Search tips
Search criteria 


Logo of nihpaAbout Author manuscriptsSubmit a manuscriptHHS Public Access; Author Manuscript; Accepted for publication in peer reviewed journal;
Int J Behav Dev. Author manuscript; available in PMC 2016 July 1.
Published in final edited form as:
PMCID: PMC4562770

The development of hippocampal-dependent memory functions: Theoretical comments on Jabès and Nelson review (2015)


Studies investigating the development of memory processes and their neural substrates have flourished over the last two decades. The review by Jabès and Nelson (2015) adds an important piece to our understanding of the maturation of different elements and circuits within the hippocampal system and their association with the progressive development of hippocampal-dependent memory processes in humans. In this accompanying commentary, we explore some additional connections between the nonhuman primate work and the human data, and take the opportunity to highlight some common and additional interpretations of the results. This commentary makes three points: (1) the recognition processes present in the first few days of life may be linked to the early maturation of the medial temporal cortical areas instead of, or in addition to, the early maturation of the subiculum; (2) recent findings on the differential protracted maturation of spatial relational memory processes in monkeys further support the notion proposed by Jabès and Nelson that this protracted development may reflect progressive maturation of the CA1 field of the hippocampus followed by further maturation of CA3/dentate gyrus; (3) finally, further considerations of the differential maturation of the longitudinal hippocampal axis and of the diencephalon are proposed as additional contributors to the refinement of episodic memory functions during development.

Keywords: incidental recognition, relational memory, medial temporal lobe, Macaca mulatta, longitudinal hippocampal axis, thalamus

There has been a great deal of progress in the last half century in our understanding of the neural substrates involved in memory processing in humans and animals. Through the course of examining patients with damage restricted to the medial temporal lobe region, such as H.M. (Corkin, Amaral, Gonzalez, Johnson, & Hyman, 1997; Scoville & Milner, 1957), as well as more recent animal models with rodents (Eichenbaum, 1992, 2003) and nonhuman primates (Alvarado & Bachevalier, 2008; Meunier & Bachevalier, 2010), memory processes have classically been divided into two major types: procedural and declarative memory (Squire, 1992; Tulving, 1972). Thus, human temporal lobe amnesia severely and selectively disrupts declarative memory and leads in most patients to dense impairments in both recall and recognition tasks, while sparing procedural memory.

The accumulating evidence that these two memory systems do indeed exist elicited renewed interest to investigate their ontogenetic development. Thus, using behavioral tasks that are known to be selectively sensitive (or not) to hippocampal damage in adults, studies in rodents (Rudy et al., 1987; Green & Stanton, 1989), monkeys (Bachevalier & Mishkin, 1984; Mahut & Moss, 1986), and humans (Diamond, 1990; Overman et al., 1992) have suggested that the two memory systems are developmentally dissociable with the procedural memory system emerging earlier in ontogeny than the declarative memory system. In reviewing these earlier findings, Nelson (1995) concluded that the procedural memory system preserved in amnesic subjects with hippocampal lesions is present early in life and suggested an early maturation of brain structures mediating this function, namely the striatum and cerebellum. By contrast, the declarative memory system impaired in amnesic subjects develops later in infancy and appears to have memory processes emerging early in infancy that were labelled as “pre-explicit” memory (Nelson, 1995), whereas other “more sophisticated forms” of declarative memory became apparent later in childhood and early adolescence. At the time, the author proposed that this progressive postnatal maturation of declarative memory processes reflected the progressive development of the hippocampus and its connectional system with medial temporal lobe cortical areas as well as the prefrontal cortex. In light of critical observations on the anatomical and functional organization of the different components of the hippocampal system as well as of the flow of information coursing through this system during the last 20 years (Lavenex & Amaral, 2000), in the present review Jabès and Nelson (2015) reexamine recent results on the ontogeny of declarative memory processes and attempt to link the progressive maturation of these different processes to progressive maturation of distinct elements and circuits within the hippocampal system. Despite the inherent difficulty in correlating maturation of specific hippocampal circuits with emergence of specific memory processes, the authors demonstrate that the early emergence of incidental recognition memory processes (in the first days of life) appears to be associated with an early maturation of the subiculum, whereas other relational memory processes progressively emerge during the first decade of life in humans. Within these protracted relational memory processes, spatial and non-spatial relation memory becomes apparent within the 1–2 years of life and is linked with the progressive maturation during this period of the CA1 circuitry, followed by that of the CA3 and dentate gyrus circuits. Finally, episodic memory (the memory for specific events), which represents the latest emerging hippocampal-dependent function, may be linked to the continuous arrival of new granule cells within the dentate gyrus. This commentary makes three points: (1) the recognition processes present in the first few days of life may be linked to the early maturation of the medial temporal cortex instead of, or in addition to, the early maturation of the subiculum; (2) recent findings on the differential protracted maturation of spatial relational memory processes in monkeys further support the notion proposed by Jabès and Nelson that this protracted development may reflect progressive maturation of the CA1 field of the hippocampus followed by further maturation of CA3/dentate gyrus; (3) finally, further considerations of the differential maturation of the longitudinal hippocampal axis and of the diencephalon are proposed as additional contributors to the refinement of episodic memory functions during development.

