How the Internally Organized Direction Sense Is Used to Navigate.
ABSTRACT: Head-direction cells preferentially discharge when the head points in a particular azimuthal direction, are hypothesized to collectively function as a single neural system for a unitary direction sense, and are believed to be essential for navigating extra-personal space by functioning like a compass. We tested these ideas by recording medial entorhinal cortex (MEC) head-direction cells while rats navigated on a familiar, continuously rotating disk that dissociates the environment into two spatial frames: one stationary and one rotating. Head-direction cells degraded directional tuning referenced to either of the externally referenced spatial frames, but firing rates, sub-second cell-pair action potential discharge relationships, and internally referenced directional tuning were preserved. MEC head-direction cell ensemble discharge collectively generates a subjective, internally referenced unitary representation of direction that, unlike a compass, is inconsistently registered to external landmarks during navigation. These findings indicate that MEC-based directional information is subjectively anchored, potentially providing for navigation without a stable externally anchored direction sense.
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.
Project description:Neurons coding for head-direction are crucial for spatial navigation. Here we explored the cellular basis of head-direction coding in the rat dorsal presubiculum (PreS). We found that layer2 is composed of two principal cell populations (calbindin-positive and calbindin-negative neurons) which targeted the contralateral PreS and retrosplenial cortex, respectively. Layer3 pyramidal neurons projected to the medial entorhinal cortex (MEC). By juxtacellularly recording PreS neurons in awake rats during passive-rotation, we found that head-direction responses were preferentially contributed by layer3 pyramidal cells, whose long-range axons branched within layer3 of the MEC. In contrast, layer2 neurons displayed distinct spike-shapes, were not modulated by head-direction but rhythmically-entrained by theta-oscillations. Fast-spiking interneurons showed only weak directionality and theta-rhythmicity, but were significantly modulated by angular velocity. Our data thus indicate that PreS neurons differentially contribute to head-direction coding, and point to a cell-type- and layer-specific routing of directional and non-directional information to downstream cortical targets.
Project description:The head-direction (HD) system functions as a compass, with member neurons robustly increasing their firing rates when the animal's head points in a specific direction. HD neurons may be driven by peripheral sensors or, as computational models postulate, internally generated (attractor) mechanisms. We addressed the contributions of stimulus-driven and internally generated activity by recording ensembles of HD neurons in the antero-dorsal thalamic nucleus and the post-subiculum of mice by comparing their activity in various brain states. The temporal correlation structure of HD neurons was preserved during sleep, characterized by a 60°-wide correlated neuronal firing (activity packet), both within and across these two brain structures. During rapid eye movement sleep, the spontaneous drift of the activity packet was similar to that observed during waking and accelerated tenfold during slow-wave sleep. These findings demonstrate that peripheral inputs impinge on an internally organized network, which provides amplification and enhanced precision of the HD signal.
Project description:The rat limbic system contains head direction (HD) cells that fire according to heading in the horizontal plane, and these cells are thought to provide animals with an internal compass. Previous work has found that HD cell tuning correlates with behavior on navigational tasks, but a direct, causal link between HD cells and navigation has not been demonstrated. Here, we show that pathway-specific optogenetic inhibition of the nucleus prepositus caused HD cells to become directionally unstable under dark conditions without affecting the animals' locomotion. Then, using the same technique, we found that this decoupling of the HD signal in the absence of visual cues caused the animals to make directional homing errors and that the magnitude and direction of these errors were in a range that corresponded to the degree of instability observed in the HD signal. These results provide evidence that the HD signal plays a causal role as a neural compass in navigation.
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.
Project description:Gravity sensing provides a robust verticality signal for three-dimensional navigation. Head direction cells in the mammalian limbic system implement an allocentric neuronal compass. Here we show that head-direction cells in the rodent thalamus, retrosplenial cortex and cingulum fiber bundle are tuned to conjunctive combinations of azimuth and tilt, i.e. pitch or roll. Pitch and roll orientation tuning is anchored to gravity and independent of visual landmarks. When the head tilts, azimuth tuning is affixed to the head-horizontal plane, but also uses gravity to remain anchored to the allocentric bearings in the earth-horizontal plane. Collectively, these results demonstrate that a three-dimensional, gravity-based, neural compass is likely a ubiquitous property of mammalian species, including ground-dwelling animals.
