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

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

Path integration: a sense of position Nest Food Homeward path 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.)

More on PI /b_riecke_arvo2000.pdf Desert ants (Cataglyphis sp.) Nest Food Homeward path Search path Animals compute straight path home after circuitous outward path

BeeBehavior/images/06waggleDance_jpg.jpg Sun Compass and Memory in Bees 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) The basic task

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. Pigeons Budzynski, Dyer & Bingman 2000 To get food in box, birds must chose correct angle relative to sun, compensated for solar movement 10:00 (Test) Training 12:00 14:00 Food Solar positions seen Birds naïve about the morning sun can nevertheless use it correctly based to find compass directions learned in afternoon

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

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 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

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

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

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

Robotic simulations Source: Möller, R., Universität Bielefeld

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

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

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 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

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

Varieties of cognitive maps? (Gallistel 1990) 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 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’.

Varieties of cognitive maps? Most rodent research Humans in cities Humans in corridors, cities Humans in rooms Insects (digger wasps, bees) 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 Type 1Type 2 Type 3

Toward the implementational level Rat brain Section through hippocampus Some evidence: Input from integrative sensory areas Output to neocortex Lesion studies suggest role in memory Is the hippocampus the locus of the cognitive map of mammals? CA1 CA3

Hippocampus and spatial cognition 1. Lesion experiments (rats & birds): selective effect on spatial memory 4. Place cells 2. Comparisons of hippocampus size: correlation between HC size and reliance on spatial memory Normal (top) and HC- lesioned brains 67/Lecture2_Cognitive_mapping/sld001.htm Maguire, E.A Science 280: Functional neuroimaging (humans)

Place Cells Ensemble of hippocampal cells "maps" space. This shows the 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.) Rat with recording apparatus Rat in arena 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:

Place Cells (cont'd) Remapping of place fields of when animal goes into different environments; one cell's place fields are shown 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

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…..

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"

Transitive inference: non-spatial function of hippocampus in rats Rat chooses one odor over another 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: IF: A > B > C > D > E, then…. A > C (or D or E); B > D (or E)

Place cells encode more than just place: role for hippocampus in episodic memory? 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: Rats are trained on alternating T-maze

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:

Episodic Memory in Animals? Episodic Memory in Birds: where did I put that worm and when did I put it there? on/Birding/California/Calif17.jpg Clayton & Dickinson 1998 Worms Degrade Worms Stay Tasty Worms Disappear 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.

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)

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)