What brain areas are important for visual

landmark control of
Head Direction & Place Cell activity?

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

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

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 Visual Attention

To test which pathways are important, we conducted 90

landmark rotation experiments on HD cells in animals with
lesions of various brain areas.

Head Direction cell responses to 90 cue card

rotations
Frequency Distribution
for Shift Amounts

90

180

270

Control

Arrow represents
the mean vector

Amount of Shift

Head Direction Signal

Generative Circuit

Hippocampus

Entorhinal
Cortex
PoS

ADN

Generative
Circuit

LMN

PoS: Postsubiculum
ADN: Anterodorsal Thalamus
LMN: Lateral Mammillary Nuc.

Subcortical Areas: Dorsal Tegmental Nuc. & Supragenual Nuc.

Head Direction Signal

Generative Circuit

Entorhinal
Cortex

Hippocampus

PoS

ADN

Generative
Circuit

LMN

Subcortical Areas

PoS: Postsubiculum
ADN: Anterodorsal Thalamus
LMN: Lateral Mammillary Nuc.

Control

Limbic Pathway

None
Hippocampus
lesion

Visual Streams for Processing Landmark Information:

Dorsal Stream
Parietal
Retspl

Visual
Cortex
Entorhinal
Cortex

Hippocampus

PoS

Visual Streams for Processing Landmark Information:

Dorsal Stream
Parietal
Retspl

Visual
Cortex
Entorhinal
Cortex

Hippocampus

PoS
ADN

Control

Dorsal Stream Pathway

90

180

None

270

Limbic Pathway

Parietal Cortex
lesion

90

180

270

Hippocampus
lesion

Retrosplenial
Cortex lesion

MildModerate

Visual Streams for Processing Landmark Information:

Ventral Stream
Parietal
Retspl

Visual
Cortex
Hippocampus

Entorhinal
Cortex
PoS

Visual Streams for Processing Landmark Information:

Ventral Stream
Parietal
Retspl

Visual
Cortex
Hippocampus

Entorhinal
Cortex
PoS

ADN

Control

Dorsal Stream Pathway

Ventral Stream Pathway

90

180

None

270

Limbic Pathway

Parietal Cortex
lesion

90

180

270

Hippocampus
lesion

Retrosplenial
Cortex lesion

Entorhinal Cortex
lesion

Visual Streams for Processing Landmark Information:

Tectal Stream
via
LDN: Lateral Dorsal
Thalamus
Superior Colliculus
Pulvinar

Parietal

Tectal Stream
LDN
Hippocampus

Entorhinal
Cortex

PoS
Superior
Colliculus

Visual
Cortex

Visual Streams for Processing Landmark Information:

Tectal Stream
via
LDN: Lateral Dorsal
Thalamus
Superior Colliculus
Pulvinar

Parietal

Tectal Stream
LDN
Hippocampus

Entorhinal
Cortex

PoS
Superior
Colliculus

Visual
Cortex

Control

Dorsal Stream Pathway

Ventral Stream Pathway

90

180

270

Limbic Pathway

Parietal Cortex
lesion

90

180

270

Hippocampus
lesion

Tectal
Pathway

None
Lateral Dorsal
Thalamus lesion

Retrosplenial
Cortex lesion

Entorhinal Cortex
lesion

Visual Streams for Processing Landmark Information:

Direct Projection:
Visual Cortex PoS
Postsubiculum

Parietal

Tectal Stream
LDN
Hippocampus

Entorhinal
Cortex
PoS

Visual
Cortex

Visual Streams for Processing Landmark Information:

Direct Projection:
Visual Cortex PoS
Postsubiculum

Parietal

Tectal Stream
LDN
Hippocampus

Entorhinal
Cortex
PoS

ADN
LMN

Visual
Cortex

Control

Dorsal Stream Pathway

Ventral Stream Pathway

Postsubiculum
Lesions

90

180

270

Limbic Pathway

Parietal Cortex
lesion

Entorhinal Cortex
lesion

ADN Recording

90
90
180
180

270

Tectal
Pathway

Hippocampus
lesion

Severe

270

LMN Recording

Retrosplenial
Cortex lesion

Hippocampal Place
Cell Recording
Lateral Dorsal
Thalamus lesion

Place field absent

Visual Streams for Processing Landmark Information:

