Dissociating two aspects of human 3D spatial perception by studying fighter pilots.

Human perception of 3D space has been investigated extensively, but there are conflicting reports regarding its distortions. A possible solution to these discrepancies is that 3D perception is in fact comprised of two different processes-perception of traveled space, and perception of surrounding space. Here we tested these two aspects on the same subjects, for the first time. To differentiate these two aspects and investigate whether they emerge from different processes, we asked whether these two aspects are affected differently by the individual's experience of 3D locomotion. Using an immersive high-grade flight-simulator with realistic virtual-reality, we compared these two aspects of 3D perception in fighter pilots-individuals highly experienced in 3D locomotion-and in control subjects. We found that the two aspects of 3D perception were affected differently by 3D locomotion experience: the perception of 3D traveled space was plastic and experience-dependent, differing dramatically between pilots and controls, while the perception of surrounding space was rigid and unaffected by experience. This dissociation suggests that these two aspects of 3D spatial perception emerge from two distinct processes.

Are grid cells used for navigation? On local metrics, subjective spaces, and black holes.

The symmetric, lattice-like spatial pattern of grid-cell activity is thought to provide a neuronal global metric for space. This view is compatible with grid cells recorded in empty boxes but inconsistent with data from more naturalistic settings. We review evidence arguing against the global-metric notion, including the distortion and disintegration of the grid pattern in complex and three-dimensional environments. We argue that deviations from lattice symmetry are key for understanding grid-cell function. We propose three possible functions for grid cells, which treat real-world grid distortions as a feature rather than a bug. First, grid cells may constitute a local metric for proximal space rather than a global metric for all space. Second, grid cells could form a metric for subjective action-relevant space rather than physical space. Third, distortions may represent salient locations. Finally, we discuss mechanisms that can underlie these functions. These ideas may transform our thinking about grid cells.

Organization of projections from the entorhinal cortex to the hippocampal formation of the Egyptian fruit bat Rousettus aegyptiacus.

The hippocampal formation and entorhinal cortex are crucially involved in learning and memory as well as in spatial navigation. The conservation of these structures across the entire mammalian lineage demonstrates their importance. Information on a diverse set of spatially tuned neurons has become available, but we only have a rudimentary understanding of how anatomical network structure affects functional tuning. Bats are the only order of mammals that have evolved true flight, and with this specialization comes the need to navigate and behave in a three dimensional (3D) environment. Spatial tuning of cells in the entorhinal-hippocampal network of bats has been studied for some time, but whether the reported tuning in 3D is associated with changes in the entorhinal-hippocampal network is not known. Here we investigated the entorhinal-hippocampal projections in the Egyptian fruit bat (Rousettus aegyptiacus), by injecting chemical anterograde tracers in the entorhinal cortex. Detailed analyses of the terminations of these projections in the hippocampus showed that both the medial and lateral entorhinal cortex sent projections to the molecular layer of all subfields of the hippocampal formation. Our analyses showed that the terminal distributions of entorhinal fibers in the hippocampal formation of Egyptian fruit bats-including the proximo-distal and longitudinal topography and the layer-specificity-are similar to what has been described in other mammalian species such as rodents and primates. The major difference in entorhinal-hippocampal projections that was described to date between rodents and primates is in the terminal distribution of the DG projection. We found that bats have entorhinal-DG projections that seem more like those in primates than in rodents. It is likely that the latter projection in bats is specialized to the behavioral needs of this species, including 3D flight and long-distance navigation.

Spatial coding in the hippocampus and hyperpallium of flying owls.

The elucidation of spatial coding in the hippocampus requires exploring diverse animal species. While robust place-cells are found in the mammalian hippocampus, much less is known about spatial coding in the hippocampus of birds. Here we used a wireless-electrophysiology system to record single neurons in the hippocampus and other two dorsal pallial structures from freely flying barn owls (Tyto alba), a central-place nocturnal predator species with excellent navigational abilities. The owl's 3D position was monitored while it flew between perches. We found place cells-neurons that fired when the owl flew through a spatially restricted region in at least one direction-as well as neurons that encoded the direction of flight, and neurons that represented the owl's perching position between flights. Many neurons encoded combinations of position, direction, and perching. Spatial coding was maintained stable and invariant to lighting conditions. Place cells were observed in owls performing two different types of flying tasks, highlighting the generality of the result. Place coding was found in the anterior hippocampus and in the posterior part of the hyperpallium apicale, and to a lesser extent in the visual Wulst. The finding of place-cells in flying owls suggests commonalities in spatial coding across mammals and birds.

Contextual and pure time coding for self and other in the hippocampus.

