1. Food Storing Birds and Episodic Memory

2. Controversy over studies of comparative cognition Recent research showing human-like abilities in other species: – There is a tendency to use anthropomorphic interpretations for episodic memory Timing manufacture and use of tools – Clever appearing behavior can be explained by simple mechanisms Simple associative mechanisms Simple innate mechanisms – Keeping Humans and Non-human animals separated Non-human animals do not have minds They are not conscious decision makers Provides a clear separation between humans and other animals

3. Food caching and recovery Foraging behavior Food Caching is storing food when there is an abundance to be recovered later when there is less food available Common in some mammals such as squirrels and bird species such as Clark's Nutcracker, Jays and Chickadees Caching and recovery of food is related to the ecosystem – Chickadees – store several hundred food items and recover them in a few days. – More caching in Alaska then in Colorado Recovery of cached food requires spatial memory and species that specialize in caching food have better spatial memory then those that do not cache food So Spatial Memory is important in the wild for recovery of food previously stored

4. Food caching and recovery Clark’s nutcracker – – Part of Corvidae “crow family” which includes the crows, ravens, rooks, jackdaws, jays, magpies, treepies, choughs, and nutcrackers – diet the seeds of pines also includes a wide range of insect prey, berries and other fruits, – Average caches of 4 or 5 seeds usually in the ground – stores up to 33,000 seeds in late summer and autumn and recovers several thousand in the winter. Recovery rates of 50 -60%. – Online book chapter Linking Life Zones, Life History Traits, Ecology, and Spatial Cognition in Four Allopatric Southwestern Seed Caching Corvids Russell P. Balda & Alan C. Kamil Linking Life Zones, Life History Traits, Ecology, and Spatial Cognition in Four Allopatric Southwestern Seed Caching Corvids Russell P. Balda & Alan C. Kamil

5. Food caching and recovery Western Scrub-Jays are also part of Corvidae “crow family” Lower altitude western North American mountains nonmigratory feed on small animals, eggs, insects, and (particularly in winter) grains, nuts, and berries. Use caching all year round Caches both perishable worms and nonperishable seeds Can be habituated to eat from peoples hands Easy to work with in the lab setting

6. Spatial Memory in Food Caching and Recovery Spatial memory used in recovery of cached food can be studied in the laboratory Some of this research is similar to that studied with 8-Arm Radial maze Research has focused on how they remember the food locations – A. spatial memory for cache location: evidence from field and lab studies – B. random searching among possible cache sites: no evidence – C. specific favored locations for storing: do have some preference for hear large objects but this does not explain recovery rates (50-60%) random searching near large objects by birds that did not place the cache only recover a few percent – D. mark cache sites in some way: no evidence – E. ability to smell or see the stored food: no evidence Food Hoarding in Animals By Stephen B. Vander Wall 1990

7. Kamil & Balda (1985) Study with Clark’s Nutcracker 180 sand cups – 18 open for caching 4 successive recovery sessions - 10 days after seeds had been stored by nutcrackers All 180 sites available – recovery accuracy was above chance Figure 12.1 How do we know they were not using smell of food at the location? Run controls in which food is removed before the test session

8. FIGURE 12.1 Left panel: Floor plan of the apparatus used by Kamil and Balda (1985) to test the spatial memory of Clark’s nutcrackers. Filled circles represent sand cups. Other symbols represent rocks, logs, and a feeder in the middle. Right panel: Recovery accuracy, compared to chance, during four successive recovery sessions started 10 days after the birds stored pine seeds (after Kamil & Balda, 1985). The Principles of Learning and Behavior, 7e by Michael Domjan Copyright © 2015 Wadsworth Publishing, a division of Cengage Learning. All rights reserved.

9. Comparisons of food caching and non caching species Olson (1991) – Compare Nutcrackers, scrub jays, pigeons – Spatial nonmatching to position – better retention for nutcrackers than scrub jays or pigeons Kamil, Balda, & Olson (1994) – 4 species of jays: nutcrackers, pinyon, scrub and Mexican jays – Nutcrackers showed better retention of hidden seed locations than the other jays Olson, Kamil, Balda, & Nims (1995) – 4 species of jays: nutcrackers, pinyon, scrub and Mexican jays – Using color nonmatching to sample – no retention differences Superior spatial memory but not a generally superior memory – evolved superior spatial memory as an adaptive specialization

10. Episodic Memory in Food Caching and Recovery Memory for a specific event or episode such as getting hit by a car while crossing the street Remembering: What, Where and When (WWW) of the episode Tulving claims episodic is only fully present in humans – Must have an “autonoetic” sense of self to be episodic – Domjan refers to this as the phenomenological aspect of episodic links between the ability to construct episodes of the past and imagine potential future episodes human episodic memory is not defined as WWW information – can report WWW information from history (the shooting of Abraham Lincoln) without being able to mentally relive the events – Memory retrieval produces reconsolidation so WWW information for an event you have experienced could be factually

11. Episodic Memory in Food Caching and Recovery Scrub jays Studied by Clayton & Dickinson in (1999) Scrub jays prefer worms to peanuts General Method for deteriorate study – Give jays practice caching worms and peanuts in ice cube trays – Figure 12.2 Figure 12.2 – Cache either worms or peanuts – Delay of either 4 or 124 hours before recovery – Figure 12.3 Figure 12.3

12. The Principles of Learning and Behavior, 7e by Michael Domjan Copyright © 2015 Wadsworth Publishing, a division of Cengage Learning. All rights reserved.

13. FIGURE 12.3 Procedure used to train scrub jays to remember what, where, and when they stored worms and peanuts (based on Clayton & Dickinson, 1999). The Principles of Learning and Behavior, 7e by Michael Domjan Copyright © 2015 Wadsworth Publishing, a division of Cengage Learning. All rights reserved.