Direct Projection:
Visual Cortex PoS
Postsubiculum

Parietal

Tectal Stream
LDN
Hippocampus

Entorhinal
Cortex
PoS

ADN
LMN

Visual
Cortex

Control

Dorsal Stream Pathway

Ventral Stream Pathway

Postsubiculum
Lesions

90

180

270

Limbic Pathway

Parietal Cortex
lesion

Entorhinal Cortex
lesion

ADN Recording

90
90
180
180

0
270
270

Tectal
Pathway

Hippocampus
lesion

LMN Recording

Retrosplenial
Cortex lesion

None
Lateral Dorsal
Thalamus lesion

Anterior Dorsal
Thalamus lesion
Place cell recording

Hippocampal Place
Cell Recording
Place field absent

So, what can

we conclude ?

Parietal
Retspl

Tectal Stream
LDN
Entorhinal
Cortex

Hippocampus

PoS
Superior
Colliculus

Generative
Circuit

ADN
LMN

Subcortical Areas

Visual
Cortex

So, what can

we conclude ?

Parietal
Retspl

Tectal Stream
LDN
Entorhinal
Cortex

Hippocampus

PoS
Superior
Colliculus

Generative
Circuit

ADN
LMN

Subcortical Areas

Visual
Cortex

So, what can

we conclude ?

Parietal
Retspl

Tectal Stream
LDN
Entorhinal
Cortex

Hippocampus

PoS
Superior
Colliculus

Generative
Circuit

ADN
LMN

Subcortical Areas

Visual
Cortex

So, what can

we conclude ?

Parietal
Retspl

Tectal Stream
LDN
Entorhinal
Cortex

Hippocampus

PoS
Superior
Colliculus

Generative
Circuit

ADN
LMN

Subcortical Areas

Visual
Cortex

So, what can

we conclude ?

Parietal
Retspl

Tectal Stream
LDN
Entorhinal
Cortex

Hippocampus

PoS
Superior
Colliculus

Generative
Circuit

ADN
LMN

Subcortical Areas

Visual
Cortex

Conclusion: For
processing visual
landmark information:
the direct pathway
from Visual Areas
17, 18 --> PoS is
critical.

Parietal
Retspl

Tectal Stream
LDN
Entorhinal
Cortex

Hippocampus

PoS
Superior
Colliculus

ADN

Generative
Circuit

Landmark control in
ADN and LMN
occurs because of
the feedback loop
from PoS LMN
and ADN.

LMN

Subcortical Areas

Visual
Cortex

But Studies with Humans might suggest otherwise..

Imaging Expts and the Identification of a Brain Area Involved in

the Recognition of Places
Parahippocampal Place Area (PPA)
Epstein & Kanwisher

Scenes activate the PPA

Results demonstrating that the PPA
responds selectively to scenes. a.
Examples of intact and scrambled
versions of the four different types of
stimuli (top), and the average per cent
signal change for each stimulus type
in the PPA averaged overall subjects
(bottom). The difference between
intact and scrambled versions of each
picture is a measure of the response
in the PPA to each stimulus type
partially unconfounded from the
response to its low-level visual
features. Half of the scenes were
outdoor scenes of the MIT campus,
and half were indoor scenes of
unfamiliar locations. b. The time
course of the percent change in MR
signal intensity in the PPA over the
period of the scan. Per cent signal
change was calculated individually for
each subject using that subjects
fixation activation as baseline and then
averaging across subjects (black dot
indicates fixation epochs). i, intact; s,
scrambled; S, scenes; F, faces; O,
objects; H, houses.

Anatomical location of the PPA

a, A single slice from each of the nine subjects in
experiment 1 showing the PPA; functional data
from this experiment is overlaid on a highresolution T1-weighted anatomical image of the
same slice. Right hemisphere appears on the left.
Significance levels reflect the results of a
Kolmogorov-Smirnov test comparing the MR
signal intensity during viewing of intact scenes to
signal intensity during viewing of intact objects
and faces. Note that the location of the PPA
(indicated with yellow arrows) is strikingly
consistent across subjects. The activated region
was larger in the right hemisphere than the left
hemisphere. Significant activation was also found
in the anterior calcarine sulcus, but because of the
proximity of this region to retinotopic cortex, this
activation is not discussed here. b, Two adjacent
slices form a single subject demonstrating that the
PPA (yellow arrows) does not overlap with the
posterior part of the hippocampus (green arrows).
Posterior slices appears on the left. Talairach
coordinates of the PPA activation for this subject
are -6, 18, -39 and -6, -34, 30 (S-I, M-L, A-P).