Navigation and episodic memory depend critically on representing temporal sequences. Hippocampal 'time cells' form temporal sequences, but it is unknown whether they represent context-dependent experience or time per se. Here we report on time cells in bat hippocampal area CA1, which, surprisingly, formed two distinct populations. One population of time cells generated different temporal sequences when the bat hung at different locations, thus conjunctively encoding spatial context and time-'contextual time cells'. A second population exhibited similar preferred times across different spatial contexts, thus purely encoding elapsed time. When examining neural responses after the landing moment of another bat, in a social imitation task, we found time cells that encoded temporal sequences aligned to the other's landing. We propose that these diverse time codes may support the perception of interval timing, episodic memory and temporal coordination between self and others.

Natural switches in behaviour rapidly modulate hippocampal coding.

Throughout their daily lives, animals and humans often switch between different behaviours. However, neuroscience research typically studies the brain while the animal is performing one behavioural task at a time, and little is known about how brain circuits represent switches between different behaviours. Here we tested this question using an ethological setting: two bats flew together in a long 135 m tunnel, and switched between navigation when flying alone (solo) and collision avoidance as they flew past each other (cross-over). Bats increased their echolocation click rate before each cross-over, indicating attention to the other bat1-9. Hippocampal CA1 neurons represented the bat's own position when flying alone (place coding10-14). Notably, during cross-overs, neurons switched rapidly to jointly represent the interbat distance by self-position. This neuronal switch was very fast-as fast as 100 ms-which could be revealed owing to the very rapid natural behavioural switch. The neuronal switch correlated with the attention signal, as indexed by echolocation. Interestingly, the different place fields of the same neuron often exhibited very different tuning to interbat distance, creating a complex non-separable coding of position by distance. Theoretical analysis showed that this complex representation yields more efficient coding. Overall, our results suggest that during dynamic natural behaviour, hippocampal neurons can rapidly switch their core computation to represent the relevant behavioural variables, supporting behavioural flexibility.

Locally ordered representation of 3D space in the entorhinal cortex.

As animals navigate on a two-dimensional surface, neurons in the medial entorhinal cortex (MEC) known as grid cells are activated when the animal passes through multiple locations (firing fields) arranged in a hexagonal lattice that tiles the locomotion surface1. However, although our world is three-dimensional, it is unclear how the MEC represents 3D space2. Here we recorded from MEC cells in freely flying bats and identified several classes of spatial neurons, including 3D border cells, 3D head-direction cells, and neurons with multiple 3D firing fields. Many of these multifield neurons were 3D grid cells, whose neighbouring fields were separated by a characteristic distance-forming a local order-but lacked any global lattice arrangement of the fields. Thus, whereas 2D grid cells form a global lattice-characterized by both local and global order-3D grid cells exhibited only local order, creating a locally ordered metric for space. We modelled grid cells as emerging from pairwise interactions between fields, which yielded a hexagonal lattice in 2D and local order in 3D, thereby describing both 2D and 3D grid cells using one unifying model. Together, these data and model illuminate the fundamental differences and similarities between neural codes for 3D and 2D space in the mammalian brain.

Multiscale representation of very large environments in the hippocampus of flying bats.

Hippocampal place cells encode the animal's location. Place cells were traditionally studied in small environments, and nothing is known about large ethologically relevant spatial scales. We wirelessly recorded from hippocampal dorsal CA1 neurons of wild-born bats flying in a long tunnel (200 meters). The size of place fields ranged from 0.6 to 32 meters. Individual place cells exhibited multiple fields and a multiscale representation: Place fields of the same neuron differed up to 20-fold in size. This multiscale coding was observed from the first day of exposure to the environment, and also in laboratory-born bats that never experienced large environments. Theoretical decoding analysis showed that the multiscale code allows representation of very large environments with much higher precision than that of other codes. Together, by increasing the spatial scale, we discovered a neural code that is radically different from classical place codes.

Directional tuning in the hippocampal formation of birds.

Birds strongly rely on spatial memory and navigation. Therefore, it is of utmost interest to reveal how space is represented in the avian brain. Here we used tetrodes to record neurons from the hippocampal formation of Japanese quails-a ground-dwelling species-while the quails roamed in an open-field arena. Whereas spatially modulated cells (place cells, grid cells, border cells) were generally not encountered, the firing rate of about 12% of the neurons was unimodally and significantly modulated by the head azimuth-i.e., these were head-direction cells (HD cells). Typically, HD cells were maximally active at one preferred direction and minimally at the opposite null direction, with preferred directions spanning all 360° across the population. The preferred direction was independent of the animal's position and speed and was stable during the recording session. The HD tuning was broader compared to that of HD cells in rodents, and most cells had non-zero baseline firing in all directions. However, similar to findings in rodents, the HD tuning usually rotated with the rotation of a salient visual cue in the arena. Thus, these findings support the existence of an allocentric HD representation in the quail hippocampal formation and provide the first demonstration of HD cells in birds.

