ReviewTen years of research into avian models of episodic-like memory and its implications for developmental and comparative cognition
Research highlights
▶ Western scrub-jays are capable of episodic-like memory, in that they recall what happened, when and where, in an integrated representation, that can also be used flexibly to update these memories when new information becomes available after the initial information was encoded. ▶ Magpies and black-capped chickadees have been shown to possess what-where-when memories, and future work should test whether the birds’ memories for what happened where and when is stored as an integrated representation, and its capacity to be flexibly deployed. ▶ Studies using non-verbal tasks can address the question of whether children under the age of four are incapable of episodic recall or they simply cannot share their episodic memories in the absence of language. Furthermore, the relationship between episodic-like memory and episodic memory can be inferred by studying the relative timing at which such memories develop in young children. ▶ Birds are a highly promising biomedical model to study episodic-like memory and episodic recall with the respective underlying brain areas due to functional as well as some mechanistic similarities between the avian and mammalian hippocampus.
Introduction
It was in 1972 that Endel Tulving first coined the term ‘episodic memory’ to describe our ability to remember specific events or episodes that happened in our personal past, in contrast to the ability to simply acquire knowledge about the world. To do so he described episodic memory in the information processing terms which were common at that time:
“Episodic memory is an information processing system that a) receives and stores information about temporally dated episodes or events, and about temporal-spatial relations among these events, b) retains various aspects of this information, and c) upon instruction transmits specific retained information to other systems, including those responsible for translating it into behavior and conscious awareness.” [1, p. 385]
Since the time of its introduction the concept of episodic memory has changed considerably. According to Tulving, the major transition in his concept of episodic memory was the “shift from the general idea of “consciousness” that applied to both episodic and semantic memory in 1972 to “autonoetic consciousness” in 1999” [2], namely that “Memory requires more than mere dating of the fact in the past. It must be dated in my past.” [3].
When Clayton and Dickinson [4] started their pioneering work with Western scrub-jays (Aphelocoma californica), they argued that there are no agreed behavioural markers of consciousness in non-linguistic animals, and consequently it is not possible to empirically evaluate the autonoetic component of episodic memory in animals, or pre-verbal children for that matter. Therefore they returned to Tulving's original description of episodic memory [1] to ask whether the birds could remember what, where and when of specific past caching episodes, focusing on Tulving's original description for a memory that “receives and stores temporally dated episodes or events, and about temporal-spatial relations among these events” [[1], p. 385]. They termed this ability ‘episodic-like’ memory to make a distinction between the behavioural and phenomenological criteria for episodic memory, given that the phenomenological aspects that usually accompany conscious recollection in humans are impossible to assess in non-human animals and pre-verbal children.
Their seminal paper on episodic-like memory in Western scrub-jays [4] has inspired a number of studies in a wide range of species over the past 10 years, from primates and rodents to pigeons and passerine birds. The mammalian studies will be discussed elsewhere in this issue [5], [6], [7]. Here we shall first review avian studies of what-where-when memory, namely in the Western scrub-jays mentioned above [[4], for recent reviews see [8], [9]], and subsequent work in other species of bird, from a fellow corvid, the magpie [10], and another food-hoarding species, the black-capped chickadee [11]. We shall then describe studies on domestic pigeons and present an alternative approach for studying what-where-when memory [12], [13], [14]. We will close this section with a discussion of the various approaches to study episodic-like memory. In the second section we suggest that the non-verbal caching and item finding paradigm is an ideal task to study the development of episodic-memory in pre-verbal children. In the final section we want to draw attention to topics where we believe the bird model could prove highly valuable, namely as a biomedical model system to better understand the neural basis of episodic memory.
Section snippets
Review episodic memory in birds
Episodic memory is the only memory to be oriented in time [15], and more precisely in subjective time. Since the “subjective experience of having a past event from one's life projected into the present is not just an additional criterion for defining episodic memory” [[16], p. 566] but critical for the concept of episodic memory, it is essential to demonstrate in animals that they remember when a particular event occurred in the past as well as what happened where on the basis of a single past
Developmental models for pre-verbal children
Adult humans, with proficient language skills, can report on their memories and mental states, while infants cannot. Babies start without language, and from birth to year one, language comprehension (understanding of language) develops before language production with about a 5 month delay in between the two. Furthermore each of the four main components of language (i.e. phonology, semantics, grammar, and pragmatics) has its own developmental periods [73]. Since babies and toddlers understand
Birds as biomedical model for studying the neural basis of episodic memory
When combining recent advances in avian neuroscience with a neuro-ethological approach [93] as outlined for food-caching species the study of birds can critically facilitate insights into brain function and underlying development and maintenance of cognition in general and episodic memory in particular. In the remaining section we shall – only very briefly – exemplify the new understanding of the avian brain, and sketch selected similarities between the avian hippocampus and the human
Final remarks
Western scrub-jays have been shown to be a promising species for investigating complex cognitive capacities. The focus of this review paper was on episodic-like memory, and we have summarised numerous studies that establish beyond doubts that scrub-jays are capable of episodic-like memory. In the 10 years since the first publication by Clayton and co-workers a few other bird species have been shown to be capable of a what-where-when memory (the content criterion), but these studies are only in
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