Learning & Memory in the Head Direction Cell...
Transcript of Learning & Memory in the Head Direction Cell...
![Page 1: Learning & Memory in the Head Direction Cell Circuitonline.itp.ucsb.edu/online/neuro14/taube/pdf/Taube_Neuro14_KITP.pdfVisual Tectal Pathway - Attention To test this, we conducted](https://reader033.fdocuments.us/reader033/viewer/2022060812/6090ae78db5476096a394d55/html5/thumbnails/1.jpg)
Learning & Memory in the Head Direction
Cell Circuit
Jeffrey Taube
Psychological & Brain Sciences
Dartmouth College
Hanover, NH
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• Circuitry issues – How the Head Direction signal is
generated?
• Involvement of vestibular & motor cues
• How visual landmark information is processed
• How HD signals guide behavior
• How head direction cells respond in 3-D, as well as under
micro-gravity conditions?
What our Lab studies:
![Page 3: Learning & Memory in the Head Direction Cell Circuitonline.itp.ucsb.edu/online/neuro14/taube/pdf/Taube_Neuro14_KITP.pdfVisual Tectal Pathway - Attention To test this, we conducted](https://reader033.fdocuments.us/reader033/viewer/2022060812/6090ae78db5476096a394d55/html5/thumbnails/3.jpg)
• Circuitry issues – How the HD signal is generated?
• Involvement of vestibular & motor cues
• How visual landmark information is processed
• How HD signals guide behavior
• How head direction cells respond in 3-D, as well as under
micro-gravity conditions?
• Grid cell generation
Review a number of HD cell studies that we have conducted that involve
learning and memory and inform us about some of the underlying neural
processes involved in navigation.
What our Lab studies:
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Contributors
Stephane Valerio
Brett Gibson
Ed GolobJeremy Goodridge
Gary Muir Jeffrey Calton
Ben Clark
Others:
Josh Bassett Joel Brown
Paul Dudchenko Russ Frohardt
Jennifer Rilling Mike Shinder
Bob Stackman Sarah Wang
Shawn Winter Ryan Yoder
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Two Components of Spatial Orientation
• Location - Place cells - 1971 - John O’Keefe
• Directional heading
But place cells do not provide information
about directional heading.
A second category of spatial cells encodes
for directional heading :
Head Direction cells
- Postsubiculum (dorsal presubiculum)
- found in many limbic system structures
1984 - James Ranck
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Head Direction Cell Video
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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.
0
°
90
°
180
°
270
°
Peak firing rate
Preferred
firing
direction
Background firing rate
Directional
firing
range
Head Direction (°)
Firing
Rate
(spikes/s)
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Where is the Postsubiculum?
M Witter (1989) In Hippocampus: New Vistas
Postsubiculum
- Deep layers
Dorsal portion of Presubiculum = Postsubiculum
Subicular Complex
• Subiculum (S)
• Presubiculum (PRE)
• Parasubiculum (PAR)
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3 Typical HD cells from different brain areas
Taube, Muller, Ranck (1990) J Neurosci; Taube (1995) J Neurosci; Stackman & Taube (1998) J Neurosci
Head Direction (°)
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# of Samples: 1267
Mean ISI: 12.14
Std. Dev.: 5.07
: 0.418
Info. Content:
2.021
Vector Length:
0.913
ATI:
23.7
Gamma function r:
0.977
Firin
g R
ate
(spik
es/s
)
Head Direction (°)
Time (msec)
Num
b
er
0
50
100
150
0-500-1000 500 1000
C
Interspike Interval (msec)
0 10 20 30 40 50 60
Fre
qu
en
cy (%
)
8
6
4
2
0
10
12
Firin
g R
ate
(spik
es/s
)
# of Samples: 815
Mean ISI: 14.57
Std. Dev.: 10.08
: 0.692
Info. Content: 1.853
Vector Length: 0.838
ATI: 39.8
Gamma function r: 0.933
Num
b
er
0-500-1000 500 10000
25
50
75
8
6
4
2
00 10 20 30 40 50 60 70
Fre
qu
en
cy (%
)B
# of Samples: 635
Mean ISI: 25.01
Std. Dev.: 20.67
: 0.826
Info. Content: 1.481
Vector Length: 0.872
ATI: 75.4
Gamma function r: 0.898
Firin
g R
ate
(spik
es/s
)N
um
b
er
0-500-1000 500 10000
10
20
30
5
4
3
2
1
0
Fre
qu
en
cy (%
)
0 12020 40 60 10080
A
No evidence for
theta-modulation
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Inhibitory
Excitatory
Place Cells
Angular Head Velocity Cells
Grid Cells
HD Cells
Head Direction Cell Circuitry
Interpeduncular
Nucleus
?
Nucleus
Prepositus
Medial
Vestibular
Nucleus
Supragenual
Nucleus
Retrosplenial
Cortex
Hippocampus
Postrhinal
Cortex
Parietal
Cortex
Entorhinal
Cortex
Anterior Dorsal
Thalamic Nuc.
Lateral
Mammillary
Nucleus
Dorsal
Tegmental
Nucleus
Postsubiculum
Taube (2007) Ann Rev Neurosci
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White cue card acts as the sole intentional orienting cue.
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Taube et al. (1990) J Neurosci
180° Cue Card Rotation
The cue card exerts stimulus control over
head-direction cell firing
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What brain areas are important for visual landmark
control of Head Direction & Place Cell activity?
