scholarly journals Three-dimensional tuning of head direction cells in rats

2019 ◽  
Vol 121 (1) ◽  
pp. 4-37 ◽  
Author(s):  
Michael E. Shinder ◽  
Jeffrey S. Taube

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.

2007 ◽  
Vol 97 (4) ◽  
pp. 2958-2964 ◽  
Author(s):  
Stefan Glasauer ◽  
Thomas Brandt

After whole body rotations around an earth-vertical axis in darkness, subjects can indicate their orientation in space with respect to their initial orientation reasonably well. This is possible because the brain is able to mathematically integrate self-velocity information provided by the vestibular system to obtain self-orientation, a process called path integration. For rotations around multiple axes, however, computations are more demanding to accurately update self-orientation with respect to space. In such a case, simple integration is no longer sufficient because of the noncommutativity of rotations. We investigated whether such updating is possible after three-dimensional whole body rotations and whether the noncommutativity of three-dimensional rotations is taken into account. The ability of ten subjects to indicate their spatial orientation in the earth-horizontal plane was tested after different rotational paths from upright to supine positions. Initial and final orientations of the subjects were the same in all cases, but the paths taken were different, and so were the angular velocities sensed by the vestibular system. The results show that seven of the ten subjects could consistently indicate their final orientation within the earth-horizontal plane. Thus perceived final orientation was independent of the path taken, i.e., the noncommutativity of rotations was taken into account.


2018 ◽  
Vol 119 (1) ◽  
pp. 192-208 ◽  
Author(s):  
Hector J. I. Page ◽  
Jonathan J. Wilson ◽  
Kate J. Jeffery

In the mammalian brain, allocentric (Earth-referenced) head direction, called azimuth, is encoded by head direction (HD) cells, which fire according to the facing direction of the animal’s head. On a horizontal surface, rotations of the head around the dorsoventral (D-V) axis, called yaw, correspond to changes in azimuth and elicit appropriate updating of the HD “compass” signal to enable large-scale navigation. However, if the animal moves through three-dimensional (3D) space then there is no longer a simple relationship between yaw rotations and azimuth changes, and so processing of 3D rotations is needed. Construction of a global 3D compass would require complex integration of 3D rotations, and also a large neuronal population, most neurons of which would be silent most of the time since animals rarely sample all available 3D orientations. We propose that, instead, the HD system treats the 3D space as a set of interrelated 2D surfaces. It could do this by updating activity according to both yaw rotations around the D-V axis and rotations of the D-V axis around the gravity-defined vertical axis. We present preliminary data to suggest that this rule operates when rats move between walls of opposing orientations. This dual-axis rule, which we show is straightforward to implement using the classic one-dimensional “attractor” architecture, allows consistent representation of azimuth even in volumetric space and thus may be a general feature of mammalian directional computations even for animals that swim or fly.NEW & NOTEWORTHY Maintaining a sense of direction is complicated when moving in three-dimensional (3D) space. Head direction cells, which update the direction sense based on head rotations, may accommodate 3D movement by processing both rotations of the head around the axis of the animal’s body and rotations of the head/body around gravity. With modeling we show that this dual-axis rule works in principle, and we present preliminary data to support its operation in rats.


2001 ◽  
Vol 85 (1) ◽  
pp. 105-116 ◽  
Author(s):  
James J. Knierim ◽  
Bruce L. McNaughton

“Place” cells of the rat hippocampus are coupled to “head direction” cells of the thalamus and limbic cortex. Head direction cells are sensitive to head direction in the horizontal plane only, which leads to the question of whether place cells similarly encode locations in the horizontal plane only, ignoring the z axis, or whether they encode locations in three dimensions. This question was addressed by recording from ensembles of CA1 pyramidal cells while rats traversed a rectangular track that could be tilted and rotated to different three-dimensional orientations. Cells were analyzed to determine whether their firing was bound to the external, three-dimensional cues of the environment, to the two-dimensional rectangular surface, or to some combination of these cues. Tilting the track 45° generally provoked a partial remapping of the rectangular surface in that some cells maintained their place fields, whereas other cells either gained new place fields, lost existing fields, or changed their firing locations arbitrarily. When the tilted track was rotated relative to the distal landmarks, most place fields remapped, but a number of cells maintained the same place field relative to the x-y coordinate frame of the laboratory, ignoring the z axis. No more cells were bound to the local reference frame of the recording apparatus than would be predicted by chance. The partial remapping demonstrated that the place cell system was sensitive to the three-dimensional manipulations of the recording apparatus. Nonetheless the results were not consistent with an explicit three-dimensional tuning of individual hippocampal neurons nor were they consistent with a model in which different sets of cells are tightly coupled to different sets of environmental cues. The results are most consistent with the statement that hippocampal neurons can change their “tuning functions” in arbitrary ways when features of the sensory input or behavioral context are altered. Understanding the rules that govern the remapping phenomenon holds promise for deciphering the neural circuitry underlying hippocampal function.


