Evidence for allocentric boundary and goal direction information in the human entorhinal cortex and subiculum

Shine, Jonathan P.; Valdés-Herrera, José P.; Tempelmann, Claus; Wolbers, Thomas

doi:10.1038/s41467-019-11802-9

Cited by 41 publications

(30 citation statements)

References 66 publications

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“…Thus, particularly for rodents, it is unclear how the distance tuning of receptive fields several body-lengths from the animal (up to 60 cm 12 ) might be established. While the visual systems of primates and rodents differ substantially, recent findings provide evidence for (allocentric) boundary coding in primates 89,90 . Furthermore, parietal and frontal eye field neglect reported in rats 91 (BOX 1) might reflect homologous functions.…”

Section: [H2] Sensory Input Underlying Egocentric Codingmentioning

confidence: 99%

Neuronal vector coding in spatial cognition

2020

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Several types of neurons involved in spatial navigation and memory encode the distance and direction (that is, the vector) between an agent and items in its environment. Such vectorial information provides a powerful basis for spatial cognition by representing the geometric relationships between the self and the external world. Here, we review the explicit encoding of vectorial information by neurons in and around the hippocampal formation, far from the sensory periphery. The parahippocampal, retrosplenial and parietal cortices, as well as the hippocampal formation and striatum, provide a plethora of examples of vector coding at the single neuron level. We provide a functional taxonomy of cells with vectorial receptive fields as reported in experiments and proposed in theoretical work. The responses of these neurons may provide the fundamental neural basis for the (bottom-up) representation of environmental layout and (top-down) memoryguided generation of visuo-spatial imagery and navigational planning. [H1] Introduction Place cells fire whenever an animal traverses a specific location in an environment (the spatial receptive field [G] of that neuron, also known as its 'place field', FIG. 1a). Since the discovery of place cells in the rat hippocampus by O'Keefe and Dostrovsky 1 , researchers have uncovered a multitude of additional spatially-selective cell types in rodents: that is, neurons whose receptive fields reference some aspect of an organism's location, state of motion, pose or its relationship to environmental features (such as boundaries, landmarks and other objects). The spatial receptive fields of some of these cells correspond to vectors, indicating the distance and direction in space (relative to the animal's current location) within which the presence of an environmental feature will drive the neuron to fire. Such 'vectorial codes' for space have received comparatively less attention than the coding performed by place cells or other well-known spatially-selective cell types, such as grid cells [G] 2 (FIG. 1a) and head direction cells [G] 3,4. Vectorial codes for space are expressed by boundary vector cells 5,6 , border cells 7,8 , landmark vector cells 9 and object vector cells 10 in allocentric (that is, world-centered) coordinates. Just like place fields, the receptive fields of these vector-coding cells do not reflect the orientation of the animal but do rotate together with the prominent environmental features that control head direction cell firing 11. Egocentric counterparts of some of these cells-in which the direction of receptive fields are referenced relative to the facing direction of the agent-have also been found 12-15 , as well as cells that exhibit head direction-modulated boundary responses 16,17 .

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Section: [H2] Sensory Input Underlying Egocentric Codingmentioning

confidence: 99%

Neuronal vector coding in spatial cognition

2020

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“…Based on this rotation, the mouse dorsal SUB is generally believed to be homologous to the human posterior SUB and mouse ventral SUB is homologous to anterior human SUB. Functional evidence supports this view as the mouse dorsal SUB and human posterior SUB are involved in visuospatial navigation 10,[17][18][19] . In contrast, the mouse ventral SUB and human anterior SUB are related to limbic emotional processing and social behaviors 12,20,21 .…”

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confidence: 74%

Homologous laminar organization of the mouse and human subiculum

Bienkowski

Sepehrband

Kurniawan

et al. 2021

Sci Rep

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The subiculum is the major output component of the hippocampal formation and one of the major brain structures most affected by Alzheimer’s disease. Our previous work revealed a hidden laminar architecture within the mouse subiculum. However, the rotation of the hippocampal longitudinal axis across species makes it unclear how the laminar organization is represented in human subiculum. Using in situ hybridization data from the Allen Human Brain Atlas, we demonstrate that the human subiculum also contains complementary laminar gene expression patterns similar to the mouse. In addition, we provide evidence that the molecular domain boundaries in human subiculum correspond to microstructural differences observed in high resolution MRI and fiber density imaging. Finally, we show both similarities and differences in the gene expression profile of subiculum pyramidal cells within homologous lamina. Overall, we present a new 3D model of the anatomical organization of human subiculum and its evolution from the mouse.

