Role of age, post‐training consolidation, and conjunctive associations in the ontogeny of the context preexposure facilitation effect

Jablonski, Sarah A.; Schiffino, Felipe L.; Stanton, Mark E.

doi:10.1002/dev.20621

Cited by 48 publications

(96 citation statements)

References 42 publications

(84 reference statements)

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“…Similarly, contextual memories, studied using contextual fear conditioning, are observed at PN18 but rapidly decay, and their retention comes to resemble that in adult rats starting at PN23 (Pugh and Rudy, 1996). Other hippocampal-type learning, such as context pre-exposure facilitation, emerges at PN23-PN24 (Jablonski et al, 2012). Similar patterns are observed in the ontogeny of trace fear conditioning, a type of associative learning in which the animal learns to temporally separate the conditioned stimulus (CS) from the unconditioned stimulus (US) by an extended interstimulus interval.…”

Section: Hippocampus-dependent Learning and Its Ontogenymentioning

confidence: 63%

Infantile Amnesia: A Critical Period of Learning to Learn and Remember

2017

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Infantile amnesia, the inability of adults to recollect early episodic memories, is associated with the rapid forgetting that occurs in childhood. It has been suggested that infantile amnesia is due to the underdevelopment of the infant brain, which would preclude memory consolidation, or to deficits in memory retrieval. Although early memories are inaccessible to adults, early-life events, such as neglect or aversive experiences, can greatly impact adult behavior and may predispose individuals to various psychopathologies. It remains unclear how a brain that rapidly forgets, or is not yet able to form long-term memories, can exert such a long-lasting and important influence. Here, with a particular focus on the hippocampal memory system, we review the literature and discuss new evidence obtained in rats that illuminates the paradox of infantile amnesia. We propose that infantile amnesia reflects a developmental critical period during which the learning system is learning how to learn and remember.The long-lasting influence of episodic infantile experiences and the paradox of infantile amnesia How do we develop our abilities to learn and remember facts, people, things, relationships, and places? These memories define our identities; they store autobiographical episodes that can be consciously declared, and are therefore termed declarative memories. Declarative memories include both the experience of specific things, people, and events of a given time and place (episodic memories), and general knowledge about the world (semantic memories). They are also known as explicit memories because they require conscious recollection (Graf and Schacter, 1985). These are the memories that are lost in Alzheimer's disease or aging-related memory impairment. Parallels of these memories exist in nonhuman animals and include contextual, spatial, and episodic memories (Ergorul and Eichenbaum, 2004). Collectively, such memories store information about "who, what, when and where," and are therefore termed "wwww" memories. In both humans and nonhuman mammals, wwww memories are processed by the hippocampus-dependent (or medial temporal lobe-dependent) learning and memory system (Eichenbaum, 2006; Squire and Wixted, 2011;Lavenex and Banta Lavenex, 2013;Albani et al., 2014).A large body of clinical and behavioral evidence has demonstrated the critical importance of infantile episodic experiences for brain function throughout life. However, little is known about the biological mechanisms underlying the development of the hippocampus-dependent learning and memory system. Many studies have shown that hippocampus-dependent memories (also referred to as hippocampal memories) are severely compromised by challenges occurring early in life. These challenges may be either psychological (e.g., trauma, neglect, or deprivation of social experience) or biological (e.g., the impact of genetic mutations on development). All of these events can predispose individuals to psychopathologies, such as post-traumatic stress disorder, borderline personality ...

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Section: Hippocampus-dependent Learning and Its Ontogenymentioning

confidence: 63%

Infantile Amnesia: A Critical Period of Learning to Learn and Remember

2017

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“…Hippocampus-dependent spatial memory develops between P16 and P21 in rats as measured by delayed alternation and water maze memory (Freeman & Stanton, 1991; Green & Stanton, 1989; Rudy, Stadler-Morris, & Albert, 1987). Contextual fear conditioning and the context preexposure facilitation effect also depend on the hippocampus and emerges ontogenetically at around P23 in rats (Jablonski, Schiffino, & Stanton, 2012; Rudy, 1993; Rudy & Morledge, 1994; Schiffino, Murawski, Rosen, & Stanton, 2011). Moreover, disrupting hippocampal development with early ethanol exposure impairs the context preexposure facilitation effect in developing rats (Jablonski & Stanton, 2014).…”