Nonoscillatory Phase Coding and Synchronization in the Bat Hippocampal Formation.

Hippocampal theta oscillations were proposed to be important for multiple functions, including memory and temporal coding of position. However, previous findings from bats have questioned these proposals by reporting absence of theta rhythmicity in bat hippocampal formation. Does this mean that temporal coding is unique to rodent hippocampus and does not generalize to other species? Here, we report that, surprisingly, bat hippocampal neurons do exhibit temporal coding similar to rodents, albeit without any continuous oscillations at the 1-20 Hz range. Bat neurons exhibited very strong locking to the non-rhythmic fluctuations of the field potential, such that neurons were synchronized together despite the absence of oscillations. Further, some neurons exhibited "phase precession" and phase coding of the bat's position-with spike phases shifting earlier as the animal moved through the place field. This demonstrates an unexpected type of neural coding in the mammalian brain-nonoscillatory phase coding-and highlights the importance of synchrony and temporal coding for hippocampal function across species.

Optimal dynamic coding by mixed-dimensionality neurons in the head-direction system of bats.

Ethologically relevant stimuli are often multidimensional. In many brain systems, neurons with "pure" tuning to one stimulus dimension are found along with "conjunctive" neurons that encode several dimensions, forming an apparently redundant representation. Here we show using theoretical analysis that a mixed-dimensionality code can efficiently represent a stimulus in different behavioral regimes: encoding by conjunctive cells is more robust when the stimulus changes quickly, whereas on long timescales pure cells represent the stimulus more efficiently with fewer neurons. We tested our predictions experimentally in the bat head-direction system and found that many head-direction cells switched their tuning dynamically from pure to conjunctive representation as a function of angular velocity-confirming our theoretical prediction. More broadly, our results suggest that optimal dimensionality depends on population size and on the time available for decoding-which might explain why mixed-dimensionality representations are common in sensory, motor, and higher cognitive systems across species.

Social place-cells in the bat hippocampus.

Social animals have to know the spatial positions of conspecifics. However, it is unknown how the position of others is represented in the brain. We designed a spatial observational-learning task, in which an observer bat mimicked a demonstrator bat while we recorded hippocampal dorsal-CA1 neurons from the observer bat. A neuronal subpopulation represented the position of the other bat, in allocentric coordinates. About half of these "social place-cells" represented also the observer's own position-that is, were place cells. The representation of the demonstrator bat did not reflect self-movement or trajectory planning by the observer. Some neurons represented also the position of inanimate moving objects; however, their representation differed from the representation of the demonstrator bat. This suggests a role for hippocampal CA1 neurons in social-spatial cognition.

Vectorial representation of spatial goals in the hippocampus of bats.

To navigate, animals need to represent not only their own position and orientation, but also the location of their goal. Neural representations of an animal's own position and orientation have been extensively studied. However, it is unknown how navigational goals are encoded in the brain. We recorded from hippocampal CA1 neurons of bats flying in complex trajectories toward a spatial goal. We discovered a subpopulation of neurons with angular tuning to the goal direction. Many of these neurons were tuned to an occluded goal, suggesting that goal-direction representation is memory-based. We also found cells that encoded the distance to the goal, often in conjunction with goal direction. The goal-direction and goal-distance signals make up a vectorial representation of spatial goals, suggesting a previously unrecognized neuronal mechanism for goal-directed navigation.

The Representation of Prediction Error in Auditory Cortex.

To survive, organisms must extract information from the past that is relevant for their future. How this process is expressed at the neural level remains unclear. We address this problem by developing a novel approach from first principles. We show here how to generate low-complexity representations of the past that produce optimal predictions of future events. We then illustrate this framework by studying the coding of 'oddball' sequences in auditory cortex. We find that for many neurons in primary auditory cortex, trial-by-trial fluctuations of neuronal responses correlate with the theoretical prediction error calculated from the short-term past of the stimulation sequence, under constraints on the complexity of the representation of this past sequence. In some neurons, the effect of prediction error accounted for more than 50% of response variability. Reliable predictions often depended on a representation of the sequence of the last ten or more stimuli, although the representation kept only few details of that sequence.

3-D Maps and Compasses in the Brain.