Place cell
Place cell place fields also shift following
rotation of the salient visual cue
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What brain areas are important for visual landmark control
of Head Direction & Place Cell activity?
General view for processing visual information:
Dorsal stream important for processing spatial information - Parietal
cortex
![Page 16: Learning & Memory in the Head Direction Cell Circuitonline.itp.ucsb.edu/online/neuro14/taube/pdf/Taube_Neuro14_KITP.pdfVisual Tectal Pathway - Attention To test this, we conducted](https://reader033.fdocuments.us/reader033/viewer/2022060812/6090ae78db5476096a394d55/html5/thumbnails/16.jpg)
What brain areas are important for visual landmark control
of Head Direction & Place Cell activity?
General view for processing visual information:
Dorsal stream important for processing spatial information - Parietal
cortex
Ventral stream important for processing object recognition - Inferior
temporal cortex
![Page 17: Learning & Memory in the Head Direction Cell Circuitonline.itp.ucsb.edu/online/neuro14/taube/pdf/Taube_Neuro14_KITP.pdfVisual Tectal Pathway - Attention To test this, we conducted](https://reader033.fdocuments.us/reader033/viewer/2022060812/6090ae78db5476096a394d55/html5/thumbnails/17.jpg)
What brain areas are important for visual landmark control
of Head Direction & Place Cell activity?
General view for processing visual information:
Dorsal stream important for processing spatial information – Parietal
Cortex
Ventral stream important for processing object recognition – Inferior
Temporal Cortex
Visual Tectal Pathway - Attention
To test this, we conducted 90° landmark rotation experiments on HD
cells in animals with lesions of various brain areas.
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Head Direction cell responses to 90° cue card
rotations
Amount of ShiftFrequency Distribution
for Shift Amounts
Control
90
270
0180
Arrow represents
the mean vector
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Generative
Circuit
PoS
Entorhinal
CortexHippocampus
ADN
LMN
Subcortical Areas: Dorsal Tegmental Nuc. & Supragenual Nuc.
Head Direction Signal
Generative Circuit
PoS: Postsubiculum
ADN: Anterodorsal Thalamus
LMN: Lateral Mammillary Nuc.
![Page 20: Learning & Memory in the Head Direction Cell Circuitonline.itp.ucsb.edu/online/neuro14/taube/pdf/Taube_Neuro14_KITP.pdfVisual Tectal Pathway - Attention To test this, we conducted](https://reader033.fdocuments.us/reader033/viewer/2022060812/6090ae78db5476096a394d55/html5/thumbnails/20.jpg)
PoS: Postsubiculum
ADN: Anterodorsal Thalamus
LMN: Lateral Mammillary Nuc.
Generative
Circuit
PoS
Entorhinal
CortexHippocampus
ADN
LMN
Subcortical Areas
Head Direction Signal
Generative Circuit
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Control
Hippocampus
lesion
Limbic Pathway
None
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Visual
Cortex
Parietal
Retspl
PoS
Entorhinal
CortexHippocampus
Visual Streams for Processing Landmark Information:
Dorsal Stream
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Visual
Cortex
Parietal
Retspl
PoS
Entorhinal
CortexHippocampus
Visual Streams for Processing Landmark Information:
Dorsal Stream
ADN
![Page 24: Learning & Memory in the Head Direction Cell Circuitonline.itp.ucsb.edu/online/neuro14/taube/pdf/Taube_Neuro14_KITP.pdfVisual Tectal Pathway - Attention To test this, we conducted](https://reader033.fdocuments.us/reader033/viewer/2022060812/6090ae78db5476096a394d55/html5/thumbnails/24.jpg)
90
270
0180
Parietal Cortex
lesion
Dorsal Stream Pathway
Retrosplenial
Cortex lesion
90
270
0180
Control
Hippocampus
lesion
Limbic Pathway
Mild-
Moderate
None
![Page 25: Learning & Memory in the Head Direction Cell Circuitonline.itp.ucsb.edu/online/neuro14/taube/pdf/Taube_Neuro14_KITP.pdfVisual Tectal Pathway - Attention To test this, we conducted](https://reader033.fdocuments.us/reader033/viewer/2022060812/6090ae78db5476096a394d55/html5/thumbnails/25.jpg)
Visual
Cortex
Parietal
Retspl
PoS
Entorhinal
CortexHippocampus
Visual Streams for Processing Landmark Information:
Ventral Stream
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Visual
Cortex
Parietal
Retspl
PoS
Entorhinal
CortexHippocampus
Visual Streams for Processing Landmark Information:
Ventral Stream
ADN
![Page 27: Learning & Memory in the Head Direction Cell Circuitonline.itp.ucsb.edu/online/neuro14/taube/pdf/Taube_Neuro14_KITP.pdfVisual Tectal Pathway - Attention To test this, we conducted](https://reader033.fdocuments.us/reader033/viewer/2022060812/6090ae78db5476096a394d55/html5/thumbnails/27.jpg)
Entorhinal Cortex
lesion
90
270
0180
Parietal Cortex
lesion
Dorsal Stream Pathway Ventral Stream Pathway
Retrosplenial
Cortex lesion
90
270
0180
Control
Hippocampus
lesion
Limbic Pathway
None
