Grid cells are modulated by local head direction.
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ABSTRACT:
SUBMITTER: Gerlei K
PROVIDER: S-EPMC7445272 | biostudies-literature |
REPOSITORIES: biostudies-literature
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Project description:Prior studies of head direction (HD) cells indicate strong landmark control over the preferred firing direction of these cells, with few studies exhibiting shifts away from local reference frames over time. We recorded spiking activity of grid and HD cells in the medial entorhinal cortex of rats, testing correlations of local environmental cues with the spatial tuning curves of these cells' firing fields as animals performed continuous spatial alternation on a T-maze that shared the boundaries of an open-field arena. The environment was rotated into configurations the animal had either seen or not seen in the past recording week. Tuning curves of both cell types demonstrated commensurate shifts of tuning with T-maze rotations during less recent rotations, more so than recent rotations. This strongly suggests that animals are shifting their reference frame away from the local environmental cues over time, learning to use a different reference frame more likely reliant on distal or idiothetic cues. In addition, grid fields demonstrated varying levels of "fragmentation" on the T-maze. The propensity for fragmentation does not depend on grid spacing and grid score, nor animal trajectory, indicating the cognitive treatment of environmental subcompartments is likely driven by task demands.
| S-EPMC4014184 | biostudies-literature
Project description:The discovery of speed-modulated grid, head direction, and conjunctive grid x head direction cells in the medial entorhinal cortex has led to the hypothesis that path integration, the updating of one's spatial representation based on movement, may be carried out within this region. This hypothesis has been formalized by many computational models, including a class known as attractor network models. While many of these models propose specific mechanisms by which path integration might occur, predictions of these specific mechanisms have not been tested. Here I derive and test a key prediction of one attractor network path integration mechanism. Specifically, I first demonstrate that this mechanism predicts a periodic distribution of conjunctive cell preferred directions in order to minimize drift. Next, I test whether conjunctive cell preferred directions are in fact periodically organized. Results indicate that conjunctive cells are preferentially tuned to increments of 36°, consistent with drift minimization in this path integration mechanism. By contrast, no periodicity was observed in the preferred directions of either pure grid or pure head direction cells. These results provide the first neural evidence of a nonuniform structure in the directional preferences of any head direction representation found in the brain.
| S-EPMC4803195 | biostudies-literature
Project description:The brain has an extraordinary ability to create an internal spatial map of the external world [1]. This map-like representation of environmental surroundings is encoded through specific types of neurons, located within the hippocampus and entorhinal cortex, which exhibit spatially tuned firing patterns [2, 3]. In addition to encoding space, these neurons are believed to be related to contextual information and memory [4-7]. One class of such cells is the grid cells, which are located within the entorhinal cortex, presubiculum, and parasubiculum [3, 8]. Grid cell firing forms a hexagonal array of firing fields, a pattern that is largely thought to reflect the operation of intrinsic self-motion-related computations [9-12]. If this is the case, then fields should be relatively uniform in size, number of spikes, and peak firing rate. However, it has been suggested that this is not in fact the case [3, 13]. The possibility exists that local spatial information also influences grid cells, which-if true-would greatly change the way in which grid cells are thought to contribute to place coding. Accordingly, we asked how discriminable the individual fields of a given grid cell are by looking at the distribution of field firing rates and reproducibility of this distribution across trials. Grid fields were less uniform in intensity than expected, and the pattern of strong and weak fields was spatially stable and recurred across trials. The distribution remained unchanged even after arena rescaling, but not after remapping. This suggests that additional local information is being overlaid onto the global hexagonal pattern of grid cells.
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Project description:Navigation depends on multiple neural systems that encode the moment-to-moment changes in an animal's direction and location in space. These include head direction (HD) cells representing the orientation of the head and grid cells that fire at multiple locations, forming a repeating hexagonal grid pattern. Computational models hypothesize that generation of the grid cell signal relies upon HD information that ascends to the hippocampal network via the anterior thalamic nuclei (ATN). We inactivated or lesioned the ATN and subsequently recorded single units in the entorhinal cortex and parasubiculum. ATN manipulation significantly disrupted grid and HD cell characteristics while sparing theta rhythmicity in these regions. These results indicate that the HD signal via the ATN is necessary for the generation and function of grid cell activity.
