues even when they are informative. Notably, these experiments have almost always been performed in single-chamber environments in which there is no ambiguity about place identity. We examined the navigational behavior of mice in a two-chamber paradigm in which animals had to both recognize the chamber in which they were located (place recognition) and recover their facing direction within that chamber (heading retrieval). In two experiments, we found that mice used nongeometric features for place recognition, but simultaneously faile...
Electrophysiological and behavioral studies in many species have demonstrated mirror-image confus... more Electrophysiological and behavioral studies in many species have demonstrated mirror-image confusion for objects, perhaps because many objects are vertically symmetric (e.g., a cup is the same cup when seen in left or right profile). In contrast, the navigability of a scene changes when it is mirror reversed, and behavioral studies reveal high sensitivity to this change. Thus, we predicted that representations in object-selective cortex will be unaffected by mirror reversals, whereas representations in scene-selective cortex will be sensitive to such reversals. To test this hypothesis, we ran an event-related functional magnetic resonance imaging adaptation experiment in human adults. Consistent with our prediction, we found tolerance to mirror reversals in one object-selective region, the posterior fusiform sulcus, and a strong sensitivity to these reversals in two scene-selective regions, the transverse occipital sulcus and the retrosplenial complex. However, a more posterior object-selective region, the lateral occipital sulcus, showed sensitivity to mirror reversals, suggesting that the sense information that distinguishes mirror images is represented at earlier stages in the object-processing hierarchy. Moreover, one scene-selective region (the parahippocampal place area or PPA) was tolerant to mirror reversals. This last finding challenges the hypothesis that the PPA is involved in navigation and reorientation and suggests instead that scenes, like objects, are processed by distinct pathways guiding recognition and action.
Prior work suggests that our understanding of how things work (''intuitive physics") and how peop... more Prior work suggests that our understanding of how things work (''intuitive physics") and how people work (''intuitive psychology") are distinct domains of human cognition. Here we directly test the dissociability of these two domains by investigating knowledge of intuitive physics and intuitive psychology in adults with Williams syndrome (WS)-a genetic developmental disorder characterized by severely impaired spatial cognition, but relatively spared social cognition. WS adults and mental-age matched (MA) controls completed an intuitive physics task and an intuitive psychology task. If intuitive physics is a distinct domain (from intuitive psychology), then we should observe differential impairment on the physics task for individuals with WS compared to MA controls. Indeed, adults with WS performed significantly worse on the intuitive physics than the intuitive psychology task, relative to controls. These results support the hypothesis that knowledge of the physical world can be disrupted independently from knowledge of the social world.
... 1 McGovern Institute for Brain Research, MIT; 2 McGovern Institute for Brain Research, MIT; 3... more ... 1 McGovern Institute for Brain Research, MIT; 2 McGovern Institute for Brain Research, MIT; 3 McGovern Institute for Brain Research, MIT. Abstract. A recent study (Williams et al., 2008) reported the surprising finding that the region ...
... of Philosophy, Tufts University; 2 McGovern Institute for Brain Research, MIT; 3 Laboratory o... more ... of Philosophy, Tufts University; 2 McGovern Institute for Brain Research, MIT; 3 Laboratory of Brain and Cognition, NIMH, NIH; 4 Schepens Eye Research Institute, Harvard Medical School; 5 McGovern Institute for Brain Research, MIT. Abstract. ...
We explore the environment not only by navigating, but also by viewing our surroundings with our ... more We explore the environment not only by navigating, but also by viewing our surroundings with our eyes. Here we review growing evidence that the mammalian hippocampal formation, extensively studied in the context of navigation and memory, mediates a representation of visual space that is stably anchored to the external world. This visual representation puts the hippocampal formation in a central position to guide viewing behavior and to modulate visual processing beyond the medial temporal lobe (MTL). We suggest that vision and navigation share several key computational challenges that are solved by overlapping and potentially common neural systems, making vision an optimal domain to explore whether and how the MTL supports cognitive operations beyond navigation.
In this issue of Neuron, Kornblith et al. (2013) identify two regions in macaque occipitotemporal... more In this issue of Neuron, Kornblith et al. (2013) identify two regions in macaque occipitotemporal cortex that encode both spatial and nonspatial aspects of visual scenes and might be the homolog of the human parahippocampal place area.