![Page 28: Learning & Memory in the Head Direction Cell Circuitonline.itp.ucsb.edu/online/neuro14/taube/pdf/Taube_Neuro14_KITP.pdfVisual Tectal Pathway - Attention To test this, we conducted](https://reader033.fdocuments.us/reader033/viewer/2022060812/6090ae78db5476096a394d55/html5/thumbnails/28.jpg)
Visual
Cortex
Parietal
PoS
LDN
Tectal Stream
Entorhinal
CortexHippocampus
Visual Streams for Processing Landmark Information:
Tectal Stream
via
LDN: Lateral Dorsal
Thalamus
Superior Colliculus
Pulvinar
Superior
Colliculus
![Page 29: Learning & Memory in the Head Direction Cell Circuitonline.itp.ucsb.edu/online/neuro14/taube/pdf/Taube_Neuro14_KITP.pdfVisual Tectal Pathway - Attention To test this, we conducted](https://reader033.fdocuments.us/reader033/viewer/2022060812/6090ae78db5476096a394d55/html5/thumbnails/29.jpg)
Visual
Cortex
Parietal
PoS
LDN
Entorhinal
CortexHippocampus
Visual Streams for Processing Landmark Information:
Tectal Stream
via
LDN: Lateral Dorsal
Thalamus
Superior Colliculus
Pulvinar
Tectal Stream
Superior
Colliculus
![Page 30: Learning & Memory in the Head Direction Cell Circuitonline.itp.ucsb.edu/online/neuro14/taube/pdf/Taube_Neuro14_KITP.pdfVisual Tectal Pathway - Attention To test this, we conducted](https://reader033.fdocuments.us/reader033/viewer/2022060812/6090ae78db5476096a394d55/html5/thumbnails/30.jpg)
Entorhinal Cortex
lesion
90
270
0180
Parietal Cortex
lesion
Lateral Dorsal
Thalamus lesion
Dorsal Stream Pathway Ventral Stream Pathway
Tectal
Pathway
Retrosplenial
Cortex lesion
90
270
0180
Control
Hippocampus
lesion
Limbic Pathway
None
![Page 31: Learning & Memory in the Head Direction Cell Circuitonline.itp.ucsb.edu/online/neuro14/taube/pdf/Taube_Neuro14_KITP.pdfVisual Tectal Pathway - Attention To test this, we conducted](https://reader033.fdocuments.us/reader033/viewer/2022060812/6090ae78db5476096a394d55/html5/thumbnails/31.jpg)
Visual
Cortex
Parietal
PoS
LDN
Tectal Stream
Entorhinal
CortexHippocampus
Visual Streams for Processing Landmark Information:
Direct Projection:
Visual Cortex PoS
Postsubiculum
![Page 32: Learning & Memory in the Head Direction Cell Circuitonline.itp.ucsb.edu/online/neuro14/taube/pdf/Taube_Neuro14_KITP.pdfVisual Tectal Pathway - Attention To test this, we conducted](https://reader033.fdocuments.us/reader033/viewer/2022060812/6090ae78db5476096a394d55/html5/thumbnails/32.jpg)
Visual
Cortex
Parietal
PoS
LDN
Tectal Stream
Entorhinal
CortexHippocampus
Visual Streams for Processing Landmark Information:
ADN
LMN
Direct Projection:
Visual Cortex PoS
Postsubiculum
Place cells
HD cells
HD cells
![Page 33: Learning & Memory in the Head Direction Cell Circuitonline.itp.ucsb.edu/online/neuro14/taube/pdf/Taube_Neuro14_KITP.pdfVisual Tectal Pathway - Attention To test this, we conducted](https://reader033.fdocuments.us/reader033/viewer/2022060812/6090ae78db5476096a394d55/html5/thumbnails/33.jpg)
Entorhinal Cortex
lesion
90
270
0180
Parietal Cortex
lesion
LMN Recording
90
270
0180
Dorsal Stream Pathway Ventral Stream Pathway
Retrosplenial
Cortex lesion
90
270
0180
Control
Hippocampus
lesion
Limbic Pathway
Lateral Dorsal
Thalamus lesion
Tectal
Pathway
ADN Recording
Postsubiculum
Lesions
Hippocampal Place
Cell Recording
Place field absent
Severe
![Page 34: Learning & Memory in the Head Direction Cell Circuitonline.itp.ucsb.edu/online/neuro14/taube/pdf/Taube_Neuro14_KITP.pdfVisual Tectal Pathway - Attention To test this, we conducted](https://reader033.fdocuments.us/reader033/viewer/2022060812/6090ae78db5476096a394d55/html5/thumbnails/34.jpg)
Visual
Cortex
Parietal
PoS
LDN
Tectal Stream
Entorhinal
CortexHippocampus
Visual Streams for Processing Landmark Information:
Direct Projection:
Visual Cortex PoS
Postsubiculum
ADN
LMN
Place cells
![Page 35: Learning & Memory in the Head Direction Cell Circuitonline.itp.ucsb.edu/online/neuro14/taube/pdf/Taube_Neuro14_KITP.pdfVisual Tectal Pathway - Attention To test this, we conducted](https://reader033.fdocuments.us/reader033/viewer/2022060812/6090ae78db5476096a394d55/html5/thumbnails/35.jpg)
Entorhinal Cortex
lesion
90
270
0180
Parietal Cortex
lesion
Hippocampal Place
Cell Recording
LMN Recording
90
270
0180
Place field absent
Dorsal Stream Pathway Ventral Stream Pathway
Retrosplenial
Cortex lesion
90
270
0180
Anterior Dorsal
Thalamus lesion
Place cell recording
ADN Recording
Postsubiculum
Lesions
Control
Hippocampus
lesion
Limbic Pathway
Lateral Dorsal
Thalamus lesion
Tectal
Pathway
None
![Page 36: Learning & Memory in the Head Direction Cell Circuitonline.itp.ucsb.edu/online/neuro14/taube/pdf/Taube_Neuro14_KITP.pdfVisual Tectal Pathway - Attention To test this, we conducted](https://reader033.fdocuments.us/reader033/viewer/2022060812/6090ae78db5476096a394d55/html5/thumbnails/36.jpg)
Visual
Cortex
Parietal
Retspl
PoS
LDN
Tectal Stream
Entorhinal
CortexHippocampus
ADN
LMN
Subcortical AreasGe
nera
tive
Circu
it
So, what can
we conclude ?