Project description:Mammals navigate by means of a metric cognitive map. Insects, most notably bees and ants, are also impressive navigators. The question whether they, too, have a metric cognitive map is important to cognitive science and neuroscience. Experimentally captured and displaced bees often depart from the release site in the compass direction they were bent on before their capture, even though this no longer heads them toward their goal. When they discover their error, however, the bees set off more or less directly toward their goal. This ability to orient toward a goal from an arbitrary point in the familiar environment is evidence that they have an integrated metric map of the experienced environment. We report a test of an alternative hypothesis, which is that all the bees have in memory is a collection of snapshots that enable them to recognize different landmarks and, associated with each such snapshot, a sun-compass-referenced home vector derived from dead reckoning done before and after previous visits to the landmark. We show that a large shift in the sun-compass rapidly induced by general anesthesia does not alter the accuracy or speed of the homeward-oriented flight made after the bees discover the error in their initial postrelease flight. This result rules out the sun-referenced home-vector hypothesis, further strengthening the now extensive evidence for a metric cognitive map in bees.
Project description:Spatial navigation requires landmark coding from two perspectives, relying on viewpoint-invariant and self-referenced representations. The brain encodes information within each reference frame but their interactions and functional dependency remains unclear. Here we investigate the relationship between neurons in the rat's retrosplenial cortex (RSC) and entorhinal cortex (MEC) that increase firing near boundaries of space. Border cells in RSC specifically encode walls, but not objects, and are sensitive to the animal's direction to nearby borders. These egocentric representations are generated independent of visual or whisker sensation but are affected by inputs from MEC that contains allocentric spatial cells. Pharmaco- and optogenetic inhibition of MEC led to a disruption of border coding in RSC, but not vice versa, indicating allocentric-to-egocentric transformation. Finally, RSC border cells fire prospective to the animal's next motion, unlike those in MEC, revealing the MEC-RSC pathway as an extended border coding circuit that implements coordinate transformation to guide navigation behavior.
Project description:Navigation by mammals is believed to rely on a network of neurons in the hippocampal formation, which includes the hippocampus, the medial entorhinal cortex (MEC), and additional nearby regions. Neurons in these regions represent spatial information by tuning to the position, orientation, and speed of the animal in the form of head direction cells, speed cells, grid cells, border cells, and unclassified spatially modulated cells. While the properties of single cells are well studied, little is known about the functional structure of the network in the MEC. Here, we use a generalized linear model to study the network of spatially modulated cells in the MEC. We found connectivity patterns between all spatially encoding cells and not only grid cells. In addition, the neurons' past activity contributed to the overall activity patterns. Finally, position-modulated cells and head direction cells differed in the dependence of the activity on the history. Our results indicate that MEC neurons form a local interacting network to support spatial information representations and suggest an explanation for their complex temporal properties.
Project description:Magnetoreception has been demonstrated in all five vertebrate classes. In rodents, nest building experiments have shown the use of magnetic cues by two families of molerats, Siberian hamsters and C57BL/6 mice. However, assays widely used to study rodent spatial cognition (e.g. water maze, radial arm maze) have failed to provide evidence for the use of magnetic cues. Here we show that C57BL/6 mice can learn the magnetic direction of a submerged platform in a 4-armed (plus) water maze. Naïve mice were given two brief training trials. In each trial, a mouse was confined to one arm of the maze with the submerged platform at the outer end in a predetermined alignment relative to magnetic north. Between trials, the training arm and magnetic field were rotated by 180(°) so that the mouse had to swim in the same magnetic direction to reach the submerged platform. The directional preference of each mouse was tested once in one of four magnetic field alignments by releasing it at the center of the maze with access to all four arms. Equal numbers of responses were obtained from mice tested in the four symmetrical magnetic field alignments. Findings show that two training trials are sufficient for mice to learn the magnetic direction of the submerged platform in a plus water maze. The success of these experiments may be explained by: (1) absence of alternative directional cues (2), rotation of magnetic field alignment, and (3) electromagnetic shielding to minimize radio frequency interference that has been shown to interfere with magnetic compass orientation of birds. These findings confirm that mice have a well-developed magnetic compass, and give further impetus to the question of whether epigeic rodents (e.g., mice and rats) have a photoreceptor-based magnetic compass similar to that found in amphibians and migratory birds.