To interact rapidly and effectively with the environment, the mammalian brain needs a representat... more To interact rapidly and effectively with the environment, the mammalian brain needs a representation of the spatial layout of the external world (or a “cognitive map”). A person might need to know where she is standing to find her way home, for instance, or might need to know where she is looking to reach for her out-of-sight keys. For many behaviors, however, simply possessing a map is not enough; in order for a map to be useful in a dynamic world, it must be anchored to stable environmental cues. The goal of the present research is to address this spatial anchoring problem in two different domains: navigation and vision. In the first part of the thesis, which comprises Chapters 1-3, we examine how navigators use perceptual information to re-anchor their cognitive map after becoming lost, a process known as spatial reorientation. Using a novel behavioral paradigm with rodents, in Chapter 2 we show that the cognitive map is reoriented by dissociable inputs for identifying where one ...
To guide spatial behavior, the brain must retrieve memories that are appropriately associated wit... more To guide spatial behavior, the brain must retrieve memories that are appropriately associated with different navigational contexts. Contextual memory might be mediated by cell ensembles in the hippocampal formation that alter their responses to changes in context, processes known as remapping and realignment in the hippocampus and entorhinal cortex, respectively. However, whether remapping and realignment guide context-dependent spatial behavior is unclear. To address this issue, human participants learned object-location associations within two distinct virtual reality environments and subsequently had their memory tested during functional MRI (fMRI) scanning. Entorhinal grid-like representations showed realignment between the two contexts, and coincident changes in fMRI activity patterns consistent with remapping were observed in the hippocampus. Critically, in a third ambiguous context, trial-by-trial remapping and realignment in the hippocampal-entorhinal network predicted conte...
The ability to recover one's bearings when lost is a skill that is fundamental for spatial naviga... more The ability to recover one's bearings when lost is a skill that is fundamental for spatial navigation. We review the cognitive and neural mechanisms that underlie this ability, with the aim of linking together previously disparate findings from animal behavior, human psychology, electrophysiology, and cognitive neuroscience. Behavioral work suggests that reorientation involves two key abilities: first, the recovery of a spatial reference frame (a cognitive map) that is appropriate to the current environment; and second, the determination of one's heading and location relative to that reference frame. Electrophysiological recording studies, primarily in rodents, have revealed potential correlates of these operations in place, grid, border/boundary, and headdirection cells in the hippocampal formation. Cognitive neuroscience studies, primarily in humans, suggest that the perceptual inputs necessary for these operations are processed by neocortical regions such as the retrosplenial complex, occipital place area and parahippocampal place area, with the retrosplenial complex mediating spatial transformations between the local environment and the recovered spatial reference frame, the occipital place area supporting perception of local boundaries, and the parahippocampal place area processing visual information that is essential for identification of the local spatial context. By combining results across these various literatures, we converge on a unified account of reorientation that bridges the cognitive and neural domains.
Cerebral cortex (New York, N.Y. : 1991), Jun 1, 2016
A salient aspect of objects is their real-world size. Large objects tend to be fixed in the world... more A salient aspect of objects is their real-world size. Large objects tend to be fixed in the world and can act as navigational barriers and landmarks, whereas small objects tend to be moveable and manipulable. Previous work has identified regions of visual cortex that respond differentially to large versus small objects, but the role of size in organizing representations of object categories has not been fully explored. To address this issue, we scanned subjects while they viewed large and small objects drawn from 20 categories, with retinotopic extent equated across size classes. Univariate analyses replicated previous results showing a greater response to large than small objects in scene-responsive regions and the converse effect in the left occipitotemporal sulcus. Critically, multivariate analyses revealed organization-by-size both within and across functional regions, as evidenced by activation patterns that were more similar for object categories of the same size than for obje...
Highlights d TMS to the OPA impairs accuracy of navigation to locations in a virtual arena d This... more Highlights d TMS to the OPA impairs accuracy of navigation to locations in a virtual arena d This impairment is observed for locations defined by distance to a bounding wall d This impairment is not found for locations defined by landmarks or visual markings d Results causally implicate OPA in the perception of environmental boundaries
Proceedings of the National Academy of Sciences of the United States of America, Jan 19, 2015
A lost navigator must identify its current location and recover its facing direction to restore i... more A lost navigator must identify its current location and recover its facing direction to restore its bearings. We tested the idea that these two tasks-place recognition and heading retrieval-might be mediated by distinct cognitive systems in mice. Previous work has shown that numerous species, including young children and rodents, use the geometric shape of local space to regain their sense of direction after disorientation, often ignoring nongeometric cues even when they are informative. Notably, these experiments have almost always been performed in single-chamber environments in which there is no ambiguity about place identity. We examined the navigational behavior of mice in a two-chamber paradigm in which animals had to both recognize the chamber in which they were located (place recognition) and recover their facing direction within that chamber (heading retrieval). In two experiments, we found that mice used nongeometric features for place recognition, but simultaneously faile...