Early developing recognition memory processes

Recent longitudinal studies of recognition memory in monkeys have led to important information on our understanding of the role of the hippocampus in incidental memory processes measured by visual paired-comparison (VPC) task. This task measures the ability of subjects to look longer at novel stimuli occurring in their environment as compared to familiar ones (novelty preference). In monkeys (Bachevalier, Brickson, & Hagger, 1993; Gunderson & Sackett, 1984; Gunderson & Swartz, 1985, 1986), as in humans (Pascalis & de Schonen, 1994; Pascalis, de Haan, Nelson, & de Schonen, 1998; Pascalis & de Haan, 2003), novelty preference is present in the first days of life and becomes stronger with age when long delays are used (Pascalis & de Haan, 2003; Morgan & Hayne, 2011). In a recent longitudinal study following the developmental trajectory of recognition memory in monkeys from 1 to 18 months, Zeamer and colleagues (Zeamer, Heuer, & Bachevalier, 2010) demonstrated that novelty preference was present at the youngest age (1 month) across all delays (10s to 120s) and became more robust by 6 months of age. By 18 months of age, however, a delay-dependent effect emerged with novelty preference being more robust at the shortest delay of 10s (74 % of looking towards novel images) and weakening (65 %) at the longest delay of 120s. This delay-dependent effect is similar to that described in adult animals and its emergence between 6 and 18 months suggested critical changes during this period within the neural substrate supporting incidental recognition memory. To investigate whether the delay-dependent effect reflected functional shifts within the hippocampus, novelty preference was assessed at the same ages (1–18 months) in monkeys that had received selective bilateral neurotoxic hippocampal lesions (Neo-H) between 10–12 days of age (Zeamer et al., 2010). Preference for novelty in Neo-H monkeys was similar to that of controls and became stronger from 1 to 6 months of age, suggesting that structures other than the hippocampus could support this function in the first postnatal months. However, by 18 months of age, the decrease in novelty preference across all delays was steeper in Neo-H monkeys as compared to controls, with no group difference at the shortest delays but a significant decrease in novelty preference for the Neo-H monkeys at the longest delay of 120s. This pattern of impairment is strikingly similar to that reported in monkeys with adult-onset hippocampal lesions (Nemanic, Alvarado, & Bachevalier, 2004) and suggests that with maturation the animals with Neo-H lesions grow into a recognition memory deficit. Thus, both the emergence of delay-dependent recognition memory performance at 18 months of age in the control animals together with the recognition memory impairment observed after neonatal hippocampal lesions at that same age indicate that important maturational changes in the neural substrate supporting incidental recognition memory occurred after 6 months of age in monkeys. In their review, Jabès and Nelson (2015) interpreted the strong novelty preference at all delays in both the controls and Neo-H animals prior to 6 months of age as resulting from early maturation of the subiculum, an hippocampal field mostly spared in the animals with Neo-H lesions. However, when re-examining the extent of neonatal hippocampal lesions (Zeamer et al., 2010), it appears that two animals in the Neo-H group (Neo-H2 and Neo-H3; see Figs. 2–3) had extensive bilateral damage to the entire hippocampus, including the subiculum; yet, these two animals showed strong novelty preference at all delays prior to 6 months of age (see Table 3). Thus, we offered an alternative interpretation to the results and suggested that the normal novelty preference after neonatal hippocampal lesions in the first few months after birth could be supported by medial temporal cortical areas, such as the perirhinal and parahippocampal cortex, thought to be critical for familiarity judgments in adults (Brown & Aggleton, 2001; Buffalo, Ramus, Clark, Teng, Squire, & Zola, 1999; Murray, 2000; Nemanic et al., 2004; Yonelinas, 2002). This idea is supported by neurobehavioral experiments in adult monkeys as well as structural development of the medial temporal cortical areas in monkeys. First, although damage to the perirhinal cortex in adult monkeys impaired recognition memory as measured by VPC as did hippocampal lesions, the pattern of deficits varied according to the lesion site. That is, hippocampal lesions resulted in impairment only at delays longer than 60s, whereas perirhinal lesions altered recognition memory at all delays tested, except the shortest delays of 1s. Second, most of the neurogenesis in medial temporal cortical areas occurs prenatally with some morphological and neurochemical changes continuing in the first few months postnatally. Thus, at birth, the anatomical organization and chemical characteristics of the perirhinal and entorhinal cortex in the primate can be clearly identified and appear adult-like (Berger & Alvarez, 1994). Thus, if our interpretation is correct, one would predict that, unlike neonatal hippocampal lesions, damage to the perirhinal cortex in infancy might result in greater deleterious effects on incidental recognition memory processes, especially at the youngest ages. Our results are consistent with this prediction. Neonatal perirhinal lesions in monkeys altered novelty preference across all delays and at all ages tested (i.e. 1.5, 6 and 18 months) and this deficit became more profound as the animals matured (Zeamer & Bachevalier, 2014). Thus, the neurobiological evidence together with the present behavioral findings indicate the emergence of significant changes in functional interactions between the medial temporal cortical areas, such as the perirhinal cortex, and the hippocampus after 6 months of age. Similar changes in the functional organization of the medial temporal cortical areas and the hippocampus have recently been demonstrated in a functional neuroimaging studies in children and adolescents (Ghetti, DeMaster, Yonelinas, & Bunge, 2010). Thus, evidence suggests that incidental recognition memory processes appear to be more widely distributed in the immature brain but become more refined and committed to the hippocampal functioning as development progresses (Zeamer, Alvarado & Bachevalier, 2009; Webster, Ungerleider, & Bachevalier, 1995).