14. Episodic Memory in Food Caching and Recovery Worms decay after 124 hours but not 4 hours, peanuts are always ok At the 4 hour recovery they preferred the worms At the 124 hour recovery they preferred the peanuts General methods for replenish study – same as deteriorate study except – worms were always replenished with fresh worms for recovery they preferred worms at both recovery times Figure 12.4 Jays learn that worms will deteriorate with long but not short recovery periods

15. FIGURE 12.4 Searching for worms versus peanuts in scrub jays that previously learned that worms deteriorate with time (deteriorate group, left panel) and scrub jays for which worms were always replenished during training (replenish group, right panel). The choice tests were conducted 4 or 124 hours after the caching of worms (based on Clayton & Dickinson, 199). The Principles of Learning and Behavior, 7e by Michael Domjan Copyright © 2015 Wadsworth Publishing, a division of Cengage Learning. All rights reserved.

16. Mental Time Travel (MTT) MTT is reliving past events and entertaining possible future scenarios. Requires Episodic Memory abilities – Tulving defined Episodic memory as a type of information (what, where and when) stored with an emphasis on “autonoetic” (self-knowing) consciousness. – Autonoetic consciousness is the subjective (recollective) experience associated with travelling back to a point in time and re-experiencing a past event. Clayton and colleagues cautiously refer to ‘episodic-like’ memory – because the phenomenological experience defined by Tulving – autonoetic consciousness – could not readily be shown to exist. – It is implied that jays use what, where, when information – it is not implied that their memory retrieval is anything like remembering past episodes. – nonhuman animals using autonoetic consciousness is an open question that researchers have not yet been able to effectively test

17. Foresight in nonhuman animals – Nonhuman animals have a number of mechanisms that give them capabilities for dealing with future events – some of these are seasonal adaptations such as migration or seasonal reproduction these systems are not flexible they are triggered by changes in the light cycle – simple associative conditioning produces expectations of getting food the expectations may not have much detail of WWW information – episodic memory is the most flexible in that it contains W WW information that can be projected into the future to obtain goals Humans have a large episodic memory capacity – can contain a large amount of information including subjective sense of self projected into the future – it is not clear how much capacity for this nonhuman animals have Mental Time Travel (MTT)

18. Recent studies on What Where When “WWW memory” – Clayton & Dickinson (1999) results have been difficult to replicate in other non-human animals such as rats, chimpanzees and other primates Seem to have most difficulty with when component – WWW memory should work together as an integrated unit – whether the “when” represents “how long since food was found” – which is mental travel into the past but not the future Recent study with rats on an 8-arm radial maze produced similar results to Clayton & Dickinson (1999) Mental Time Travel (MTT)

19. Episodic memory studies extended to rats (Crystal 2009) rats were required to enter four runways that contained food on a radial maze – Three runways contained standard rat-chow flavored reward pellets – fourth runway contained a highly valued reward of chocolate-flavored pellet – rats waited during a retention interval, after which the trial continued in a test phase with all eight doors open – After a short retention interval, only the previously inaccessible runways contained chow pellets in the test phase – In the test phase after a long retention interval, the previously inaccessible runways contained chow pellets – the arm on which they had found chocolate earlier now contained chocolate again – rats learned to revisit the chocolate location more frequently after long than after short retention intervals – suggests that they learned that chocolate-locations replenish after the long, but not after the short, delay Mental Time Travel (MTT)

20. Food specific satiety experiment with Scrub Jays – Correia, Dickinson, Clayton 2007 – the birds were given either pine seeds or kibbles to eat for 3 hr – immediately afterward a 10 min preference test in which both food types were available for eating and caching. – 30 min later a second period of feeding on one of the two food types for 3 hr – followed immediately by the opportunity to recover the caches they had made for 10 min – Weak evidence Stored only around one item per cache with little difference in satiated food Stopped caching one of the food items – Requires better procedures to test the satiety effect

21. MMT in Primates Roberts (2006) squirrel monkeys anticipation of thirst – a choice between 1 and 4 pieces of dates – 4 pieces followed by water for 3 hours later – 1 piece followed by water half an hour later – After several experiences preferred the 1 piece over the 4 pieces – Was not replicated in a study using Rhesus monkeys unless the delay was dropped – Delay of gratification which is short in nonhuman animals chimpanzees waited for up to 8min to receive a reward that was 40 times larger than the other reward Mulcahy and Call (2006) Tool Use in Great Apes – trained 3 bonobos and 3 orangutans to use a tool to obtain a food reward The tool and distracter items were present in the room they could take these objects with them when they went into a waiting room half of the time they carried the target tool to the waiting room Returned later to use the tool to get food Mental Time Travel (MTT)

22. MMT in Primates Dufour and Sterck (2008) – They trained 10 chimpanzees to exchange a token for a food reward over 20 consecutive days to clearly establish the relationship. – Subjects were then given the opportunity to collect the tokens in anticipation of an exchange session an hour later – did not collect and bring the token to the test compartment for the exchange any more than any of the distracter items that were available. Mental Time Travel (MTT)

23. Research should consider the following four criteria in designing future studies – use of single trials avoids repeated exposure to the same stimulus-reward sequence which can produce simple associative conditioning – use of novel problems avoids innate response tendencies avoids individual learning histories – use of clear temporal–spatial separation To ensure use of long-term memory To prevent spatial cueing – use problems from a range of domains demonstrate the flexibility of foresight Demonstrate that the behavior is not innate behavior patterns Mental Time Travel (MTT)