Activation of PPA to Landmarks

LM

LS

ER

FR

OS

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 respond

during vertical plane or
inverted (upside-down)
locomotion?

HD cell responses in the Vertical Plane

Generally normal directional

responses on walls.
Cells contain directional tuning
curve relative to the room
reference frame.

Animal defines its horizontal reference frame as the plane it happens to be

locomoting in. Thus, it rotates [translates] its plane of locomotion by 90
as it moves into the vertical plane and defines this new surface as its
horizontal reference frame.
Room Reference Frame
North Wall

North Wall

90

90
90

180

0 180

180

270

270

Floor

Up

Down

East Wall

270
90

West Wall

East Wall

West Wall

180

Floor

270
90

180

0
270

South Wall

South Wall

Direction of Cell Firing Along Walls

But, what about inverted orientation?

To test it is easier to go Space-bound

Why does this matter?

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
Space Motion Sickness

Resulting in problems:
Flipping switches in wrong direction
Emergency egress
Otolith reinterpretation upon return to gravitational
environment

Visual Reorientation Illusions (VRIs)

All-of-a-sudden perception of feeling
inverted (upside-down).
Surface nearest your feet seems like a
floor. Surfaces parallel to body seem
like walls.
The orientation of your own body or
that of a person you look at
redefines down.

Probability of illusion depends on

visual vertical cues, visual attention
and your familiarity with the interior.
Occurs spontaneously, but can be
cognitively initiated and reversed
(e.g., simply closing eyes).
Incidence is almost universal.
Susceptibility persists for months.

Nexus Cube

VRIs are similar to looking at a Nexus cube, where you perception flips
back-and-forth between seeing the blocks either open towards you or
away from you.
Similarly, VRIs can come and go very quickly, where your perception of
what is down can flip back-and-forth quickly.

0-G Inversion Illusions

Less common: < 25% of crew
experience it.
Paradoxical sensation of being
continuously gravitationally upside
down, even when visually upright in
the cabin.
Persists with eyes closed.
Fluid shift, visceral elevation, and
otolith unloading likely contribute.
Temporarily reversible with
proprioceptive or visual cues.
Uncommon after flight day 2.

Extra-Vehicular Activity - EVA Height Vertigo

Viewing Earth beneath your own feet

during EVA can trigger sudden sense
of height vertigo, fear of falling, and
enhanced awareness of orbital motion.
The natural compulsion to hang on
can sometimes be disabling.
Turning away from Earth and putting
spacecraft below instead of Earth
can resolve problem.

These Illusions Lead to Space Motion Sickness

Akin to motion sickness in car or boat.
Perceived self orientation change is
not accompanied by normal confirming
semicircular canal or gravity-receptor
cues.
Multiple VRIs can cause motion sickness.
A single VRI can trigger vomiting in a
person already sick.
Examples
Seeing an inverted crewmember
floating nearby.
Viewing the Earth in an unexpected
direction.

Motion Sickness
Space motion sickness is akin to motion sickness on Earth and is similar to sea- or carsickness. It arises from a conflict between the spatial information derived from different sensory
cues - the most common of which is visual vs. vestibular.

Two different examples of sensory conflicts:

In a cabin on ship in high seas --->
Visual information says you are not moving, but the vestibular system detects the movement
of your head and says you are moving.
IMAX theatre with large screen and movie shows picture of the view from the cockpit of a
plane as it banks during a turn --->
Visual information (optic flow) says you are moving as the entire visual field moves across
your retina, but the vestibular system does not detect any movement of the head and says
you are not moving.