Maturation of relational memory processes

In their review, Jabès and Nelson (2015) showed that relational memory has a more protracted development than recognition memory. They suggest that more basic relational memory skills (i.e. memory for object-object relationships and object-location associations) appear by the end of the first year and second year in humans and might be associated with the maturation of the CA1 field and its connections. By contrast, more flexible relational memory skills emerge later (4–5 years in humans), corresponding to the maturation of the CA3 field and dentate gyrus. A similar protracted development of relational memory has recently been shown in monkeys as well (Blue, Richardson, & Bachevalier, 2013).

In this study, the same control monkeys and monkeys with Neo-H lesions reported above were also given a modified version of the VPC task to measure spatial-relational memory. A VPC-Spatial-Location task tested memory for object-locations that could be solved using an egocentric spatial frame of reference and a VPC-Object-In-Place task taxed memory for spatial relations using an allocentric reference frame. All animals were tested in both tasks as infants (8 months), juveniles (18 months), and adults (5–6 years). The data from control animals demonstrated that spatial memory has a protracted development as has been shown already in humans (Ribordy, Jabès, Banta Lavenex, & Lavenex, 2012), and that memory for spatial locations emerged earlier in the juvenile period, while memory for object/place association occurred later. Although the exact ages at which both types of memory becomes available are still unknown, it is likely that memory for a familiar object in a new location may be present by the end of the first year in monkeys (Lavenex & Banta Lavenex, 2006). Yet, development of memory for object/place associations occurred later in early adolescence. This developmental patterns of spatial relational memory support the notion developed by Jabès and Nelson (2015), and following their suggestion may reflect a progressive development first of the CA1 field of the hippocampus followed by maturation the CA3 and dentate gyrus later on. Interestingly, significant increases in CA3/DG volumes were recently demonstrated in humans from childhood to early adolescence and these volumetric changes were positively correlated with memory performance (Lee, Ekstrom, & Ghetti, 2014). In light of these findings, it was not surprising to find that neonatal damage of the hippocampus did impact performance on both tasks and more importantly this impairment occurred at an age when these types of memory first emerged in the control monkeys, i.e. at 18 months for the VPC-object-location and adults for the VPC-object-in-place (Blue et al., 2013). The effects of Neo-H lesions parallel those reported in recent studies of spatial memory performance in developmental amnesic cases with perinatal hippocampal damage who demonstrate as adolescents normal performance on task measuring visuo-spatial memory that could be solved using an egocentric frame of reference (Gadian et al., 2000), but profound memory deficits for scenes and topographical information using an allocentric frame of reference (Bird, Vargha-Khadem, & Burgess, 2008; King, Trinkler, Hartley, Vargha-Khadem, & Burgess, 2004; Spiers et al., 2001).

Other considerations