The world has a complex, three-dimensional (3-D) spatial structure, but until recently the neural representation of space was studied primarily in planar horizontal environments. Here we review the emerging literature on allocentric spatial representations in 3-D and discuss the relations between 3-D spatial perception and the underlying neural codes. We suggest that the statistics of movements through space determine the topology and the dimensionality of the neural representation, across species and different behavioral modes. We argue that hippocampal place-cell maps are metric in all three dimensions, and might be composed of 2-D and 3-D fragments that are stitched together into a global 3-D metric representation via the 3-D head-direction cells. Finally, we propose that the hippocampal formation might implement a neural analogue of a Kalman filter, a standard engineering algorithm used for 3-D navigation.

Hippocampal global remapping for different sensory modalities in flying bats.

Hippocampal place cells encode the animal's spatial position. However, it is unknown how different long-range sensory systems affect spatial representations. Here we alternated usage of vision and echolocation in Egyptian fruit bats while recording from single neurons in hippocampal areas CA1 and subiculum. Bats flew back and forth along a linear flight track, employing echolocation in darkness or vision in light. Hippocampal representations remapped between vision and echolocation via two kinds of remapping: subiculum neurons turned on or off, while CA1 neurons shifted their place fields. Interneurons also exhibited strong remapping. Finally, hippocampal place fields were sharper under vision than echolocation, matching the superior sensory resolution of vision over echolocation. Simulating several theoretical models of place-cells suggested that combining sensory information and path integration best explains the experimental sharpening data. In summary, here we show sensory-based global remapping in a mammal, suggesting that the hippocampus does not contain an abstract spatial map but rather a 'cognitive atlas', with multiple maps for different sensory modalities.

Whisking, Sniffing, and the Hippocampal θ-Rhythm: A Tale of Two Oscillators.

The hippocampus has unique access to neuronal activity across all of the neocortex. Yet an unanswered question is how the transfer of information between these structures is gated. One hypothesis involves temporal-locking of activity in the neocortex with that in the hippocampus. New data from the Matthew E. Diamond laboratory shows that the rhythmic neuronal activity that accompanies vibrissa-based sensation, in rats, transiently locks to ongoing hippocampal θ-rhythmic activity during the sensory-gathering epoch of a discrimination task. This result complements past studies on the locking of sniffing and the θ-rhythm as well as the relation of sniffing and whisking. An overarching possibility is that the preBötzinger inspiration oscillator, which paces whisking, can selectively lock with the θ-rhythm to traffic sensorimotor information between the rat's neocortex and hippocampus.

Spatial cognition in bats and rats: from sensory acquisition to multiscale maps and navigation.

Spatial orientation and navigation rely on the acquisition of several types of sensory information. This information is then transformed into a neural code for space in the hippocampal formation through the activity of place cells, grid cells and head-direction cells. These spatial representations, in turn, are thought to guide long-range navigation. But how the representations encoded by these different cell types are integrated in the brain to form a neural 'map and compass' is largely unknown. Here, we discuss this problem in the context of spatial navigation by bats and rats. We review the experimental findings and theoretical models that provide insight into the mechanisms that link sensory systems to spatial representations and to large-scale natural navigation.

A sensory-motor control model of animal flight explains why bats fly differently in light versus dark.

Animal flight requires fine motor control. However, it is unknown how flying animals rapidly transform noisy sensory information into adequate motor commands. Here we developed a sensorimotor control model that explains vertebrate flight guidance with high fidelity. This simple model accurately reconstructed complex trajectories of bats flying in the dark. The model implies that in order to apply appropriate motor commands, bats have to estimate not only the angle-to-target, as was previously assumed, but also the angular velocity ("proportional-derivative" controller). Next, we conducted experiments in which bats flew in light conditions. When using vision, bats altered their movements, reducing the flight curvature. This change was explained by the model via reduction in sensory noise under vision versus pure echolocation. These results imply a surprising link between sensory noise and movement dynamics. We propose that this sensory-motor link is fundamental to motion control in rapidly moving animals under different sensory conditions, on land, sea, or air.

Three-dimensional head-direction coding in the bat brain.

Navigation requires a sense of direction ('compass'), which in mammals is thought to be provided by head-direction cells, neurons that discharge when the animal's head points to a specific azimuth. However, it remains unclear whether a three-dimensional (3D) compass exists in the brain. Here we conducted neural recordings in bats, mammals well-adapted to 3D spatial behaviours, and found head-direction cells tuned to azimuth, pitch or roll, or to conjunctive combinations of 3D angles, in both crawling and flying bats. Head-direction cells were organized along a functional-anatomical gradient in the presubiculum, transitioning from 2D to 3D representations. In inverted bats, the azimuth-tuning of neurons shifted by 180°, suggesting that 3D head direction is represented in azimuth × pitch toroidal coordinates. Consistent with our toroidal model, pitch-cell tuning was unimodal, circular, and continuous within the available 360° of pitch. Taken together, these results demonstrate a 3D head-direction mechanism in mammals, which could support navigation in 3D space.