Spatial Cognition

1. Spatial Cognition • Navigation: Finding the way to a goal • Discriminate different headings (need a sense of direction) • External directional reference: sun, magnetic field, landmarks • Internal directional reference: vestibular/inertial cues • Determine the correct heading (need a sense of position) • Path integration • Knowledge of familiar landmarks in home range • Geographical positioning system (e.g., position relative to large-scale coordinate system defined by global geophysical features)--migratory birds, whales, turtles

2. Spatial Cognition and Navigation • Navigational Processes That Use Internally Represented Spatial Knowledge • Path integration • Sun compass • Landmarks: cognitive maps

3. Path integration: a sense of position • Ants travel straight path home after circuitous outward path • We can exclude use of odor trails, visual beacons, or memory of outward path • Instead, ants compute direct homeward path based on measurements of directions and distances traveled on outward path (Wehner et al.) Food Homeward path Nest

4. Animals compute straight path home after circuitous outward path Desert ants (Cataglyphis sp.) Food Search path Homeward path Nest http://axon.bhs.mq.edu.au/PSY236/space/20path_int_error_2.jpg www.kyb.tuebingen.mpg.de/bu/poster/ 2000/b_riecke_arvo2000.pdf More on PI

5. Sun Compass and Memory in Bees The basic task http://www.scottcamazine.com/photos/ BeeBehavior/images/06waggleDance_jpg.jpg • Bees encode (allocentric?) flight direction in dances • As sun moves, dances change • Dances change even when bees can’t see sun (thus compensate by memory) • Reference for memory: landmarks (Dyer & Gould 1981; Dyer &Dickinson 1996)

6. Pigeons Budzynski, Dyer & Bingman 2000 Solar positions seen To get food in box, birds must chose correct angle relative to sun, compensated for solar movement Food Birds naïve about the morning sun can nevertheless use it correctly based to find compass directions learned in afternoon 10:00 (Test) 14:00 12:00 Celestial compasses: birds and bees • Pattern of solar movement • Non-linear over day • Varies with season and latitude • Animals learn current, local pattern of solar movement • Learning: not just a list of time-linked solar positions, but a function that can be used to find unknown positions of the sun. Training

7. Landmarks: Cognitive Maps From: Tolman, EC 1948 Cognitive maps of rats and men. Psychol Rev 40: 40-60.

8. What does it mean to have a cognitive map? • One operational definition: a representation of spatial relationships that enables computation of novel shortcuts between known locations (O'Keefe & Nadel 1978. The hippocampus as a cognitive map) • Alternative hypotheses: • Route memory (A--> B already familiar) • Recognize familiar landmarks associated with goal, even if from novel vantage point Task: get from A to B, having experienced routes to A and B separately

9. Learning local landmarks Insects can pinpoint locations they need to find again by learning arrangement of surrounding landmarks: HOW? Niko Tinbergen (1938)

10. Search distributions Enlarge three landmarks; best match is in the same place Learning local landmarks Bees match visual image learned on previous trips Find best match given all available information But bees have some flexibility in approach path. They don’t follow stereotyped route, which Gallistel takes as evidence of generalized “map” Landmark Enlarge single landmark; to match view, bees have to move back (Bartlett & Dyer in prep)

11. Then finds goal on later approach flights by moving to reduce mismatch between current and remembered images Algorithm: snapshot model Insect records image of landmarks seen at goal (after Cartwright and Collett 1983) Is this evidence for a map? Vardy www.scs.carleton.ca/~avardy/ misc/engrSeminar/engrSeminar.pd

12. Robotic simulations Source: Möller, R., Universität Bielefeld http://www.ti.uni-bielefeld.de/html/people/moeller/analog.html

13. Or this? Bartlett, Mack & Dyer (in prep) But is this really what bees do?

14. A simpler model? • Bees encode angles (and distances) of landmarks; may be encoded in egocentric, not allocentric, reference frame • Weak evidence for a highly flexible computational strategy for using landmarks to fly to goal • Nevertheless, bees do behave as if they can recognize familiar landmarks from novel vantage points • Also, bees can use familiar landmarks encountered in unexpected context

15. What does it mean to have a cognitive map? • One operational definition: a representation of spatial relationships that enables computation of novel shortcuts between known locations (O'Keefe & Nadel 1978. The hippocampus as a cognitive map) • Alternative hypotheses: • Route memory (A--> B already familiar) • Recognize familiar landmarks associated with goal, even if from novel vantage point Task: get from A to B, having experienced routes to A and B separately

16. Do insects have cognitive map or something else? From Dyer 1991

17. Varieties of cognitive maps? (Gallistel 1990) Broader Definition (Gallistel 1990): ‘A cognitive map is a record in the central nervous system of macroscopic geometric relations among surfaces in the environment used to plan movements through the environment. A central question is what type of geometric relations a map encodes’. • Specific issues: • Spatial scale (local vs. home-range) • Geometric content (metric, topological) • Reference frame (egocentric/view-dependent vs. allocentric/view-independent) • Evidence: • People: short cuts in cities and VR (errors); mixed evidence contents of underlying map • Rodents: most studies on local scale; mixed evidence on contents • Insects: on local and home-range scale--metric, egocentric