In conclusion, the Jabès and Nelson review bridges what we know from memory development in humans with basic research with laboratory animals as well as more recent information using cutting-edge imaging techniques in children and adolescents. Clearly, the review goes a long way toward demonstrating how the emergence of memory skills from birth to 4–5 years reflects some critical structural changes within the hippocampal circuits. As noted by the authors, the field of memory development and its neural basis remains in its infancy and underscores the need to further investigate the link between the occurrences of memory processes with maturation of specific brain circuits. To the accounts provided by the authors, here are a few other accounts that will need to be considered.

The first is the increase in white matter processes, which in addition to the maturation of cellular fields of the hippocampus, is likely to strengthen memory performance across early ages. In addition, strengthening of connections and white matter increases in fiber tracts connecting the medial temporal lobe to prefrontal regions may also improve memory performance at later developmental ages (Wendelken, Lee, Pospisil, Sastre, Ross, Bunge, & Ghetti, 2014).

The second is a consideration of the functional development of the hippocampus in its anterior-posterior longitudinal axis. Both earlier studies in rodents (see for review Moser & Moser, 1998) and monkeys (Jackson, 1984; Colombo, Fernandez, Nakamura, & Gross, 1998) as well as more recent functional neuroimaging studies in humans (see for review Small, 2002; Nadel, Hoscheidt, & Ryan, 2013) demonstrate a functional differentiation along the longitudinal axis of the hippocampus, with the posterior (dorsal in rodents) hippocampus being crucial for precise spatial behavior, and the anterior (ventral in rodents) hippocampus being crucial for context coding. A recent structural neuroimaging study in children and adolescents (DeMaster, Pathman, Lee, & Ghetti, 2013) showed that adults with a smaller right anterior hippocampal volume and larger right hippocampal body obtained better episodic memory scores. This relationship between head and body of the hippocampus and episodic memory performance was not found in children. Thus, age-related changes in the longitudinal axis of the hippocampus may represent another contributor to improvement in episodic recollection.

Finally, in addition to the participation of the prefrontal cortex in the development of hippocampal-dependent memory processes, one will need to consider that of the diencephalon. Diencephalic structures, such as the medial thalamus and mammillary bodies play a critical role in recognition memory processes and episodic memory, as long known from human Korsakoff patients (whose alcoholism-induced damage to this brain region yields to global amnesia; Squire, 1982; Squire, Amaral, & Press, 1990) and from numerous lesion studies in animals (Aggleton & Mishkin, 1983; Aggleton & Brown, 1999; Vann & Aggleton, 2004). Yet, knowledge of the development of this brain area is at the present time unavailable. Thus, it is now in the hands of behavioral neuroscientists of the next generation to continue refining our knowledge on the specific neural bases of episodic memory development.


This work was supported in part by the National Institute of Mental Health (MH-58846), and the National Center for Research Resources P51RR165, currently supported by the Office of Research Infrastructure Programs/OD P51OD11132.


