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Spatial Navigation: Head Direction Cells Are Anchored by Gravity

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Spatial Navigation: Head Direction Cells Are Anchored by Gravity View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by Elsevier - Publisher Connector Dispatch R841 Spatial Navigation: Head Direction swimming from several starting points to a platform hidden in a constant Cells Are Anchored by Gravity location. The slow learning and limited performance in the clinging task contrasts markedly with the Thalamic neurons that signal an animal’s direction of heading are crucial for rapid learning and highly flexible spatial navigation. Both directional coding and flexible use of spatial memory performance in the water maze, are upended, however, when a rat has to find its way while upside down. where rats escape directly from four starting points after only a few trials. Matthew Shapiro cells have been recorded in several The tenfold difference in learning rates interconnected structures that receive suggests that different mechanisms Adaptive behavior depends on vestibular inputs, including mammilary guide learning in the two navigation predicting accurate relationships nuclei, the anterior and lateral dorsal tasks. between percepts, actions, and nuclei of the thalamus, and the Spatial behavior can be guided by outcomes. Some of these relationships retrosplenial and entorhinal cortices. several mechanisms, including taxons generalize across niches, and neural Head direction cells fire at relatively and cognitive mapping [5]. Taxons refer mechanisms for computing predictions low base rates until the rat’s head is to directed responses with respect to a among them are conserved. pointing within about 60 of the cell’s single stimulus, such as approaching a Oculomotor systems predict how preferred angle, when the firing rate poster on a wall. Such cue approach retinal images change with eye or can increase to 60 spikes per second. strategies are impaired by lesions of head movements, and violating these The preferred heading angle of a given the dorsolateral striatum that do not predictions impairs cognition in head direction cell is acquired as impair cognitive mapping [6]. surprising ways. I remember wearing animals explore an environment, is Navigation by cognitive mapping prism lenses that reversed expected stable in a constant environment, and combines spatial representations, and actual horizontal visual movement changes if prominent visual cues are defined by relationships among several and being utterly disoriented when I altered. stimuli, with path integration signals tried to walk across a room. Analogous Heading signals are crucial for that indicate the direction and distance systems use spatial computations to ‘path integration’, the ability to track of movement. Rats demonstrate guide animals as they navigate about changing location by combining the cognitive mapping by finding familiar the environment, combining distance, distance and angles of self-generated spatial goals despite the removal of heading, and location signals to movement. Vestibular signals allow one or more visual cues, or after being track movement across the surface head direction cell signals to persist in placed in an unfamiliar start location of the world. A paper published the dark, but they ‘drift’ over time until a [5]. Both types of behavioral flexibility recently in Current Biology by Gibson familiar landmark is encountered that are typical in water maze tests, et al. [1] reports evidence that these corrects or resets them. Head direction suggesting that rats use relationships two-dimensional navigation systems cell activity is weakened or abolished among distal spatial cues to navigate are tethered by gravity. by lesions of the vestibular apparatus, to the hidden platform. Biological mechanisms for orienting especially the semi-circular canals; Gibson et al. [1] assessed the in gravity begin in the otolithic organs inactivation of the otoliths has less strategy used by the inverted rats by of the inner ear, where hair cells effect, which could imply that gravity placing the animals in an unfamiliar transduce linear acceleration. The plays a relatively unimportant role starting point at the center of the vestibular nuclei relay angular velocity in heading signals. The new work apparatus [1]. The rats headed in signals to other brainstem, thalamic, of Gibson et al. [1] overturns that random directions and showed no and cerebellar nuclei that convey implication, however, by showing that sign of learning after several trials, acceleration information to the spinal both head direction cell activity in the consistent with their inability to learn cord and the cerebral cortex. The anterodorsal thalamic nucleus and to escape from more than two starting dorsal tegmental and lateral navigation are severely disrupted when points. The inability to generalize in a mammillary nuclei integrate vestibular animals walk upside down. highly familiar environment, together with other perceptual and motor Gibson et al. [1] trained rats to cling with slow learning in the familiar start signals across levels of processing. to a circular wire mesh ‘ceiling’ and, task, suggest that the rats did not use Gravity, equivalent to a constant while upside-down, walk from starting a spatial mapping strategy, but rather acceleration, activates a subset of points at the edge of the apparatus to used a taxon strategy to approach these hair cells even when the head one of four potential escape hatches specific distal cues. Indeed, when a is still [2]. near the middle of each quadrant. The curtain blocked the distal cues from Head direction cells integrate correct escape hatch let the rat climb view, the upside down rats made vestibular signals with other percepts above the mesh and stand up. After random headings even from the to compute horizontal orientation. more than 100 training trials, the rats familiar starting points, as though Head direction cells act like neuronal learned to move directly to the escape the rats no longer had a sense of Geiger counters with receptive fields hatch from each of two different direction. Indeed, head direction that span whole environments and starting points, but they could not learn signals were lost when the rats were have one trigger feature — the animal’s four. The task is operationally similar upside down. heading angle. First discovered in the to the Morris water maze [4], in which Previous work showed that head rat presubiculum [3], head direction rats learn to escape from the water by direction cell coding was maintained Current Biology Vol 23 No 18 R842 when rats walked along a horizontal place fields [10], and hippocampal problems learning new facts and maze arm and then climbed up a lesions reduce the stability of head remembering recent events [18]. vertical wall [7], suggesting that direction cells [14]. Cognitive mapping theory proposes heading signals might be independent Computational models of navigation that spatial computations define the of gravity. Gibson et al. [1] recorded propose that recurrent activation of fundamental operations of memory anterodorsal thalamic nucleus cells as place, distance, and heading encodes systems, and that these other types rats explored a cylinder on the floor and retrieves spatial paths [5,13,15,16]. of memory rely on these. Relational of the testing room before and after The models suggest that moving memory theory proposes that spatial they performed the inverted through an environment activates memory exemplifies a general memory navigation task [1]. They found that interconnected head direction, grid, system that associates stimuli that the anterodorsal thalamic nucleus cells and place units so that specific overlap in time into events and had sharply-tuned directional firing trajectories are represented by sequential episodes [19]. The correlates when the rats walked on the direction–distance–place code computational differences between floor, but the signals were disrupted sequences and stored by synaptic spatial navigation and other forms when the same cells were recorded plasticity. Familiar trajectories could be of flexible memory remain unclear. when rats were upside down. The retrieved as place-direction-distance Consider the example of rats trained animals performed the inverted task sequences; for example, when placed to distinguish between two olfactory reliably and followed consistent in a familiar start location in a water sequences that begin and end trajectories from the two familiar maze, a rat’s active hippocampal with distinct odors but contain an starting points, but the peak firing rates cells would signal that location and overlapping set of smells in the of the head direction cells declined, activate head direction cells predicting middle [19]. background firing increased, and the platform direction. The head Compare that to another example directional tuning curves were noisy direction cells would activate grid in which rats are trained to distinguish and inconsistent. During the center cells that signal distance, and together between two spatial paths that begin probe tests, the directional tuning these would activate the next and end in different places but have an declined further. Head direction cell hippocampal spatial representation on overlapping middle section. Both tasks activity returned to normal when the the way to the platform, and so on. are impaired by hippocampal damage, animals walked upright in the cylinder Heading angles thereby predict future but to what extent do they require the afterwards, and the strong tuning locations by activating spatial same computations? If non-spatial curves
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