2016 ◽  
Author(s):  
Jonathan Wilson ◽  
Hector Page ◽  
Kate Jeffery

In the mammalian brain, allocentric (Earth-referenced) heading direction, called azimuth, is encoded by head direction (HD) cells, which fire according to the facing direction of the rat's head. If the animal is on a horizontal surface then egocentric (self-referenced) rotations of the head around the dorso-ventral axis, called yaw, correspond to changes in azimuth, and elicit appropriate updating of the HD signal. However, if the surface is sloping steeply then yaw rotations no longer map linearly to changes in azimuth. The brain could solve this problem simply by always firing according to direction on the local (sloping) surface instead; however, if the animal moves between surfaces having different compass orientations then errors would accumulate in the subsequent azimuth signal. These errors could be avoided if the HD system instead combines two updating rules: yaw rotations around the D-V axis and rotations of the D-V axis around the gravity-defined vertical axis. We show here that when rats move between vertical walls of different orientations then HD cells indeed rotate their activity by an amount corresponding to the amount of vertical-axis rotation. With modelling, we then show how this reference-frame rotation, which may be driven by inputs from the vestibular nuclei or vestibulocerebellum, allows animals to maintain a simple yaw-based updating rule while on a given plane, but also to avoid accumulation of heading errors when moving between planes.


1999 ◽  
Vol 81 (1) ◽  
pp. 267-276 ◽  
Author(s):  
Douglas R. W. Wylie ◽  
Barrie J. Frost

Wylie, Douglas R. W. and Barrie J. Frost. Responses of Neurons in the nucleus of the basal optic root to translational and rotational flowfields. J. Neurophysiol. 81: 267–276, 1999. The nucleus of the basal optic root (nBOR) receives direct input from the contralateral retina and is the first step in a pathway dedicated to the analysis of optic flowfields resulting from self-motion. Previous studies have shown that most nBOR neurons exhibit direction selectivity in response to large-field stimuli moving in the contralateral hemifield, but a subpopulation of nBOR neurons has binocular receptive fields. In this study, the activity of binocular nBOR neurons was recorded in anesthetized pigeons in response to panoramic translational and rotational optic flow. Translational optic flow was produced by the “translator” projector described in the companion paper, and rotational optic flow was produced by a “planetarium projector” described by Wylie and Frost. The axis of rotation or translation could be positioned to any orientation in three-dimensional space. We recorded from 37 cells, most of which exhibited a strong contralateral dominance. Most of these cells were located in the caudal and dorsal aspects of the nBOR complex and many were localized to the subnucleus nBOR dorsalis. Other units were located outside the boundaries of the nBOR complex in the adjacent area ventralis of Tsai or mesencephalic reticular formation. Six cells responded best to rotational flowfields, whereas 31 responded best to translational flowfields. Of the rotation cells, three preferred rotation about the vertical axis and three preferred horizontal axes. Of the translation cells, 3 responded best to a flowfield simulating downward translation of the bird along a vertical axis, whereas the remaining 28 responded best to flowfields resulting from translation along axes in the horizontal plane. Seventeen of these cells preferred a flowfield resulting from the animal translating backward along an axis oriented ∼45° to the midline, but the best axes of the remaining eleven cells were distributed throughout the horizontal plane with no definitive clustering. These data are compared with the responses of vestibulocerebellar Purkinje cells.


2003 ◽  
Vol 3 ◽  
pp. 1286-1293 ◽  
Author(s):  
Soren Ventegodt ◽  
Niels Jorgen Andersen ◽  
Joav Merrick

When we acknowledge our purpose as the essence of our self, when we take all our power into use in an effortless way, and when we fully accept our own nature — including sex and sexuality, our purpose of life takes the form of a unique talent. Using this talent gives the experience of happiness. A person in his natural state of being uses his core talent in a conscious, joyful, and effortless way, contributing to the world the best he or she has to offer. Full expression of self happens when a person, in full acceptance of body and life, with whole-hearted intension, uses all his personal powers to realize his core talent and all associated talents, to contribute to his beloved and to the world. Thus, self-actualisation is a result of a person fully expressing and realizing his core talent.The theory of talent states that a core talent can be expressed optimally when a human being takes possession of a three-dimensional space with the axis of purpose, power and gender, as we have a threefold need: 1-Acknowledging our core talent (our purpose of life) and intending it 2-Understanding our potential powers and manifesting them 3-Accepting our human form including our sex and expressing itThe first dimension is spiritual, the next dimension is mental, emotional and physical, and the third dimension is bodily and sexual. We manifest our talents in a giving movement from the bottom of our soul trough our biological nature onto the subject and object of the outer world. These three dimensions can be drawn as three axes, one saggital axis called purpose or love or me-you, one vertical axis called power or consciousness (light) or heaven-earth, and one horizontal axis called gender or joy or male-female. The three core dimensions of human existence are considered of equal importance for expression of our life purpose, life mission, or core talent. Each of the dimensions is connected to special needs. When these needs are not fulfilled, we suffer and if this suffering becomes unbearable we deny the dimension or a part of is. This is why the dimensions of purpose, power and gender become suppressed from our consciousness.