Superior
Colliculus
![Page 37: Learning & Memory in the Head Direction Cell Circuitonline.itp.ucsb.edu/online/neuro14/taube/pdf/Taube_Neuro14_KITP.pdfVisual Tectal Pathway - Attention To test this, we conducted](https://reader033.fdocuments.us/reader033/viewer/2022060812/6090ae78db5476096a394d55/html5/thumbnails/37.jpg)
Visual
Cortex
Parietal
Retspl
PoS
LDN
Tectal Stream
Entorhinal
CortexHippocampus
ADN
LMN
Subcortical AreasGe
nera
tive
Circu
it
So, what can
we conclude ?
Superior
Colliculus
![Page 38: Learning & Memory in the Head Direction Cell Circuitonline.itp.ucsb.edu/online/neuro14/taube/pdf/Taube_Neuro14_KITP.pdfVisual Tectal Pathway - Attention To test this, we conducted](https://reader033.fdocuments.us/reader033/viewer/2022060812/6090ae78db5476096a394d55/html5/thumbnails/38.jpg)
Visual
Cortex
Parietal
Retspl
PoS
LDN
Tectal Stream
Entorhinal
CortexHippocampus
ADN
LMN
Subcortical AreasGe
nera
tive
Circu
it
So, what can
we conclude ?
Superior
Colliculus
![Page 39: Learning & Memory in the Head Direction Cell Circuitonline.itp.ucsb.edu/online/neuro14/taube/pdf/Taube_Neuro14_KITP.pdfVisual Tectal Pathway - Attention To test this, we conducted](https://reader033.fdocuments.us/reader033/viewer/2022060812/6090ae78db5476096a394d55/html5/thumbnails/39.jpg)
Visual
Cortex
Parietal
Retspl
PoS
LDN
Tectal Stream
Entorhinal
CortexHippocampus
ADN
LMN
Subcortical AreasGe
nera
tive
Circu
it
So, what can
we conclude ?
Superior
Colliculus
![Page 40: Learning & Memory in the Head Direction Cell Circuitonline.itp.ucsb.edu/online/neuro14/taube/pdf/Taube_Neuro14_KITP.pdfVisual Tectal Pathway - Attention To test this, we conducted](https://reader033.fdocuments.us/reader033/viewer/2022060812/6090ae78db5476096a394d55/html5/thumbnails/40.jpg)
Visual
Cortex
Parietal
Retspl
PoS
LDN
Tectal Stream
Entorhinal
CortexHippocampus
ADN
LMN
Subcortical AreasGe
nera
tive
Circu
it
So, what can
we conclude ?
Superior
Colliculus
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Visual
Cortex
Parietal
Retspl
PoS
LDN
Tectal Stream
Entorhinal
CortexHippocampus
ADN
LMN
Subcortical AreasGe
nera
tive
Circu
it
Landmark control in
ADN and LMN
occurs because of
the feedback loop
from PoS LMN
and ADN.
Conclusion: For
processing visual
landmark information:
the direct pathway
from Visual Areas
17, 18 --> PoS is
critical.
Superior
Colliculus
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How fast can Head Direction cells learn
about the visual landmarks ?
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Rats can learn landmark information very fast
Here they learned about the visual cue card in a matter of minutes.
8 min Exposure
1 min Exposure
8 min Exposure
1 min Exposure
5 out of 8 rotated well
Goodridge et al. (1998) Beh Neurosci
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Is the hippocampus important for HD cells to learn
about novel visual landmarks?
Hippocampal lesion
• We can take advantage of the fact that HD cells have different preferred
directions in geometrically different environments.
• Thus, a change in the shape of the environment will usually lead to a shift in the
cell’s preferred firing direction
Cylinder vs. Rectangle & Square
Cylinder 1
Rectangle
Cylinder 2
Square
Cylinder 3
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Suggests that learning the spatial information about landmarks is more like
perceptual learning, where visual information can drive the system directly – it is
not like episodic learning, which involves the hippocampus.
HD Cell preferred directions remain stable in a novel
environment across days, despite the absence of hippocampus
Cylinder – Familiar Novel Enclosures
Triangle
Pentagon
Golob & Taube (1997) PNAS
Novel Enclosures across days
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What is the evidence that HD cells
can guide behavior ?
Linkage between HD cell firing and behavior
•What you would like to see is that when a cell’s preferred
firing direction shifts a certain amount, that the animal’s
spatial behavior (choice) also shifts the same amount.
•Review a few studies with HD cells where we looked for
this linkage.
•What happens with HD cells following a behavioral error?