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“…It is of interest to compare the present model with a recent model (Bicanski & Burgess, ) centered on the retrosplenial cortex. This previous model is directed primarily toward spatial memory and imagery; does not deal with how eye movements affect spatial vision which is a major part of what is implemented in the primate dorsal visual system and in areas such as LIP, VIP, and area 7a together with mechanisms for reaching into space (with eye movements and reaching into space poorly developed and understood in rodents, and no set of highly developed dorsal stream cortical areas in rodents); and relies (Bicanski & Burgess, ) on boundary‐vector cells found in rodents (with a consistent human fMRI study (Shine et al, )) and not known by neuronal recording evidence to be present in primates. The previous model (Bicanski & Burgess, ) also utilizes object‐vector cells found in rodents (Hoydal, Skytoen, Andersson, Moser, & Moser, ).…”

Section: Discussionmentioning

confidence: 99%

“…In previous work, the importance of coordinate transforms utilizing allocentric and egocentric representations for spatial navigation in primates including humans has been described though without a formal neuronal network theory and model (Ekstrom, Huffman, & Starrett, ). A previous model for coordinate transforms between egocentric and allocentric coordinates holds that this is performed in the retrosplenial cortex, is described in the context of a model of spatial memory, imagery, and so forth, and depends on neurons such as allocentric boundary‐vector cells found in rodents with consistent human fMRI evidence (Shine, Valdes‐Herrera, Tempelmann, & Wolbers, ) but not shown at the neuronal level in primates, and object‐vector cells, and does not model the series of stages of the highly developed primate dorsal visual system leading to the parietal cortex with coordinate transforms starting with retinal coordinates (Bicanski & Burgess, ; Burgess & Hartley, ; Byrne, Becker, & Burgess, ; see Section 5). Furthermore, the homology between the well‐defined primate retrosplenial cortex of primates (Kobayashi & Amaral, ) and what is described as retrosplenial cortex in rodents is not clear, and there may be no posterior cingulate cortex in rodents (Vogt, ).…”

Section: Introductionmentioning

confidence: 99%

Spatial coordinate transforms linking the allocentric hippocampal and egocentric parietal primate brain systems for memory, action in space, and navigation

Rolls

2019

Hippocampus

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A theory and model of spatial coordinate transforms in the dorsal visual system through the parietal cortex that enable an interface via posterior cingulate and related retrosplenial cortex to allocentric spatial representations in the primate hippocampus is described. First, a new approach to coordinate transform learning in the brain is proposed, in which the traditional gain modulation is complemented by temporal trace rule competitive network learning. It is shown in a computational model that the new approach works much more precisely than gain modulation alone, by enabling neurons to represent the different combinations of signal and gain modulator more accurately. This understanding may have application to many brain areas where coordinate transforms are learned. Second, a set of coordinate transforms is proposed for the dorsal visual system/parietal areas that enables a representation to be formed in allocentric spatial view coordinates. The input stimulus is merely a stimulus at a given position in retinal space, and the gain modulation signals needed are eye position, head direction, and place, all of which are present in the primate brain. Neurons that encode the bearing to a landmark are involved in the coordinate transforms. Part of the importance here is that the coordinates of the allocentric view produced in this model are the same as those of spatial view cells that respond to allocentric view recorded in the primate hippocampus and parahippocampal cortex. The result is that information from the dorsal visual system can be used to update the spatial input to the hippocampus in the appropriate allocentric coordinate frame, including providing for idiothetic update to allow for self‐motion. It is further shown how hippocampal spatial view cells could be useful for the transform from hippocampal allocentric coordinates to egocentric coordinates useful for actions in space and for navigation.

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Evidence for allocentric boundary and goal direction information in the human entorhinal cortex and subiculum

Cited by 41 publications

References 66 publications

Neuronal vector coding in spatial cognition

Neuronal vector coding in spatial cognition

Homologous laminar organization of the mouse and human subiculum

Spatial coordinate transforms linking the allocentric hippocampal and egocentric parietal primate brain systems for memory, action in space, and navigation

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