  • Aggleton JP, Brown MW. Episodic memory, amnesia, and the hippocampal-anterior thalamic axis. Behavioral Brain Science. 1999;22:425–444. [PubMed]
  • Aggleton JP, Mishkin M. Visual recognition impairment following medial thalamic lesions in monkeys. Neuropsychologia. 1983;21(3):189–197. [PubMed]
  • Alvarado MC, Bachevalier J. Animal model of amnesia. In: Byrne J, editor. Learning and Memory: A comprehensive Reference, Vol 3, Memory Systems. Elsevier; Oxford, UK: 2008. pp. 143–167.
  • Bachevalier J, Brickson M, Hagger C. Limbic-dependent recognition memory in monkeys develops early in infancy. NeuroReport. 1993;4:77–80. [PubMed]
  • Bachevalier J, Mishkin M. An early and a late developing system for learning and retention in infant monkeys. Behavioral Neuroscience. 1984;98:770–778. [PubMed]
  • Berger B, Alvarez C. Neurochemical development of the hippocampal region in the fetal rhesus monkey II. Immunocytochemistry of peptides, calcium-binding proteins, DARPP-32, and monoamine innervation in the entorhinal cortex by the end of gestation. Hippocampus. 1994;4:84–114. [PubMed]
  • Bird CM, Vargha-Khadem F, Burgess N. Impaired memory for scenes but not faces in developmental hippocampal amnesia: A case study. Neuropsychologia. 2008;46(4):1050–1059. [PubMed]
  • Blue SN, Kazama AM, Bachevalier J. Development of memory for spatial locations and object/place associations in infant rhesus macaques with and without neonatal hippocampal lesions. Journal of the International Neuropsychological Society. 2013;19:1053–1064. [PMC free article] [PubMed]
  • Brown MW, Aggleton JP. Recognition memory: what are the roles of the perirhinal cortex and hippocampus? Nature Review of Neuroscience. 2001;2:51–61. [PubMed]
  • Buffalo EA, Ramus SJ, Clark RE, Teng E, Squire LR, Zola SM. Dissociation between the effects of damage to perirhinal cortex and area TE. Learning & Memory. 1999;6:572–599. [PubMed]
  • Colombo M, Fernandez T, Nakamura K, Gross CG. Functional differentiation along the anterior-posterior axis of the hippocampus in monkeys. Journal of Neurophysiology. 1998;80(2):1002–1005. [PubMed]
  • Corkin S, Amaral DG, Gonzalez RG, Johnson KA, Hyman BT. H. M.’s medial temporal lobe lesion: Findings frommagnetic resonance imaging. Journal of Neuroscience. 1997;17:3964–3979. [PubMed]
  • Ghetti S, DeMaster DM, Yonelinas AP, Bunge SA. Developmental differences in medial temporal lobe functions during memory encoding. Journal of Neuroscience. 2010;30(28):9548–9556. [PMC free article] [PubMed]
  • DeMaster D, Pathman T, Lee JK, Ghetti S. Structural development of the hippocampus and episodic memory: Developmental differences along the anterior/posterior axis. Cerebral Cortex. 2013 2013 Jun 25; [Epub ahead of print] [PubMed]
  • Diamond A. Rate of maturation of the hippocampus and the developmental progression of children’s performance on the delayed nonmatching-to-sample and visual paired comparison tasks. Annals of the New York Academy of Science. 1990;608:394–426. [PubMed]
  • Eichenbaum HB. The hippocampal system and declarative memory in animals. Journal of Cognitive Neuroscience. 1992;4:217–231. [PubMed]
  • Eichenbaum HB. Learning and Memory: Brain Systems. In: Squire LR, Bloom FE, McConnell SK, Roberts JL, Spitzer NC, Zigmond MJ, editors. Fundamental Neuroscience. New York, NY: Academic Press; 2003. pp. 1299–1328.
  • Gadian DG, Aicardi J, Watkins KE, Porter DA, Mishkin M, Vargha-Khadem F. Developmental amnesia associated with early hypoxic-ischaemic injury. Brain. 2000;123(Pt 3):499–507. [PubMed]