Does the HD also show a shift in its PFD?
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Training Trials Test Trial
Example 1: HD Cell information is not always used for solving
Spatial Tasks : Tolman Sunburst Maze
Muir & Taube (2004) Beh Brain Res
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HD Cell Plots on Error Trials for 2 Different Cells
Training Trials Test Trials in which rat made an error
……. thus, directional heading information was present,
but the animal did not use it to guide behavior.
This could explain why they had poor performance – no learning took place.
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Standard Cue Rotation Novel Environment
Example 2: Animal solves a spatial task, but is not using
HD cell information to guide its behaviorWater Reward
• Rat trained in square to go to a corner with water reward relative to
landmark.
• Receives 40-60 trials in standard session and performing ~ 77% correct.
• Rotation of landmark leads to an equal shift in the animal’s behavior and
the HD cell’s preferred firing direction.
• Rat generalizes well in the rectangle – and goes to the correct corner –
78% correct.
• But HD cells shifted their preferred directions > 72° in 12 / 13 sessions
(but their behavior did not shift the same amount) little evidence that HD
cell firing was guiding the animal’s behavior.
Behavior was not in register with the shift in the cell’s preferred direction.
La
nd
ma
rk C
ue
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Square Session
Rectangle Session
Square Session
Rectangle Session
HD cell preferred direction
remains the same
HD cell preferred
direction shifts
Golob et al (2001) Beh Neurosci
• Recordings from same cell on two consecutive trials in the rectangle.
• In both cases, rat generalized well from training in the square and
selected the correct corner in the rectangle.
• Cell’s preferred direction was different on both trials – but behavior
was similar.
• Suggests that this cell’s firing was not strongly linked to the animal’s
behavior.
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Head Direction cells and responses in 3D
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Array of Disorientation Problems & Illusions in Space
Astronauts are frequently disoriented when working in
space (0-g) and often experience several types of illusions,
including:
• Visual Reorientation Illusion (VRIs)
• Inversion Illusion
• Extra Vehicular Activity (EVA) acrophobia
Which leads to a number of problems:
• Space motion sickness
• Poor spatial awareness – worry about emergency egress
• Inability to do work
• Flipping switches in wrong direction
• Otolith reinterpretation upon return
to a gravitational environment
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HD cell responses in Vertical Plane
Experiment 1 Experiment 2
Start
Finish
Platform
Rotation
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South Wall
We
st W
all
East W
all
North Wall
0°
90°
180°
270°
0°
90°
180°
270°
xy 0°
90°
180°
270°
0°
90°
180°
270°
0°
90°
180°
270°
Floor
Animal defines its horizontal reference frame as the plane it happens to
be locomoting in. Thus, it rotates its plane of locomotion by 90° as it
moves into the vertical plane and defines this new surface as its
horizontal reference frame.
South Wall
We
st W
all
Ea
st W
all
North Wall
Floor
Room Reference Frame
UpDown
Direction of Cell Firing Along Walls
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HD cell responses in 3D: Vertical plane and
when Upside-down on ceiling
Calton & Taube (2005) J Neurosci
Barrier
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Similar to our wall-climbing findings, HD cells
treated the walls as though they were an extension
of the floor.
Cell fires duringclimb up.
Cell fires duringclimb down.
Preferreddirectionof cell.
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Running in the reverse direction, the cell is silent
on both walls.
Cell fires duringclimb up.
Cell fires duringclimb down.
Preferreddirectionof cell.
Cell is silent
during climb up.
Cell is silent during
climb down.
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For most cells: Loss of directional tuning on
ceiling, with increased background firing rate
Cell 1 Cell 2
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A few Cells Remained Directionally-tuned
Two examples:
…. but even most of these cells had markedly reduced peak firing rates.
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During inverted locomotion on the ceiling, cells had a lower
directional information content score.
Directional Information Content
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Inverted Hole Board Escape Task
Could animals learn a spatial task upside-down ?
Valerio, Clark et al. (2010) Neurobiol Learning & Memory
+
X = Four Release Points
+ = Center Release Point
x
x
Escape hole
x
x
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Performance in the Inverted Hole Board Escape Task
Esca
pe
La
ten
cy (
se
c)
Training day
0
5
10
15
20
25
30
0 5 10
1 Start Point
1SP 2SP
Num
be
r o
f S
essio
ns
to C
rite
rio
n
0
4
8
12
16
Criterion Center
Probe
La
ten
cy (
sec)
0
10
20
30
Regular
trialsBlindfolded-
to-apparatus
trials
La
ten
cy (
se
c)
0
10
20
30
Surround
Curtain
Probe
Criterion
La
ten
cy (
sec)
0
10
20
30
1 Start Point
2 Start Points
Esca
pe
La
ten
cy (
se
c)
Training day
0
5
10
15
20
25
30
5 10 15 20 25
4 Start Points
30
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Conclusions from Behavioral Task:
When task was simple (1 or 2 start points) – animals could
use a directional (or beacon) strategy – move toward a
particular landmark.
But when task was difficult (4 start points) – animals
needed a more flexible representation of their
environment.
They needed a flexible cognitive map-like spatial strategy.
It is possible that ‘normal’ HD activity is required for
generation and use of a cognitive map.
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Valerio, Clark et al. (2010) Neurobiol Learning & Memory
+
X = Familiar Release Point 1
X = Familiar Release Point 2
+ = Center Release Pointx
x
Escape hole
Record HD cells in the
Inverted Hole Board Escape Task
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Familiar
Tests
2 Start
Points .
