spatial cells in the hippocampal formation - nobel …...locations same place 10 place fields...
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Spatial Cells in the Hippocampal Formation
John O’Keefe University College London
Nobel Prize Lecture Stockholm 7 December 2014
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1926-2008 Suzanne Corkin
“… He … cannot recall anything that relied on personal experience, such as a specific Christmas gift this father had given him. He retained only the gist of personally experienced events, plain facts but no recollection of specific episodes.” Corkin, p 219
Brenda Milner
Henry Molaison
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J Lichtman, J Sanes et al
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The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat O’Keefe & Dostrovsky 1971
“These findings suggest that the hippocampus provides the rest of the brain with a spatial reference map. Deprived of this map.... it could not learn to go from where it happened to be in the environment to a particular place independently of any particular route (as in Tolman's experiments )….” p174-5
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COGNITIVE MAPS IN RATS AND MEN E. C. Tolman 1948 “We believe that in the course of learning, something like a field map of the environment gets established in the rat's brain… The stimuli … are usually worked over ... into a tentative, cognitive-like map of the environment. And it is this tentative map, indicating routes and paths and environmental relationships, which finally determines what responses, if any, the animal will finally release.” p192
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Each place cell receives two different inputs, one conveying information about a large number of environmental stimuli or events, and the other from a navigational system which calculates where an animal is in an environment independently of the stimuli impinging on it at that moment…….. When an animal had located itself in an environment (using environmental stimuli) the hippocampus could calculate subsequent positions in that environment on the basis of how far and in what direction the animal had moved in the interim….. O’Keefe 1976
A B
C
AB
AC CB
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www.cognitivemap.net
Existence of hippocampal signals coding direction, distance and speed of movement Deficits in place learning, navigation, and exploration
SPACE plays a role in all our behaviour. We live in it, move through it, explore it, defend it. We find it easy enough to point to bits of it:
the room, the mantle of the heavens, the gap between two fingers, the place left behind when the piano finally gets moved.
O’Keefe & Nadel 1978
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Richard Morris
Morris, RGM, Garrud, P, Rawlins, JNP & O’Keefe, J Nature (1982)
Morris Water Maze
Richard Morris
A B
C
AB
AC CB
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Bruce McNaughton
Carol Barnes
Firing Rate
Running Speed in Meters
Place Cell Firing Rate Modulated with Speed
1983
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Grid cells
Head Direction Cells
Place cells
Spatial cells in the hippocampal formation Boundary cells
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Place Cell
Usually only one field- omnidirectional
Omni Directional in open environments
O’Keefe & Dostrovsky 1971, O’Keefe 1976
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Place cells and cognitive maps
Different cells become active in different places
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3.4
Place cells differentiate between 2 environments
Circle only
Square only
Different locations
Same place
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10 place fields
3-Dimensional Place Fields
Yartsev & Ulanovsky Science 2013
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Temporal Coding of Location
Gyuri Buzsaki
O’Keefe and Recce 1993 Mike Recce
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Some Place Fields scale with the Distance between Sides of the Box
O’Keefe & Burgess 1996
Boundary Cells provide the Environmental Inputs
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Boundary Cells: Theory
Hartley et al 2000
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Boundary Cells in the Subiculum
Lever et al (2009); Solstad et al (2008)
Colin Lever
Boundary cells
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Head Direction Cell Head Direction Cells
Taube, Muller & Ranck 1990
Jim Ranck
Head Direction Cells
Bob Muller
Jeff Taube
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How is distance measured?
Roy Lichenstein
Wm Blake
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Firing fields lay out a regular series of equally- spaced fields in every familiar environment
Grid Cells: the universal metric in the entorhinal cortex?
Grid Cells May-Britt & Edvard Moser
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Grid Cell
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Grid Spacings are Quantised
Stensola et al Nature 2013
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Grid cells Place Cell
Grid Fields can add to produce a Place Cell Field
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Roy Lichenstein
Relationship between Grids and Stripes
Burgess, Barry & O’Keefe Hippocampus 2007
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Band-like Cells in the Parasubiculum
Krupic, Burgess & O’Keefe Science 2012
Julija Krupic Barry
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Grid & Spatially Periodic Non-grid cells
Head Direction Cells
Place cells
Spatial cells in the hippocampal formation Boundary Vector cells
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'Space is nothing but the form of all appearances of outer sense….. can be given prior to all actual perceptions, and so exist in the mind a priori, and …. can contain, prior to all experience, principles which determine the relations of these objects' (Critique of Pure Reason, p. 71).
Kant:
As it is this neo-Kantian position which we shall be adopting in this book, it is worth restating two main features of the argument: 1. Three-dimensional Euclidean space is a form imposed on experience by the mind. 2. This unitary framework, conveying the notion of an all-embracing, continuous space, is a prerequisite to the experiencing of objects and their motions. O’Keefe and Nadel 1978 p 23-4
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Wills, Cacucci, Burgess & O’Keefe Science 2010, Hui Min Tan et al unpublished; Langston, Ainge et al Science 2010
Ontogeny of spatial cells
Tom Wills Hui Min Tan
Francesca Cacucci
Eyes open Leave nest
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Grid Cells
Place cells
Grid cells and Boundary Vector cells may provide 2 independent pathways into Place Representations
Boundary Vector cells
Head Direction Cells
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Virtual Reality environment
Harvey et al, 2009; Hölscher et al, 2005; Chen, King, Burgess & O’Keefe 2013
Guifen Chen John King
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Control by visual cues on the side wall
X
25 % Fields maintained in passive probe
80 % Fields disrupted by cue removal
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Path integration (light off trial)
49% maintain fields in lights off PI trials
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The Virtual Town
70 x 70 meters
Neil Burgess
Eleanor Maguire
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Maguire, Burgess, Donnett, Frackowiak, Frith, & O’Keefe. Science 1998
Hippocampal Activation in Map-Based navigation
60
80
100
120
140
160
60 64 68 72 76 80
3 Paths to goal
Acc
urac
y
Bloodflow
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Maguire et al. (2000) PNAS
RH LH
Posterior Hippocampus is LARGER in taxicab drivers and increases with experience
-6
-4
-2
0
2
4
6 0 50 100 150 200 250 300 350 400
time as taxi driver (months)
adju
sted
VB
M re
spon
ses
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ior h
ippo
cam
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Summary The Hippocampal Formation provides a cognitive map of a familiar environment which can be used to identify the animal’s current location and to navigate from one place to another. The Mapping system provides 2 independent strategies for locating places, one based on environmental landmarks and the other on a path integration system which uses information about distances travelled in particular directions. A similar spatial system exists in humans which additionally provides the basis for human episodic memory
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EU F7 SpaceBrain SainsburyWellcome Centre