Head-direction coding in the hippocampal formation of birds

Birds strongly rely on spatial memory and navigation. However, it is unknown how space is represented in the avian brain. Here we used tetrodes to record neurons from the hippocampal formation (HPF) of Japanese quails – a migratory ground-dwelling species – while the quails roamed a 1×1-meter arena (>2,100 neurons from 21 birds). Whereas spatially-modulated cells (place-cells, border-cells, etc.) were generally not encountered, the firing-rate of 12% of the neurons was unimodally and significantly modulated by the head-azimuth – i.e. these were head-direction cells (HD cells, n=260). Typically, HD cells were maximally active at one preferred-direction and minimally at the opposite null-direction, with preferred-directions spanning all 360°. The HD tuning was relatively broad (mean= 130°), independent of the animal’s position and speed, and was stable during the recording-session. These findings support the existence of an allocentric head-direction representation in the quail HPF, and provide the first demonstration of head-direction cells in birds.

Download Full-text

A spatial map in the somatosensory cortex

10.1101/473090 ◽

2018 ◽

Cited By ~ 6

Author(s):

Xiaoyang Long ◽

Sheng-Jia Zhang

Keyword(s):

Somatosensory Cortex ◽

Spatial Representation ◽

Hippocampal Formation ◽

Place Cells ◽

Border Cells ◽

Head Direction ◽

Head Direction Cells ◽

Sensory Inputs ◽

Boundary Vector ◽

The Brain

AbstractSpatially selective firing in the forms of place cells, grid cells, boundary vector/border cells and head direction cells are the basic building blocks of a canonical spatial navigation system centered on the hippocampal-entorhinal complex. While head direction cells can be found throughout the brain, spatial tuning outside the hippocampal formation are often non-specific or conjunctive to other representations such as a reward. Although the precise mechanism of spatially selective activities is not understood, various studies show sensory inputs (particularly vision) heavily modulate spatial representation in the hippocampal-entorhinal circuit. To better understand the contribution from other sensory inputs in shaping spatial representation in the brain, we recorded from the primary somatosensory cortex in foraging rats. To our surprise, we were able to identify the full complement of spatial activity patterns reported in the hippocampal-entorhinal network, namely, place cells, head direction cells, boundary vector/border cells, grid cells and conjunctive cells. These newly identified somatosensory spatial cell types form a spatial map outside the hippocampal formation and support the hypothesis that location information is necessary for body representation in the somatosensory cortex, and may be analogous to spatially tuned representations in the motor cortex relating to the movement of body parts. Our findings are transformative in our understanding of how spatial information is used and utilized in the brain, as well as functional operations of the somatosensory cortex in the context of rehabilitation with brain-machine interfaces.

Download Full-text

Functional connectivity of the entorhinal–hippocampal space circuit

Philosophical Transactions of the Royal Society B Biological Sciences ◽

10.1098/rstb.2012.0516 ◽

2014 ◽

Vol 369 (1635) ◽

pp. 20120516 ◽

Cited By ~ 23

Author(s):

Sheng-Jia Zhang ◽

Jing Ye ◽

Jonathan J. Couey ◽

Menno Witter ◽

Edvard I. Moser ◽

...

Keyword(s):

Entorhinal Cortex ◽

Cell Types ◽

Place Cells ◽

Projection Neurons ◽

Border Cells ◽

Head Direction ◽

Grid Cells ◽

Head Direction Cells ◽

Dynamic Interactions ◽

Cell Groups

The mammalian space circuit is known to contain several functionally specialized cell types, such as place cells in the hippocampus and grid cells, head-direction cells and border cells in the medial entorhinal cortex (MEC). The interaction between the entorhinal and hippocampal spatial representations is poorly understood, however. We have developed an optogenetic strategy to identify functionally defined cell types in the MEC that project directly to the hippocampus. By expressing channelrhodopsin-2 (ChR2) selectively in the hippocampus-projecting subset of entorhinal projection neurons, we were able to use light-evoked discharge as an instrument to determine whether specific entorhinal cell groups—such as grid cells, border cells and head-direction cells—have direct hippocampal projections. Photoinduced firing was observed at fixed minimal latencies in all functional cell categories, with grid cells as the most abundant hippocampus-projecting spatial cell type. We discuss how photoexcitation experiments can be used to distinguish the subset of hippocampus-projecting entorhinal neurons from neurons that are activated indirectly through the network. The functional breadth of entorhinal input implied by this analysis opens up the potential for rich dynamic interactions between place cells in the hippocampus and different functional cell types in the entorhinal cortex (EC).