N
S
W E
NCenter
Tests
180
S
W E
.
N
S
W E
180
S
W E
N
Sample PathsTrajectories
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What are Head Direction Cells doing in this Task?
2nd Session on Floor:
Upright
Session on Floor:
Upright
Head Direction
Firin
g R
ate
Rats trained from two locations
NW
SW
Thus, rats were accurately performing the simple version of the inverted
spatial task - despite the absence of a HD signal.
NW Inverted Trial
Correct
Inverted Trial: Center
Error
SW Inverted Trial
Correct
I n v e r t e d T r i a l s
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Conclusions
The results suggest that the head direction signal is
needed for accurate navigation in situations that require a
flexible representation of space (i.e., an allocentric
cognitive-mapping strategy), but not for situations that
utilize habit-like associative spatial learning.
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Looking for the linkage between HD cells and
behavior using a task involving path integration.
What happens with HD cells following
a behavioral error?
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Reorientation
Cells get Reset to their previously established relationship with the
familiar landmarks
I thought that building
would be on my left
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Place Cell Remapping
Bostock, Kubie, Muller, 1991, Hippocampus
White
Cue Card
Black
Cue Card
Cylinder vs. Rectangle & Square
Head Direction Cell Remapping
Taube, Muller, Ranck, 1990, J Neurosci
A change in the shape of the environment usually
lead to a shift in the cell’s preferred firing direction.
In addition to Resetting, cells can also Remap
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Food-Carrying task requiring Path Integration:
Behavior compared to Cell Activity
Refuge
Return
Point
Barrier
Food
Pellet
Outbound path
Return path
Valerio & Taube (2012) Nat Neurosci
Rats are blindfolded
Curtain
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Hypothetical Results for Two Consecutive Trials
Initial Refuge session
(6 min)
80
0
20
40
60
Firin
g r
ate
(spik
es/s
ec)
36060 120 180 240 3000
Head direction (°)
PFD = 90°
PFD = Preferred Firing Direction
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Hypothetical Results for Two Consecutive Trials
PFD = Preferred Firing Direction
Trial 1Initial Refuge session
(6 min)
Heading error = - 30°
PFD shift = - 30°
80
0
20
40
60
Firin
g r
ate
(spik
es/s
ec)
36060 120 180 240 3000
Head direction (°)
PFD = 90°80
0
20
40
60
36060 120 180 240 3000
PFD = 60°
Head direction (°)
- 30°
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Hypothetical Results for Two Consecutive Trials
PFD = Preferred Firing Direction
Trial 1Initial Refuge session
(6 min)
Refuge
Inter-trial 1
Heading error = - 30°
PFD shift = - 30°
Reorientation:
Resetting
80
0
20
40
60
Firin
g r
ate
(spik
es/s
ec)
36060 120 180 240 3000
Head direction (°)
PFD = 90°80
0
20
40
60
36060 120 180 240 3000
PFD = 90°
Head direction (°)
80
0
20
40
60
36060 120 180 240 3000
PFD = 60°
Head direction (°)
The PFD gets reset to
the previous refuge
value.
- 30°
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Hypothetical Results for Two Consecutive Trials
Trial 1 Trial 2Initial Refuge session
(6 min)
Refuge
Inter-trial 1
- 30°
Heading error = - 30°
PFD shift = - 30°
Reorientation:
Resetting
80
0
20
40
60
Firin
g r
ate
(spik
es/s
ec)
36060 120 180 240 3000
Head direction (°)
PFD = 90°80
0
20
40
60
36060 120 180 240 3000
PFD = 90°
Head direction (°)
80
0
20
40
60
36060 120 180 240 3000
PFD = 60°
Head direction (°)
Heading error = + 60°
PFD shift = + 60°
+ 60°
80
0
20
40
60
36060 120 180 240 3000
PFD = 150°
Head direction (°)
The PFD gets reset to
the previous refuge
value.PFD = Preferred Firing Direction
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Hypothetical Results for Two Consecutive Trials
PFD = Preferred Firing Direction
Trial 1 Trial 2Initial Refuge session
(6 min)
Refuge
Inter-trial 1
Refuge
Inter-trial 2
Heading error = - 30°
PFD shift = - 30°
Reorientation:
ResettingReorientation
Correction Process:
Remapping
80
0
20
40
60
Firin
g r
ate
(spik
es/s
ec)
36060 120 180 240 3000
Head direction (°)
PFD = 90°80
0
20
40
60
36060 120 180 240 3000
PFD = 90°
Head direction (°)
80
0
20
40
60
36060 120 180 240 3000
PFD = 60°
Head direction (°)
Heading error = + 60°
PFD shift = + 60°
80
0
20
40
60
36060 120 180 240 3000
PFD = 150°
Head direction (°)
80
0
20
40
60
36060 120 180 240 3000
PFD = 150°
Head direction (°)
The PFD gets reset to
the previous refuge
value.
The PFD does not get
reset to the previous
refuge value.