Electrophysiological and behavioral studies in many species have demonstrated mirror-image confus... more Electrophysiological and behavioral studies in many species have demonstrated mirror-image confusion for objects, perhaps because many objects are vertically symmetric (e.g., a cup is the same cup when seen in left or right profile). In contrast, the navigability of a scene changes when it is mirror reversed, and behavioral studies reveal high sensitivity to this change. Thus, we predicted that representations in object-selective cortex will be unaffected by mirror reversals, whereas representations in scene-selective cortex will be sensitive to such reversals. To test this hypothesis, we ran an event-related functional magnetic resonance imaging adaptation experiment in human adults. Consistent with our prediction, we found tolerance to mirror reversals in one object-selective region, the posterior fusiform sulcus, and a strong sensitivity to these reversals in two scene-selective regions, the transverse occipital sulcus and the retrosplenial complex. However, a more posterior object-selective region, the lateral occipital sulcus, showed sensitivity to mirror reversals, suggesting that the sense information that distinguishes mirror images is represented at earlier stages in the object-processing hierarchy. Moreover, one scene-selective region (the parahippocampal place area or PPA) was tolerant to mirror reversals. This last finding challenges the hypothesis that the PPA is involved in navigation and reorientation and suggests instead that scenes, like objects, are processed by distinct pathways guiding recognition and action.
Prior work suggests that our understanding of how things work (''intuitive physics") and how peop... more Prior work suggests that our understanding of how things work (''intuitive physics") and how people work (''intuitive psychology") are distinct domains of human cognition. Here we directly test the dissociability of these two domains by investigating knowledge of intuitive physics and intuitive psychology in adults with Williams syndrome (WS)-a genetic developmental disorder characterized by severely impaired spatial cognition, but relatively spared social cognition. WS adults and mental-age matched (MA) controls completed an intuitive physics task and an intuitive psychology task. If intuitive physics is a distinct domain (from intuitive psychology), then we should observe differential impairment on the physics task for individuals with WS compared to MA controls. Indeed, adults with WS performed significantly worse on the intuitive physics than the intuitive psychology task, relative to controls. These results support the hypothesis that knowledge of the physical world can be disrupted independently from knowledge of the social world.
... 1 McGovern Institute for Brain Research, MIT; 2 McGovern Institute for Brain Research, MIT; 3... more ... 1 McGovern Institute for Brain Research, MIT; 2 McGovern Institute for Brain Research, MIT; 3 McGovern Institute for Brain Research, MIT. Abstract. A recent study (Williams et al., 2008) reported the surprising finding that the region ...
... of Philosophy, Tufts University; 2 McGovern Institute for Brain Research, MIT; 3 Laboratory o... more ... of Philosophy, Tufts University; 2 McGovern Institute for Brain Research, MIT; 3 Laboratory of Brain and Cognition, NIMH, NIH; 4 Schepens Eye Research Institute, Harvard Medical School; 5 McGovern Institute for Brain Research, MIT. Abstract. ...
We explore the environment not only by navigating, but also by viewing our surroundings with our ... more We explore the environment not only by navigating, but also by viewing our surroundings with our eyes. Here we review growing evidence that the mammalian hippocampal formation, extensively studied in the context of navigation and memory, mediates a representation of visual space that is stably anchored to the external world. This visual representation puts the hippocampal formation in a central position to guide viewing behavior and to modulate visual processing beyond the medial temporal lobe (MTL). We suggest that vision and navigation share several key computational challenges that are solved by overlapping and potentially common neural systems, making vision an optimal domain to explore whether and how the MTL supports cognitive operations beyond navigation.
In this issue of Neuron, Kornblith et al. (2013) identify two regions in macaque occipitotemporal... more In this issue of Neuron, Kornblith et al. (2013) identify two regions in macaque occipitotemporal cortex that encode both spatial and nonspatial aspects of visual scenes and might be the homolog of the human parahippocampal place area.
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