  • Ghetti S, DeMaster DM, Yonelinas AP, Bunge SA. Developmental differences in medial temporal lobe function during memory encoding. Journal of Neuroscience. 2010;30(28):9548–9556. [PMC free article] [PubMed]
  • Green RJ, Stanton ME. Differential ontogeny of working memory and reference memory in the rat. Behavioral Neuroscience. 1989;103(1):98–105. [PubMed]
  • Gunderson VM, Sackett GP. Development of pattern recognition in infant pigtailed macaques (Macaca nemestrina) Developmental Psychology. 1984;20:418–426.
  • Gunderson VM, Swartz KB. Visual recognition in infant pigtailed macaques after 24-hour delay. American Journal of Primatology. 1985;8:259–264.
  • Gunderson VM, Swartz KB. Effects of familiarization time on visual recognition memory in infant pigtailed macaques (Macaca nemestrina) Developmental Psychology. 1986;22:477–480.
  • Jackson WJ. Regional hippocampal lesions alter matching by monkeys: an anorexiant effect. Physiology and Behavior. 1984;32:593–601. [PubMed]
  • Jabès A, Nelson CA. 20 years after “The ontogeny of human memory: A cognitive neuroscience perspective”, Where are we? International Journal of Behavioral Development. 2015 in press.
  • King JA, Trinkler I, Hartley T, Vargha-Khadem F, Burgess N. The hippocampal role in spatial memory and the familiarity-recollection distinction: A case study. Neuropsychology. 2004;18(3):405–417. [PubMed]
  • Lavenex P, Amaral DG. Hippocampal-neocortical interaction: A hierarchy of associativity. Hippocampus. 2000;10(4):420–430. [PubMed]
  • Lavenex P, Banta Lavenex P. Spatial relational memory in 9-month-old macaque monkeys. Learning & Memory. 2006;13(1):84–96. [PubMed]
  • Lee JK, Ekstrom AD, Ghetti S. Volume of hippocampal subfields and episodic memory in childhood and adolescence. NeuroImage. 2014;94:162–171. [PubMed]
  • Mahut H, Moss M. The monkey and the sea horse. In: Isaacson RL, Pribram KH, editors. The hippocampus. New York: Plenum Press; 1986.
  • Meunier M, Bachevalier J. The neural basis of recognition memory in nonhuman primates. In: Koob GF, Le Moal M, Thompson RF, editors. Encyclopedia of Behavioral Neuroscience. Vol. 2. Oxford, UK: Academic Press; 2010. pp. 327–333.
  • Morgan K, Hayne H. Age-related changes in visual recognition memory during infancy and early childhood. Developmental Neuropsychology. 2011;53:157–165. [PubMed]
  • Moser MB, Moser EI. Functional differentiation in the hippocampus. Hippocampus. 1998;8(6):608–619. [PubMed]
  • Murray EA. Memory for objects in nonhuman primates. In: Gazzaniga MS, editor. The New Cognitive Neurosciences. Cambridge, MA: MIT Press; 2000. pp. 753–764.
  • Nadel L, Hoscheidt S, Ryan LR. Spatial Cognition and the Hippocampus: The Anterior–Posterior Axis. Journal of Cognitive Neuroscience. 2013;25(1):22–28. [PubMed]
  • Nelson CA. The Ontogeny of Human Memory: A Cognitive Neuroscience Perspective. Developmental Psychology. 1995;31(5):723–738.
  • Nemanic S, Alvarado MC, Bachevalier J. The hippocampal/parahippocampal regions and recognition memory: insights from visual paired comparison versus object-delayed nonmatching in monkeys. Journal of Neuroscience. 2004;24:2013–2026. [PubMed]
  • Overman WH, Bachevalier J, Turner M, Peuster A. Object recognition versus object discrimination: Comparison between human infants and infant monkeys. Behavioral Neuroscience. 1992;106:15–29. [PubMed]
  • Pascalis O, de Schonen S. Recognition memory in 3- to 4-day-old human neonates. NeuroReport. 1994;5:1721–1724. [PubMed]