Problems from time in Space

Loss of muscle mass

Reduction of quick head

turns due to
Otolith Reinterpretation

Otolith Reinterpretation
Interpretation of gravity vector involving gravity + accelerative forces
Example: Pilot taking off from an aircraft carrier with high accelerative forces exerted on him.
Gravity
vector
Aligned
along
longitudinal
body
axis

Normal

Compensates by Steering
plane downwards

Acceleration
vector

Upon accelerating
during take-off

Perceived gravity vector aligned along body axis;

feels like you are tilted upwards

Adaptation to a 0-g environment and then return to Earth.

When in 0-g, astronauts learn to reinterpret otolith signal as only encoding linear movement
(compared to on Earth where it encodes the combination of gravity and linear movement).
However, upon return to Earth, for the first couple of days astronauts interpret any change in
otolith signal as only linear movement. Thus, a slight tilt of the head (which changes the gravity
vector on the otolith) is interpreted as a linear acceleration in the horizontal plane, and the

subject perceives that they are rapidly moving across the floor.

Spatial Disorientation - Difficulty in determining up/down:

Astronauts are just as likely to work upside-down as right-side up.

Disorientation in 3-D
Difficulty in drawing spatial layout and pointing to another module

On the International Space Station, nodes have 6 possible entryways.

This could be a problem for astronauts during an emergency egress.

HD cell firing in 0-g with parabolic flights

NASA KC-135 aircraft

40 parabolas; each parabola ~20 sec 0-g.

Rats monitored in 4 x 2 x 2 ft. rectangular cage with wire mesh on three
surfaces - floor, wall, ceiling.

Directional heading was hand-scored from video tapes off-line and

compared to cell activity.

Humans can
experience
VRIs during these
exercises, too.

HD cell tuning curves in 0-g conditions

HD cell tuning curves in 0-g conditions

HD cell responses when upside-down on ceiling on Earth

Similar to our wall-climbing findings, HD cells

treated the walls as though they were an extension
of the floor.

Cell fires during

climb up.

Cell fires during

climb down.

Preferred
direction
of cell.

Running in the reverse direction, the cell is silent

on both walls.

Cell
Cell
is fires
silentduring
during
climb
up.
ciimb
down.

Cell
fires
during
Cell
is silent
climbciimb
down.
during
up.

Preferred
direction
of cell.

For most cells: Loss of directional tuning on

ceiling, with increased background firing rate

Cell 1

Cell 2

With loss of HD signal when inverted:

Could animals learn a spatial task upside-down ?
Inverted Hole Board Escape Task

X = Four Release Points

+ = Center Release Point

x

Escape hole

Valerio, Clark et al. (2010) Neurobiol Learning & Memory

Performance in the Inverted Hole Board Escape Task

1 Start Point

30

Escape Latency (sec)

Escape Latency (sec)

4 Start Points
25
20
15
10
5
0

10

15

20

25

30

30
25
20
15

10
5
0
0

Training day
30

8
4

20
10

1SP

2SP

1 Start Point
2 Start Points

20
10
0

30

Latency (sec)

12

Latency (sec)

30

Latency (sec)

Number of Sessions
to Criterion

Training day
16

Criterion Center
Probe

10

20
10
0

Regular
trials

Blindfoldedto-apparatus
trials

Criterion Surround
Curtain
Probe

Blindfold prevents seeing surrounding visual cues on way to apparatus.

Curtain prevents seeing surrounding visual cues while on apparatus.

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.

Record HD cells in the

Inverted Hole Board Escape Task

X = Familiar Release Point 1

X = Familiar Release Point 2

+ = Center Release Point

Escape hole

Valerio, Clark et al. (2010) Neurobiol Learning & Memory

Trajectories
Familiar
Tests
2 Start
Points

Sample Paths

Center
Tests
W

180

180

What are Head Direction Cells doing in this Task?

Session on Floor:
Upright
Firing Rate

NW

SW
Head Direction

Rats trained from two locations

Inverted Trials

NW Inverted Trial
Correct

SW Inverted Trial
Correct

Inverted Trial: Center

Error

2nd Session on Floor:

Upright

Thus, rats were accurately performing the simple version of the inverted
spatial task - despite the absence of a HD signal.

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.

Conclusions about HD Responses in 3-D

HD cells show normal activity in the vertical plane, but not when the
animal is upside-down.
When inverted, the otolith signal to the brain is quite different and may
account for the loss of directional firing.
The absence of directional activity may bring about spatial disorientation
and its accompanying problems when in 0-g.