Section: Discussionmentioning

confidence: 99%

Ontogeny of septohippocampal modulation of delay eyeblink conditioning

Harmon

Freeman

2015

Developmental Psychobiology

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The current study investigated the effects of disrupting the septohippocampal theta system on the developmental emergence of delay eyeblink conditioning. Theta oscillations are defined as electroencephalographic (EEG) waveforms with a frequency between 3–8 Hz. Hippocampal theta oscillations are generated by inputs from the entorhinal cortex and the medial septum. Theta activity has been shown to facilitate learning in a variety of paradigms, including delay eyeblink conditioning. Lesions of the medial septum disrupt theta activity and slow the rate at which delay eyeblink conditioning is learned (Berry & Thompson, 1979). The role of the septohippocampal theta system in the ontogeny of eyeblink conditioning has not been examined. In the current study, infant rats received an electrolytic lesion of the medial septum on postnatal day (P)12. Rats were later given eyeblink conditioning for 6 sessions with an auditory conditioned stimulus on P17–P19, P21–23, or P24–P26. Lesions impaired eyeblink conditioning on P21–23 and P24–26 but not on P17–19. The results suggest that the septohippocampal system comes online to facilitate acquisition of eyeblink conditioning between P19 and P21. Developmental changes in septohippocampal modulation of the cerebellum may play a significant role in the ontogeny of eyeblink conditioning.

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“…It was previously thought that the hippocampus was involved in processing polymodal stimuli associated with a context [2]; however, it is now known that contextual learning can be supported by neural systems separate from the hippocampus in scenarios where the hippocampus has been compromised [3], or when contextual learning is mediated by an elemental associative system that obviates hippocampal function [4, 5]. The development of contextual learning and memory processes has been well-defined primarily using fear conditioning paradigms [1, 6-8]; yet, it is unclear whether the previously reported ontogenetic, behavioral, and neural determinants of contextual learning are applicable to other context-dependent learning tasks. Developments in behavioral techniques, such as the novelty-preference paradigm, now allows for the examination of these questions.…”

Section: Introductionmentioning

confidence: 99%

“…Rats preferentially explore the object mismatched to the testing context (novel target) based on the previous object-context pairings. The learning of object-context associations in the OiC task is incidental (without reinforcement); thus, research utilizing this task is relevant to other context-dependent incidental learning paradigms like the context preexposure facilitation effect (CPFE) [7, 8], which is also used to study memory functions of medial temporal lobe structures including the hippocampus and associated cortices [5]. …”

Section: Introductionmentioning

confidence: 99%

“…Performance of the OR task emerges before postnatal day (PD) 17 in the rat [16, 17], whereas our lab demonstrated that the OL task, which relies on hippocampal function [12, 13, 16, 20, 21], emerges between PD17 and 21 [17]. Likewise, the CPFE, a form of contextual fear conditioning that also requires incidental context learning and the hippocampus [7, 22-24], ontogenetically emerges around the same time [7, 8, but see 25]. The convergence of these findings and other reports on the development of spatial cognition [26, 27] suggest that behavioral performance in the OiC task may have a similar ontogenetic profile, given that similar underlying mechanisms are responsible for OiC memory.…”

Section: Introductionmentioning

confidence: 99%

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Ontogeny of object-in-context recognition in the rat

Ramsaran

Westbrook

Stanton

2016

Behavioural Brain Research

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The object-in-context recognition (OiC) task [19] is a spontaneous exploration task that serves as an index of incidental contextual learning and memory. During the test phase, rats prefer to explore the object mismatched to the testing context based on previous object-context pairings experienced during training. The mechanisms of OiC memory have been explored in adult rats [12, 35]; however, little is known about its determinants during development. Thus, the present study examined the ontogeny of the OiC task in preweanling through adolescent rats. We demonstrate that postnatal day (PD) 17, 21, 26, and 31 rats can perform the OiC Task (Experiment 1) and that preference for the novel target is eliminated when rats are tested in an alternate context not encountered during training (Experiment 2). Lastly, we show that PD26 but not PD17 rats can perform the OiC task when the training contexts only differed by distal spatial cues (Experiment 3). These data demonstrate for the first time that PD17 rats can acquire and retain short-term OiC memory, which involves conjunctive learning of object and context information. However, we also provide evidence that preweanling rats’ ability to utilize certain aspects of a context (i.e., distal spatial cues) in the OiC task is not equivalent to that of their older counterparts. Implications for the development of contextual memory and its related neural substrates are discussed.

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Role of age, post‐training consolidation, and conjunctive associations in the ontogeny of the context preexposure facilitation effect

Cited by 48 publications

References 42 publications

Infantile Amnesia: A Critical Period of Learning to Learn and Remember

Infantile Amnesia: A Critical Period of Learning to Learn and Remember

Ontogeny of septohippocampal modulation of delay eyeblink conditioning

Ontogeny of object-in-context recognition in the rat

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