- 30°
+ 60°
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Individual Trials for 3 Different Cells
Behavioral Heading Error correlates with Shift of HD cell’s PFD
Inter-trial interval in refuge
During foraging task
Heading Error = - 7.5°
PFD Shift = - 8.6°
Heading Error = + 8.5°
PFD Shift = + 18.0°
Heading Error = - 42.2°
PFD Shift = - 36.8°
Head Direction (deg) Head Direction (deg) Head Direction (deg)
600 120 180 240 300 360 600 120 180 240 300 360 600 120 180 240 300 360
60
40
20
0
Firin
g R
ate
40
20
0
30
10Firin
g R
ate
40
20
0
30
10Firin
g R
ate
Return trip
![Page 78: Learning & Memory in the Head Direction Cell Circuitonline.itp.ucsb.edu/online/neuro14/taube/pdf/Taube_Neuro14_KITP.pdfVisual Tectal Pathway - Attention To test this, we conducted](https://reader033.fdocuments.us/reader033/viewer/2022060812/6090ae78db5476096a394d55/html5/thumbnails/78.jpg)
Correlation between Heading Error and the amount the
Preferred Firing Direction (PFD) shifted during the
outbound trip was good
Headin
g E
rror
(°)
r = 0.72
PFD shift from refuge to when
rat found food pellet
180
90
0
-90
-180
180900-90-180
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Example When Resetting Process Occurred
Heading Error = 5.7°
PFD Shift = -5.3°
0
10
20
30
40
3600 60 120 180 240 300
Head Direction (°)
Firin
g R
ate
Outbound path
Return path
Original
Refuge
PFD = 102°
Outbound Response
Original (initial) Refuge Response
Trial 1
![Page 80: Learning & Memory in the Head Direction Cell Circuitonline.itp.ucsb.edu/online/neuro14/taube/pdf/Taube_Neuro14_KITP.pdfVisual Tectal Pathway - Attention To test this, we conducted](https://reader033.fdocuments.us/reader033/viewer/2022060812/6090ae78db5476096a394d55/html5/thumbnails/80.jpg)
Example When Resetting Process Occurred
Heading Error = 5.7°
PFD Shift = -5.3°
0
10
20
30
40
3600 60 120 180 240 300
Head Direction (°)
Refuge
Inter-trial 1
0
10
20
30
40
3600 60 120 180 240 300
Head Direction (°)
Firin
g R
ate
Outbound path
Return path
Original Refuge Response
Current Refuge Response
Original
Refuge
PFD = 102°
Return
Refuge
PFD = 108°
Trial 1
![Page 81: Learning & Memory in the Head Direction Cell Circuitonline.itp.ucsb.edu/online/neuro14/taube/pdf/Taube_Neuro14_KITP.pdfVisual Tectal Pathway - Attention To test this, we conducted](https://reader033.fdocuments.us/reader033/viewer/2022060812/6090ae78db5476096a394d55/html5/thumbnails/81.jpg)
Example When Resetting Process Occurred
Heading Error = 5.7°
PFD Shift = -5.3°
0
10
20
30
40
3600 60 120 180 240 300
Head Direction (°)
Heading Error = - 2.0°
PFD Shift = -22.3°
Refuge
Inter-trial 1
0
10
20
30
40
3600 60 120 180 240 300
Head Direction (°)
Firin
g R
ate
0
10
20
30
40
3600 60 120 180 240 300
Head Direction (°)
Error
Outbound path
Return path
Original Refuge Response
Preceding Refuge Response
Outbound Response
Original
Refuge
PFD = 102°
Return
Refuge
PFD = 108°Foraging
PFD = 80°
Trial 1 Trial 2
![Page 82: Learning & Memory in the Head Direction Cell Circuitonline.itp.ucsb.edu/online/neuro14/taube/pdf/Taube_Neuro14_KITP.pdfVisual Tectal Pathway - Attention To test this, we conducted](https://reader033.fdocuments.us/reader033/viewer/2022060812/6090ae78db5476096a394d55/html5/thumbnails/82.jpg)
Example When Resetting Process Occurred
Heading Error = 5.7°
PFD Shift = -5.3°
0
10
20
30
40
3600 60 120 180 240 300
Head Direction (°)
0
10
20
30
40
3600 60 120 180 240 300
Head Direction (°)
Heading Error = - 2.0°
PFD Shift = -22.3°
Refuge
Inter-trial 1
Refuge
Inter-trial 2
0
10
20
30
40
3600 60 120 180 240 300
Head Direction (°)
Firin
g R
ate
The PFD is reset to the refuge value upon return to the refuge.