  • Pascalis O, de Haan M, Nelson CA, de Schonen S. Long-term recognition memory for faces assessed by visual paired comparison in 3- and 6-month old infants. Journal of Experimental Psychology: Learning, Memory, Cognition. 1998;24:249–260. [PubMed]
  • Pascalis O, de Haan M. Recognition memory and novelty preference: what model? In: Hayne H, Fagan JF, editors. Progress in Infancy Research. Vol. 3. New Jersey: Lawrence Erlbaum Associates; 2003. pp. 95–120.
  • Ribordy F, Jabès A, Banta Lavenex P, Lavenex P. Development of allocentric spatial memory abilities in children from 18 months to 5 years of age. Cognitive Psychology. 2013;66(1):1–29. [PubMed]
  • Rudy JW, Keith J, Georgian K. The effect of age on children’s learning of problems that require a configural association solution. Developmental Psychobiology. 1993;26:171–184. [PubMed]
  • Scoville WB, Milner B. Loss of recent memory after bilateral hippocampal lesions. Journal of Neurology, Neurosurgery, and Psychiatry. 1957;20:11–21. [PMC free article] [PubMed]
  • Small SA. The longitudinal axis of the hippocampal formation: its anatomy, circuitry, and role in cognitive function. Reviews of Neuroscience. 2002;13(2):183–194. [PubMed]
  • Spiers HJ, Burgess N, Hartley T, Vargha-Khadem F, O’Keefe J. Bilateral hippocampal pathology impairs topographical and episodic memory but not visual pattern matching. Hippocampus. 2001;11(6):715–725. [PubMed]
  • Squire LR. Comparisons between forms of amnesia: some deficits are unique to Korsakoff’s syndrome. Journal of Experimental Psychology, Learning, Memory and Cognition. 1982;8:560–571. [PubMed]
  • Squire LR, Amaral DG, Press GA. Magnetic resonance imaging of the hippocampal formation and mammillary nuclei distinguish medial temporal lobe and diencephalic amnesia. Journal of Neuroscience. 1990;10:3106–3117. [PubMed]
  • Tulving E. Episodic and semantic memory. In: Tulving E, Donaldson WD, editors. Organization of Memory. New York: Academic Press; 1972. pp. 381–403.
  • Vann SD, Aggleton JP. The mammillary bodies: two memory systems in one? Nature Reviews of Neuroscience. 2004;5:35–44. [PubMed]
  • Webster MJ, Ungerleider LG, Bachevalier J. Development and plasticity of the neural circuitry underlying visual recognition memory. Canadian Journal of Physiology and Pharmacology. 1995;73:1364–1371. [PubMed]
  • Wendelken C, Lee JK, Pospisil J, Sastre M, 3rd, Ross JM, Bunge SA, Ghetti S. White Matter Tracts Connected to the Medial Temporal Lobe Support the Development of Mnemonic Control. Cerebral Cortex. 2014 2014 Mar 27. [Epub ahead of print] [PMC free article] [PubMed]
  • Yonelinas AP. The Nature of Recollection and Familiarity: A Review of 30 Years of Research. Journal of Memory and Language. 2002;46:441–517.
  • Zeamer A, Alvarado MC, Bachevalier J. Development of medial temporal lobe memory processes in non-human primates. In: Blumberg M, Freeman J, Robinson S, editors. Handbook of Developmental and Comparative Neuroscience: Epigenesis, Evolution and Behavior. New-York, NY: Oxford University Press; 2009. pp. 607–616.
  • Zeamer A, Heuer E, Bachevalier J. Developmental trajectory of object recognition memory in infant rhesus monkeys with and without neonatal hippocampal lesions. Journal of Neuroscience. 2010;30:9157–9165. [PMC free article] [PubMed]
  • Zeamer A, Richardson RL, Weiss AR, Bachevalier J. The development of object recognition memory in rhesus macaques with neonatal lesions of the perirhinal cortex. Journal of Developmental Cognitive Neuroscience. 2014 Jul 21; doi: 10.1016/j.dcn.2014.07.002. [Epub ahead of print] [PMC free article] [PubMed] [Cross Ref]