The evolution of episodic memory

Abstract

One prominent view holds that episodic memory emerged recently in humans and lacks a "(neo)Darwinian evolution" [Tulving E (2002) Annu Rev Psychol 53:1-25]. Here, we review evidence supporting the alternative perspective that episodic memory has a long evolutionary history. We show that fundamental features of episodic memory capacity are present in mammals and birds and that the major brain regions responsible for episodic memory in humans have anatomical and functional homologs in other species. We propose that episodic memory capacity depends on a fundamental neural circuit that is similar across mammalian and avian species, suggesting that protoepisodic memory systems exist across amniotes and, possibly, all vertebrates. The implication is that episodic memory in diverse species may primarily be due to a shared underlying neural ancestry, rather than the result of evolutionary convergence. We also discuss potential advantages that episodic memory may offer, as well as species-specific divergences that have developed on top of the fundamental episodic memory architecture. We conclude by identifying possible time points for the emergence of episodic memory in evolution, to help guide further research in this area.

Keywords: animal models; entorhinal cortex; hippocampus; parahippocampal region; prefrontal cortex.

Fig. 1.

Brain regions important for episodic memory. Anatomical comparison of the hippocampus (avian hippocampus), parahippocampal region (avian area parahippocampalis), associational neocortex (avian dorsal ventricular ridge), and prefrontal cortex (avian nidopallium caudolaterale). The mammalian hippocampus shows distinct subregions, which are less evident in the avian hippocampus. The mammalian parahippocampal region is shown in diagrams (adapted with permission from ref. 81. Copyright Wiley-Liss, Inc.) to highlight the conserved relative spatial locations among species, with similar adjacent locations of area parahippocampalis and hippocampus in birds. Neocortical areas in mammals and associational areas of the dorsal ventricular ridge are outlined. The prefrontal cortex is shown in whole brains in mammals (medial surface in rat) and in a sagittal section in the bird. Human, nonhuman primate (Macaca mulatta) and rodent (Rattus norvegicus) sections were adapted with permission from http://www.brains.rad.msu.edu, and www.brainmuseum.org supported by the US National Science Foundation, and bird (Taeniopygia guttata) sections from http://zebrafinch.brainarchitecture.org. DG, dentate gyrus; DL, dorsolateral region; DM, dorsomedial region; EC, entorhinal cortex, HC, hippocampus; PER, perirhinal cortex; PHC, parahippocampal cortex; POR, postrhinal cortex; Tr, triangular region; V, V-shaped layer.

Fig. 2.

Neural circuits underlying episodic memory capacity in mammalian and avian species. (A) Schematic diagram of neural mechanisms supporting episodic memory encoding and expression in mammals. After information from the environment reaches the neocortex, the processing of “what” and “where” information is divided in parallel streams of cortical association areas. This functional segregation is maintained in the parahippocampal region, where the information is further processed before it reaches the hippocampus. Episodic memories are formed when the hippocampus integrates information about a specific event (what happened) with the context in which it occurred (e.g., where and/or when it happened). Although what-where coding has been shown in regions CA3 and CA1, lesion studies suggest that this type of integration depends specifically on region CA3. Recent evidence suggests that region CA1 provides an internal representation of elapsed time (when), which could support the formation of what-when and what-where-when associations. Episodic recall is thought to occur when the integrated event-in-context representation is reactivated in the hippocampal network, which leads to the reactivation of the associated representations in parahippocampal and neocortical association areas. The process by which the retrieved memories can guide behavior depends on the prefrontal cortex. (B) Comparable circuit in the avian brain. (C) Fundamental circuit hypothesized to support episodic memory across species. Anatomical, behavioral, and physiological evidence demonstrate that this system involves homologous and analogous structures. DG, dentate gyrus; DL, dorsolateral region; DM, dorsomedial region (lateral and medial); DVR, dorsal ventricular ridge; LEC, lateral entorhinal cortex; MEC, medial entorhinal cortex; PER, perirhinal cortex; PHC, parahippocampal cortex; POR, postrhinal cortex; Sub, subiculum; Tr, triangular region; V, V-shaped layer.

Fig. 3.

Possible time points for the emergence of episodic memory in evolution. Initially, the role of hippocampus was likely limited to the processing of spatial information (where). We hypothesize that episodic memory capacity emerged later on, when the hippocampus began supporting the integration of information about events in context (e.g., “what”, “where,” and/or “when” information). The striking behavioral and neurobiological similarities reviewed in this paper suggest that episodic memory capacity emerged before mammals and reptiles diverged (possibility 1). However, additional evidence from birds and reptiles is needed before the alternative hypothesis that episodic memory is the result of convergent evolution (e.g., possibilities 2 and 3) can be safely rejected.