Three Components of Spatial Orientation• Head direction cells • Location - Place cells - Hippocampus• Location map – grid cells Entorhinal cortex

How do these different cell types provide Information about spatial orientation andnavigation?

Neural mechanisms underlyingorientation and navigation

Head Direction Cell

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3 Typical Head Direction Cells

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Anterior Dorsal Thalamus

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Lateral Mammillary NucleiFiring Rate (Hz)

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Dorsal Presubiculum

White cue card acts as the sole intentional orienting cueand can serve as a landmark that controls the preferred

firing direction of the cell.

180° Cue Card Rotation

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Preferred Firing Direction is Maintained in the Absence of the Cue Card

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Cell 1-Standard SessionCell 2-Standard SessionCell 1-No Cue Card SessionCell 2-No Cue Card Session

Firing Rate (Hz)

Head Direction (°)

Head direction Cells in 3D

• HD cells fire as a function of head direction in the horizontal plane.

• But how is the horizontal reference frame defined?

• How do HD cells respondduring vertical plane locomotion?

Vertical Sampling Apparatus

74 cm

Annulus

Food Cups

Wire Mesh Ladder

top view side view

Example of Recording Protocol

MESH 0° MESH 180° MESH 270° MESH 90°

(relative to HD cell's preferred firing direction)

Cylinder Floor and Annulus

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12/13 cells increased their firing rate on the annulus.

Mesh @ 0° Position

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Vertical Spiral Track

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Vertical Plane Data Summary

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• HD cell firing was maintained during vertical locomotion, if the rat approached the mesh in the cell's preferred firing direction.

• Horizontal reference frame was defined by the rat’s plane of locomotion, where the vertical surface was treated as an extension of the horizontal surface during approach.

How does an HD cell respond when a rat locomotesinverted, upside-down on the ceiling in 1-g ?

Loss of directional tuning on ceiling, with increased background firing rate.

• 70% of HD cells lose directional tuning when rat is upside down

Head Direction Cell Properties

• Direction of head, not body position.• Head direction in the horizontal plane.• Fires whether animal is moving or still.• Firing is independent of location and behavior.• Each cell exhibits one preferred firing direction.• Preferred firing directions distributed equally around

360º.• Little adaptation in cell firing when the rat holds its

head in the cell’s preferred firing direction.

Grid cells in the Medial Entorhinal Cortex

•Rat MEC in A and recording location in B. Grid field for a single MEC neuron in C. Location of firing (left), frequency (middle), and expanded grid field for the same neuron (right).

Grid cells have orderedfields with hexagonal structure

Grid fields form instantly in a new environment

Neighboring MEC grid cells have similar fields

Nearby cells fields aresimilar in spacing, but displaced by differencesin spatial phase

Grid fields size is topographic

Dorsal MEC cell fields aresmall dorsally, largerventrally

MEC grid cells modulate on top of theta rhythm

• A) Spikes as rat runs along linear track (left/right dorsal/ventral MEC) B) Firing rate modulates as rat crosses hot spots of grid field. C) Two cycles of theta wave (0 – 720 phase) show modulation of spikes relative to position and speed of rat as it moves

Place cells in the hippocampus.

• A – recording location in CA1 B – Place fields of pyramidal cells differ in the spatial environment, with primarily one location prominent for each cell.

CA place cells do not provide heading information

Head direction cells signal heading

Place cells respond regardless of direction, only signal allocentric location

Current map of navigation circuit

Vestibular Inactivation or Lesion Disrupts Spatial Firing

TTX Recovery

Pre Post 1hr 4hr 12 hr 24 hr 36 hr 48 hrPlace Cell

HD CellsPrePost 1 hrPost 12 hrPost 24 hrPost 48 hrFiring

Rate(Hz)

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TTXNa+ Arsanilate

Importance of Motor Efference & Proprioceptive Cues during Navigation

Rat is placed into arenas - preferred firing direction usually shifts by > 50°

What happens when the rat walks from the cylinder into the rectangle?

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Note that now the novel rectangle contains no familiar landmark cues, and the animal must rely on motor, vestibular, proprioception, or optic flow cues to maintain its orientation in the novel environment.

Novel Session

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Rat walks from cylinder into rectangle, preferred firing direction shifts by a mean of ± 18°