Download Full-text

A novel somatosensory spatial navigation system outside the hippocampal formation

Cell Research ◽

10.1038/s41422-020-00448-8 ◽

2021 ◽

Cited By ~ 3

Author(s):

Xiaoyang Long ◽

Sheng-Jia Zhang

Keyword(s):

Somatosensory Cortex ◽

Spatial Representation ◽

Hippocampal Formation ◽

Spatial Navigation ◽

Place Cells ◽

Head Direction ◽

Head Direction Cells ◽

Sensory Inputs ◽

Boundary Vector ◽

The Brain

AbstractSpatially selective firing of place cells, grid cells, boundary vector/border cells and head direction cells constitutes the basic building blocks of a canonical spatial navigation system centered on the hippocampal-entorhinal complex. While head direction cells can be found throughout the brain, spatial tuning outside the hippocampal formation is often non-specific or conjunctive to other representations such as a reward. Although the precise mechanism of spatially selective firing activity is not understood, various studies show sensory inputs, particularly vision, heavily modulate spatial representation in the hippocampal-entorhinal circuit. To better understand the contribution of other sensory inputs in shaping spatial representation in the brain, we performed recording from the primary somatosensory cortex in foraging rats. To our surprise, we were able to detect the full complement of spatially selective firing patterns similar to that reported in the hippocampal-entorhinal network, namely, place cells, head direction cells, boundary vector/border cells, grid cells and conjunctive cells, in the somatosensory cortex. These newly identified somatosensory spatial cells form a spatial map outside the hippocampal formation and support the hypothesis that location information modulates body representation in the somatosensory cortex. Our findings provide transformative insights into our understanding of how spatial information is processed and integrated in the brain, as well as functional operations of the somatosensory cortex in the context of rehabilitation with brain-machine interfaces.

Download Full-text

An Oscillatory Network Model of Head Direction, Spatially Periodic Cells and Place Cells Using Locomotor Inputs

10.1101/080267 ◽

2016 ◽

Author(s):

Karthik Soman ◽

Vignesh Muralidharan ◽

V. Srinivasa Chakravarthy

Keyword(s):

Path Integration ◽

Place Cells ◽

Border Cells ◽

Head Direction ◽

Grid Cells ◽

Head Direction Cells ◽

Modeling Approach ◽

Spatially Periodic ◽

Locomotor Rhythms ◽

Oscillatory Network

AbstractWe propose a computational modeling approach that explains the formation of a range of spatial cells like head direction cells, grid cells, border cells and place cells which are believed to play a pivotal role in the spatial navigation of an animal. Most existing models insert special symmetry conditions in the models in order to obtain such symmetries in the outcome; our models do not require such symmetry assumptions. Our modeling approach is embodied in two models: a simple one (Model #1) and a more detailed version (Model #2). In Model #1, velocity input is presented to a layer of Head Direction cells, with no special topology requirements, the outputs of which are presented to a layer of Path Integration neurons. A variety of spatially periodic responses resembling grid cells, are obtained using the Principal Components of Path Integration layer. In Model #2, the input consists of the locomotor rhythms from the four legs of a virtual animal. These rhythms are integrated into the phases of a layer of oscillatory neurons, whose outputs drive a layer of Head Direction cells. The Head Direction cells in turn drive a layer of Path Integration neurons, which in turn project to two successive layers of Lateral Anti Hebbian Networks (LAHN). Cells in the first LAHN resemble grid cells (with both hexagonal and square gridness), and border cells. Cells in the second LAHN exhibit place cell behaviour and a new cell type known as corner cell. Both grid cells and place cells exhibit phase precession in 1D and 2D spaces. The models outline the neural hierarchy necessary to obtain the complete range of spatial cell responses found in the hippocampal system.

Download Full-text

Hippocampal Place-Cell Firing During Movement in Three-Dimensional Space

Journal of Neurophysiology ◽

10.1152/jn.2001.85.1.105 ◽

2001 ◽

Vol 85 (1) ◽

pp. 105-116 ◽

Cited By ~ 44

Author(s):

James J. Knierim ◽

Bruce L. McNaughton

Keyword(s):

Hippocampal Neurons ◽

Horizontal Plane ◽

Three Dimensional ◽

Place Cell ◽

Place Cells ◽

Limbic Cortex ◽

Head Direction ◽

Head Direction Cells ◽

Recording Apparatus ◽

Place Fields

“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.

Download Full-text