2013 ◽  
Vol 36 (5) ◽  
pp. 523-543 ◽  
Author(s):  
Kathryn J. Jeffery ◽  
Aleksandar Jovalekic ◽  
Madeleine Verriotis ◽  
Robin Hayman

AbstractThe study of spatial cognition has provided considerable insight into how animals (including humans) navigate on the horizontal plane. However, the real world is three-dimensional, having a complex topography including both horizontal and vertical features, which presents additional challenges for representation and navigation. The present article reviews the emerging behavioral and neurobiological literature on spatial cognition in non-horizontal environments. We suggest that three-dimensional spaces are represented in a quasi-planar fashion, with space in the plane of locomotion being computed separately and represented differently from space in the orthogonal axis – a representational structure we have termed “bicoded.” We argue that the mammalian spatial representation in surface-travelling animals comprises a mosaic of these locally planar fragments, rather than a fully integrated volumetric map. More generally, this may be true even for species that can move freely in all three dimensions, such as birds and fish. We outline the evidence supporting this view, together with the adaptive advantages of such a scheme.


2019 ◽  
Author(s):  
Dora E Angelaki ◽  
J Ng ◽  
AM Abrego ◽  
HX Cham ◽  
JD Dickman ◽  
...  

SummaryHead direction cells in the mammalian limbic system are thought to function as an allocentric neuronal compass. Although traditional views hold that the compass of ground-dwelling species is planar, we show that head-direction cells in the rodent thalamus, retrosplenial cortex and cingulum fiber bundle are tuned to conjunctive combinations of azimuth, pitch or roll, similarly to presubicular cells in flying bats. Pitch and roll orientation tuning is ubiquitous, anchored to gravity, and independent of visual landmarks. When head tilts, azimuth tuning is affixed to the head-horizontal plane, but also uses gravity to remain anchored to the terrestrial allocentric world. These findings suggest that gravity defines all three degrees of freedom of the allocentric orientation compass, and only the azimuth component can flexibly remap to local cues in different environments. Collectively, these results demonstrate that a three-dimensional, gravity-based, neural compass is likely a ubiquitous property of mammalian species, including ground-dwelling animals.


1993 ◽  
Vol 69 (2) ◽  
pp. 303-317 ◽  
Author(s):  
H. S. Tan ◽  
J. van der Steen ◽  
J. I. Simpson ◽  
H. Collewijn

1. Three-dimensional rotations of both eyes were measured in alert rabbits during optokinetic stimulation about axes lying in the horizontal plane or about an earth-vertical axis, with either one or both eyes viewing the stimulus. Optokinetic stimulus speed was 2 degrees /s, either continuous or alternating in polarity (triangular stimulus). In addition to the gains of the responses, the orientations of the response axes relative to the stimulus axes were determined. 2. In comparison to the response to constant-speed optokinetic stimulation about the vertical axis, the response to constant-speed optokinetic stimulation about horizontal axes was characterized by the lack of a speed buildup. In many cases, slow phase tracking was good as long as the eye was within the central oculomotor range but deteriorated when eye deviation became more eccentric and fast phases failed to be generated. These features suggest that the optokinetic reflex about horizontal axes functions as a position-control system, rather than as a velocity-control system. 3. Binocular optokinetic stimulation at constant speed (2 degrees/s) about the roll axis (0 degrees azimuth horizontal axis) elicited disconjugate responses. Although the gain of the response was not significantly different in the two eyes (0.38 for downward and 0.44 for upward stimulation), the response axes of the two eyes differed by as much as 51 degrees. 4. Monocular, horizontal axis optokinetic stimulation at constant speed elicited responses that were grossly dissociated between the two eyes. The magnitude of the responses was anisotropic in that it varied with the azimuthal orientation of the stimulus axis; the maximum gain for each eye (0.41 for the seeing and 0.33 for the covered eye) was at 135 degrees azimuth for each eye. The axis orientation and direction (sense of rotation) of the optokinetic stimulus eliciting the maximal response for each eye coincided with the optic flow normally associated with the maximal excitation of the corresponding ipsilateral anterior canal. 5. Binocular, triangular optokinetic stimulation with small excursions (+/- 10 degrees), which avoided the saturation problems of constant-speed stimulation, elicited adequate responses without systematic directional asymmetries. Gain was approximately 0.9 for all stimulus axis orientations in the horizontal plane. 6. During monocular stimulation with triangular stimuli, the response of the seeing eye showed a gain of approximately 0.5 for all orientations of the stimulus axis. In contrast, the covered eye showed anisotropic responses, with a maximum gain of approximately 0.5 during stimulation of the seeing eye about its 45 degree axis.(ABSTRACT TRUNCATED AT 400 WORDS)


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