0
10
20
30
40
3600 60 120 180 240 300
Head Direction (°)
Error PFD is Reset
Outbound path
Return path
Original Refuge Response
Current Refuge Response
Original
Refuge
PFD = 102°
Return
Refuge
PFD = 108°Foraging
PFD = 80°Refuge
PFD = 105°
Trial 1 Trial 2
![Page 83: Learning & Memory in the Head Direction Cell Circuitonline.itp.ucsb.edu/online/neuro14/taube/pdf/Taube_Neuro14_KITP.pdfVisual Tectal Pathway - Attention To test this, we conducted](https://reader033.fdocuments.us/reader033/viewer/2022060812/6090ae78db5476096a394d55/html5/thumbnails/83.jpg)
Example When Remapping Process Occurred
Outbound path
Return path
Head Direction (°)
3600 60 120 180 240 300
80
0
20
40
60
Firin
g R
ate
Heading Error = - 43.7°
PFD Shift = - 63.8°
Original
Refuge
PFD = 196°
Refuge Response
Outbound Response
Trial 1
![Page 84: Learning & Memory in the Head Direction Cell Circuitonline.itp.ucsb.edu/online/neuro14/taube/pdf/Taube_Neuro14_KITP.pdfVisual Tectal Pathway - Attention To test this, we conducted](https://reader033.fdocuments.us/reader033/viewer/2022060812/6090ae78db5476096a394d55/html5/thumbnails/84.jpg)
Example When Remapping Process Occurred
Outbound path
Return path
Head Direction (°)
3600 60 120 180 240 300
80
0
20
40
60
Refuge
Inter-trial 1
Head Direction (°)
3600 60 120 180 240 300
80
0
20
40
60
Firin
g R
ate
Heading Error = - 43.7°
PFD Shift = - 63.8°
PFD is not Reset
Original Refuge Response
Current Refuge Response
Original
Refuge
PFD = 196°
Return
Refuge
PFD = 125°
Trial 1
![Page 85: Learning & Memory in the Head Direction Cell Circuitonline.itp.ucsb.edu/online/neuro14/taube/pdf/Taube_Neuro14_KITP.pdfVisual Tectal Pathway - Attention To test this, we conducted](https://reader033.fdocuments.us/reader033/viewer/2022060812/6090ae78db5476096a394d55/html5/thumbnails/85.jpg)
Example When Remapping Process Occurred
Outbound path
Return path
Head Direction (°)
3600 60 120 180 240 300
80
0
20
40
60
Refuge
Inter-trial 1
Head Direction (°)
3600 60 120 180 240 300
80
0
20
40
60
Firin
g R
ate
Heading Error = - 14.5°
PFD Shift =5.5°
Heading Error = - 43.7°
PFD Shift = - 63.8°
PFD is not Reset
Head Direction (°)
3600 60 120 180 240 300
80
0
20
40
60
Original Refuge Response
Preceding Refuge Response
Outbound Response
Original
Refuge
PFD = 196°
Return
Refuge
PFD = 125°Outbound
PFD = 123°
Trial 1 Trial 2
![Page 86: Learning & Memory in the Head Direction Cell Circuitonline.itp.ucsb.edu/online/neuro14/taube/pdf/Taube_Neuro14_KITP.pdfVisual Tectal Pathway - Attention To test this, we conducted](https://reader033.fdocuments.us/reader033/viewer/2022060812/6090ae78db5476096a394d55/html5/thumbnails/86.jpg)
Example When Remapping Process Occurred
Remapping Occurs - the PFD is not reset to the refuge value upon return
to the refuge, but instead retains the current PFD value (~120°) for the
next trial (#2) and subsequent trials (#s 8 and 9 are shown).
Outbound path
Return path
Head Direction (°)
3600 60 120 180 240 300
80
0
20
40
60
Head Direction (°)
3600 60 120 180 240 300
80
0
20
40
60
Refuge
Inter-trial 1
Refuge
Inter-trial 2
Head Direction (°)
3600 60 120 180 240 300
80
0
20
40
60
Firin
g R
ate
Heading Error = - 14.5°
PFD Shift =5.5°
Heading Error = - 43.7°
PFD Shift = - 63.8°
PFD is not Reset
Head Direction (°)
3600 60 120 180 240 300
80
0
20
40
60
Original
Refuge
PFD = 196°
Return
Refuge
PFD = 125°Outbound
PFD = 123°
Return Refuge
PFD 2 = 118°PFD 8 = 113°PFD 9 = 136°
Inter-trial 8
Inter-trial 9
Inter-trial 2Original Refuge
Trial 1 Trial 2
![Page 87: Learning & Memory in the Head Direction Cell Circuitonline.itp.ucsb.edu/online/neuro14/taube/pdf/Taube_Neuro14_KITP.pdfVisual Tectal Pathway - Attention To test this, we conducted](https://reader033.fdocuments.us/reader033/viewer/2022060812/6090ae78db5476096a394d55/html5/thumbnails/87.jpg)
When did Resetting and Remapping trials occur?
12090 1500 30 60
Resetting trials
Remapping trials
Heading Error (°)
Nu
mbe
r of
tria
ls
Resetting occurred more often following small heading errors.
Remapping occurred more often following large heading errors.
![Page 88: Learning & Memory in the Head Direction Cell Circuitonline.itp.ucsb.edu/online/neuro14/taube/pdf/Taube_Neuro14_KITP.pdfVisual Tectal Pathway - Attention To test this, we conducted](https://reader033.fdocuments.us/reader033/viewer/2022060812/6090ae78db5476096a394d55/html5/thumbnails/88.jpg)
Conclusions
•HD cells encode information about the animal’s perceived directional
heading in its environment.
•Can learn landmarks quickly and without the hippocampus.
•HD cells do not appear to be used when animal is using a directional
‘beacon’ strategy, but may be necessary for spatial strategies that require a
flexible representation of the spatial environment - cognitive map.
•HD cell activity and behavioral performance correlated well when animal
performed a task requiring path integration.
•When a behavioral error is made, there are two types of correction
processes: resetting and remapping.
![Page 89: Learning & Memory in the Head Direction Cell Circuitonline.itp.ucsb.edu/online/neuro14/taube/pdf/Taube_Neuro14_KITP.pdfVisual Tectal Pathway - Attention To test this, we conducted](https://reader033.fdocuments.us/reader033/viewer/2022060812/6090ae78db5476096a394d55/html5/thumbnails/89.jpg)
Grid Cell Signal Generation
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Grid Cells & Motor/Proprioceptive Cues