**2. Episodic memory**

Episodic memory has been characterized as a discrete form of memory that involves mentally re-enacting previously experienced events (Tulving 1983, 2002). Specifically, this type of memory requires the integrated recall of the "what, where and when" circumstances

Spontaneous Object Recognition in Animals: A Test of Episodic Memory 27

Clayton and Dickinson (1998) took advantage of the scrub jays' natural food-storing behaviours and allowed each bird to cache both perishable, but preferred, worms and nonperishable peanuts in opposite sides of an ice-cube tray filled with sand. Initially, the scrub jays demonstrated the ability to recall the location ("where") in which they cached each type of food ("what"), and consequently retrieved the preferred food, worms, before peanuts. In subsequent trials, the researchers replaced freshly cached worms with decayed worms if worms were cached first (124 h before retrieval) and peanuts cached second (4 h before retrieval). In contrast, fresh worms were left in their cached locations if peanuts were cached first (124 h before retrieval) and worms cached second (4 h before retrieval). Remarkably, the scrub jays quickly learned to retrieve peanuts if worms were cached first (since decayed worms are unpalatable) and to retrieve worms if peanuts were cached first. A similar result, although less compelling, was found when jays were taught that worms were removed

In numerous subsequent studies, Clayton and Dickinson further developed their case for episodic-like memory in scrub jays. Specifically, through allowing jays to cache peanuts and dog kibble and then recover these items on successive trials, they demonstrated that scrub jays update their memories about which cache sites contain food (Clayton & Dickinson, 1999). Furthermore, by making one food less preferable than another through pre-feeding, they found that jays successfully identified food caches that were both non-recovered and contained preferable food. Clayton and Dickinson (1999) argue that this ability indicates that scrub jays form episodic-like memories that integrate the type of food in a cache, the location of that cache, the last activity at that cache (recovery or caching) and how long ago food was stored. Clayton et al., (2005) have also shown that scrub jays use novel information about the decay of a food source to reverse their strategies for recovery, since jays cache more non-perishable food items if their caches are consistently degraded on recovery. Emery and Clayton (2001) found that scrub jays who have previously raided the food cache of a conspecific will re-cache food if they are observed during their own caching process. Recently, Cheke and Clayton (2011) examined caching in the Eurasian jay and demonstrated that birds distinguish between their current food preference (created by pre-feeding a specific food) and their future needs. This was evidenced by the birds overcoming motivation to cache currently desired food and instead caching currently non-preferred foods according to their future value. Taken together, these findings provide preliminary evidence that caching scrub and Eurasian jays make decisions based on past episodes and anticipated future needs. Because these results suggest that episodic-like memory includes aspects of the mental time travel involved in human episodic memory, further study in this area, including research on non-caching species, such as ant-following birds, is suggested

Many researchers have used the basic what/where/when criteria proposed by Clayton and Dickinson (1998) in their attempts to demonstrate episodic-like memory in species such as pigeons (Skov-Raquette et al., 2006), primates (Hoffman et al., 2009; Martin-Ordas et al., 2010), mice (Dere et al., 2005), and rats (Babb & Crystal, 2006; Fortin et al., 2002; Kart-Teke et al., 2006; O'Brien & Sullivan, 2007). The majority of studies have been conducted using mice

and rats, which has led to the development of several different testing paradigms.

(pilfered) if they were cached 124 h before retrieval.

(Clayton et al., 2003c; Logan et al., 2011).

**4. What/where/when memory in other species** 

of an event, the ability to recognize subjective time, and autonoetic consciousness (knowledge of self; Tulving, 1983, 2002). The main distinction between episodic memory and other forms of recall involves the recreation of a personally experienced event. Simple retrieval of discrete facts (e.g., Marconi received a wireless transmission at Signal Hill in 1901), does not require the self-consciousness nor the ability to mentally travel forward and backward in time that are indicative of episodic memory (e.g., I was on Signal Hill yesterday and read a sign about Marconi). Despite the acceptance of episodic memory in humans, its presence in non-human animals is controversial.

In the absence of a measure of consciousness in non-human animals, it has not been possible to demonstrate episodic memory that is equivalent to humans. However, by studying food caching (Clayton & Dickinson, 1998), food finding (Babb & Crystal, 2006), fear conditioning (O'Brien & Sutherland, 2007), and object exploration (Eacott & Norman, 2004), researchers claim to have demonstrated a form of episodic memory in scrub jays (Clayton & Dickinson, 1998), pigeons (Zentall et al., 2001), mice (Dere et al., 2005), rats (Eacott & Norman, 2004; O'Brien & Sutherland, 2007), gorillas (Schwartz & Evans, 2001), rhesus monkeys (Hoffman et al., 2009), and chimpanzees/bonobos (Menzel, 1999; Martin-Ordas et al., 2010).

The interpretation of such studies is often controversial because there is no consensus regarding a definition of non-human episodic memory (Hampton & Schwartz, 2004). Schwartz, Hoffman and Evans (2005) outlined five operational definitions of non-human episodic memory including: (1) the demonstration of what/where/when memory (Clayton & Dickinson, 1998; Babb & Crystal, 2006), (2) the demonstration of what/where/which memory (Eacott & Norman, 2004), (3) the demonstration of spontaneous recall (Menzel, 1999), (4) the ability to recall an event when not expecting a test (Zentall et al., 2001), and (5) the ability to report on past events over a long term (Schwartz & Evans, 2001). Unfortunately, these definitions tend to be species-specific. For example, definitions of episodic memory based on research with food-caching birds (Clayton & Dickinson, 1998) often do not fare well when applied to non-caching species (Bird et al., 2003; Hampton et al., 2005). Consequently, alternative methods and definitions have been developed for rodents, primates, and non-caching birds.