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Project description:Head direction (HD) cells fire when the animal faces that cell's preferred firing direction (PFD) in the horizontal plane. The PFD response when the animal is oriented outside the earth-horizontal plane could result from cells representing direction in the plane of locomotion or as a three-dimensional (3D), global-referenced direction anchored to gravity. To investigate these possibilities, anterodorsal thalamic HD cells were recorded from restrained rats while they were passively positioned in various 3D orientations. Cell responses were unaffected by pitch or roll up to ~90° from the horizontal plane. Firing was disrupted once the animal was oriented >90° away from the horizontal plane and during inversion. When rolling the animal around the earth-vertical axis, cells were active when the animal's ventral surface faced the cell's PFD. However, with the rat rolled 90° in an ear-down orientation, pitching the rat and rotating it around the vertical axis did not produce directionally tuned responses. Complex movements involving combinations of yaw-roll, but usually not yaw-pitch, resulted in reduced directional tuning even at the final upright orientation when the rat had full visual view of its environment and was pointing in the cell's PFD. Directional firing was restored when the rat's head was moved back-and-forth. There was limited evidence indicating that cells contained conjunctive firing with pitch or roll positions. These findings suggest that the brain's representation of directional heading is derived primarily from horizontal canal information and that the HD signal is a 3D gravity-referenced signal anchored to a direction in the horizontal plane. NEW & NOTEWORTHY This study monitored head direction cell responses from rats in three dimensions using a series of manipulations that involved yaw, pitch, roll, or a combination of these rotations. Results showed that head direction responses are consistent with the use of two reference frames simultaneously: one defined by the surrounding environment using primarily visual landmarks and a second defined by the earth's gravity vector.
| S-EPMC6383655 | biostudies-literature
Project description:Discrete populations of brain cells signal heading direction, rather like a compass. These 'head direction' cells are largely confined to a closely-connected network of sites. We describe, for the first time, a population of head direction cells in nucleus reuniens of the thalamus in the freely-moving rat. This novel subcortical head direction signal potentially modulates the hippocampal CA fields directly and, thus, informs spatial processing and memory.
| S-EPMC4115655 | biostudies-literature
Project description:Animals exhibit remarkable navigation abilities as if they have an internal compass. Head direction (HD) cells encoding the animal's heading azimuth are found in the brain of several animal species; the HD cell signals are dependent on the vestibular nuclei, where magnetic responsive cells are present in birds. However, it is difficult to determine whether HD cell signals drive the compass orientation in animals, as they do not necessarily rely on the magnetic compass under all circumstances. Recording of HD cell activities from the medial pallium of shearwater chicks (Calonectris leucomelas) just before their first migration, during which they strongly rely on compass orientation, revealed that shearwater HD cells prefer a north orientation. The preference remained stable regardless of geolocations and environmental cues, suggesting the existence of a magnetic compass regulated by internally generated HD signals. Our findings provide insight into the integration of the direction and magnetoreception senses.
| S-EPMC8816328 | biostudies-literature
Project description:Head direction (HD) cells form a fundamental component in the brain's spatial navigation system and are intricately linked to spatial memory and cognition. Although HD cells have been shown to act as an internal neuronal compass in various cortical and subcortical regions, the neural substrate of HD cells is incompletely understood. It is reported that HD cells in the somatosensory cortex comprise regular-spiking (RS, putative excitatory) and fast-spiking (FS, putative inhibitory) neurons. Surprisingly, somatosensory FS HD cells fire in bursts and display much sharper head-directionality than RS HD cells. These FS HD cells are nonconjunctive, rarely theta rhythmic, sparsely connected and enriched in layer 5. Moreover, sharply tuned FS HD cells, in contrast with RS HD cells, maintain stable tuning in darkness; FS HD cells' coexistence with RS HD cells and angular head velocity (AHV) cells in a layer-specific fashion through the somatosensory cortex presents a previously unreported configuration of spatial representation in the neocortex. Together, these findings challenge the notion that FS interneurons are weakly tuned to sensory stimuli, and offer a local circuit organization relevant to the generation and transmission of HD signaling in the brain.
| S-EPMC9109065 | biostudies-literature
Project description:People usually see things using frontal viewing, and avoid lateral viewing (or eccentric gaze) where the directions of the head and eyes are largely different. Lateral viewing interferes with attentive visual search performance, probably because the head is directed away from the target and/or because the head and eyes are misaligned. In this study, we examined which of these factors is the primary one for interference by conducting a visual identification experiment where a target was presented in the peripheral visual field. The critical manipulation was the participants' head direction and fixation position: the head was directed to the fixation location, the target position, or the opposite side of the fixation. The performance was highest when the head was directed to the target position even when there was misalignment of the head and eye, suggesting that visual perception can be influenced by both head direction and fixation position.
| S-EPMC4412404 | biostudies-literature
Project description:Mammalian navigation is thought to depend on an internal map of space consisting of functionally specialized cells in the hippocampus and the surrounding parahippocampal cortices. Basic properties of this map are present when rat pups explore the world outside of their nest for the first time, around postnatal day 16-18 (P16-P18). One of the first functions to be expressed in navigating animals is the directional tuning of the head direction cells. To determine whether head direction tuning is expressed at even earlier ages, before the start of exploration, and to establish whether vision is necessary for the development of directional tuning, we recorded neural activity in pre- and parasubiculum, or medial entorhinal cortex, from P11 onward, 3-4 days before the eyelids unseal. Head direction cells were present from the first day of recording. Firing rates were lower than in adults, and preferred firing directions were less stable, drifting within trials and changing completely between trials. Yet the cells drifted coherently, i.e., relative firing directions were maintained from one trial to the next. Directional tuning stabilized shortly after eye opening. The data point to a hardwired attractor network for representation of head direction in which directional tuning develops before vision and visual input serves primarily to anchor firing direction to the external world.
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