18. Insects (digger wasps, bees) Humans in corridors, cities Humans in rooms Humans in cities Varieties of cognitive maps? Type 1 Type 2 Type 3 Most rodent research • Computational models of cognitive maps: need to specify geometric contents (angles, distances, routes, nodes), reference frames, and operations performed on stored information? • Humans, but not insects, form Type 3 maps, but insects can flexibly use snapshots and route maps • Big question is whether map-learning is viewpoint-dependent or viewpoint-independent

19. CA1 Section through hippocampus http://www.sunysb.edu/biochem/BIOCHEM/facultypages/trimmer/gallery.html CA3 Toward the implementational level Is the hippocampus the locus of the cognitive map of mammals? • Some evidence: • Input from integrative sensory areas • Output to neocortex • Lesion studies suggest role in memory Rat brain

20. Maguire, E.A. 1998 Science 280: 921-924 Normal (top) and HC-lesioned brains http://www.psychol.ucl.ac.uk/kate.jeffery/C567/Lecture2_Cognitive_mapping/sld001.htm Hippocampus and spatial cognition 1. Lesion experiments (rats & birds): selective effect on spatial memory 2. Comparisons of hippocampus size: correlation between HC size and reliance on spatial memory 3. Functional neuroimaging (humans) 4. Place cells

21. Firing field of single cell (gray) and activity on two runs through the arena. Cell's activity is independent of heading. Muller, R. (1996) A quarter of a century of place cells. Neuron 17: 813-822 Ensemble of hippocampal cells "maps" space. This showsthe place fields of five simultaneously recorded units on an elevated triangular maze. The light gray trace represents the rat’s path as it traversed the maze. The dots in each color indicate the locations in which each of the five cells fired. (Best et al. 2000, Ann Rev. Neuroscience 24:459-86; data from C Barnes & B McNaughton.) Place Cells Rat with recording apparatus Rat in arena

22. Remapping of place fields of when animal goes into different environments; one cell's place fields are shown Place Cells (cont'd) Rat put in dark and then rotated slowly relative to featureless arena; causes shift in place field Conspicuous landmark is rotated, causing shift in place field Place fields are referenced to internal and external coordinates

23. Some properties of hippocampal place cells that imply role in spatial cognition • Highly stable firing fields in constant environment • Can be established in total darkness (referenced to vestibular cues) • Can be linked to visual cues, and then track visual cues • Individual cells can have different place fields in different environments • Ensemble of cells encodes map of familiar environment • BUT: there is no obvious way in which this system corresponds to computational models of cognitive map based on behavioral evidence. For example…..

24. Problems with the "hippocampus-as-cognitive-map" hypothesis • May not generalize to humans, because hippocampus is known to play role in non-spatial episodic memory in humans (but see O’Keefe) • Place cell ensemble in hippocampus is not enough to account for spatial behavior….encodes current location, but not goals, for example (Andre Fenton) • Even in animals, hippocampus is involved in non-spatial tasks (e.g., transitive inference) • Place cells seem to encode something more than just "place"

25. Rat can learn series of pairwise discriminations • Rat can perform transitive inference, but not if hippocampus is damaged Normal rats HC-damaged Eichenbaum, H 1999 Behav Brain Res 103: 123-133 Transitive inference: non-spatial function of hippocampus in rats • Rat chooses one odor over another IF: A > B > C > D > E, then…. A > C (or D or E); B > D (or E)

26. Place cells encode more than just place:role for hippocampus in episodic memory? Rats are trained on alternating T-maze Wood ER, Dudchenko PA, Robitsek RJ, Eichenbaum H: Hippocampal neurons encode information about different types of memory episodes occurring in the same location. Neuron 2000; 27: 623-633

27. A cell that fires in different locations when a right turn is coming up than when a left turn is coming up Context-specific activity of place cells A cell that fires in a particular place, but much more rapidly when a right turn is coming up Wood ER, Dudchenko PA, Robitsek RJ, Eichenbaum H: Hippocampal neurons encode information about different types of memory episodes occurring in the same location. Neuron 2000; 27: 623-633

28. Worms Degrade Birds are allowed to hide food (waxworms and nuts) in two caching bouts. In recovering it they can choose based on what they cached and when, and their knowledge of what happens to each food type over time. Worms Stay Tasty Worms Disappear Episodic Memory in Animals? Episodic Memory in Birds: where did I put that worm and when did I put it there? http://freespace.virgin.net/cliff.buckton/Birding/California/Calif17.jpg Clayton & Dickinson 1998

29. Interpretations for role of hippocampus in spatial cognition and memory generally • Spatial and non-spatial episodic memories involve different processes; hippocampus does them both, and has evolved to become more specialized for episodic memory in primates compared with rodents (Jacobs & Schwenk) • All experience has a spatial component, and hippocampus participates in formation/use of episodic memory because of its role in processing spatial information processing (O'Keefe) • Spatial cognition involves processes that are also required in encoding certain other kinds of relations among stimuli; hippocampus plays a more general role that leads it to participate in spatial as well as certain non-spatial tasks (Eichenbaum)

30. Where does this leave the search for neural implementation of cognitive map? • Hypotheses • Hippocampus is the cognitive map (O’Keefe) • Cognitive map (sensu Tolman and O'Keefe & Nadel) is elsewhere, but uses output from hippocampus • Cognitive map is indeed an important function of hippocampus, but computations that hippocampus carries out are very different from those developed on the basis of behavioral observations; these computations support functions other than spatial encoding (Eichenbaum and colleagues)