Contextual fear conditioning differs for infant, adolescent, and adult rats

Abstract

Contextual fear conditioning was tested in infant, adolescent, and adult rats in terms of Pavlovian conditioned suppression. When a discrete auditory conditioned stimulus (CS) was paired with footshock (unconditioned stimulus, US) within the largely olfactory context, infants and adolescents conditioned to the context with substantial effectiveness but adult rats did not. When unpaired presentations of the CS and US occurred within the context, contextual fear conditioning was strong for adults, weak for infants, but about as strong for adolescents as when pairings of CS and US occurred in the context. Nonreinforced presentations of either the CS or context markedly reduced contextual fear conditioning in infants, but, in adolescents, CS extinction had no effect on contextual fear conditioning, although context extinction significantly reduced it. Neither CS extinction nor context extinction affected responding to the CS-context compound in infants, suggesting striking discrimination between the compound and its components. Female adolescents showed the same lack of effect of component extinction on response to the compound as infants, but CS extinction reduced responding to the compound in adolescent males, a sex difference seen also in adults. Theoretical implications are discussed for the development of perceptual-cognitive processing and hippocampus role. Keywordscontextual fear conditioning; fear extinction; learning; olfactory context; hippocampus; ontogeny Contextual fear conditioning has received a lot of attention from behavioral neuroscientists during the last decade (e.g., Anagnostaras, Gale, & Fanselow, 2001;Fanselow & Poulos, 2004;Phillips & LeDoux, 1992). The purpose of this report is to assess the effectiveness of contextual fear conditioning experiments by rats at each of three disparate periods of ontogeny: late infancy, adolescence and early adulthood. The ontogeny of contextual fear conditioning is of interest because --in relation to conditioning of other events within the context--it can Publisher's Disclaimer: This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final citable form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. provide a window to the ontogeny of encoding and memory organization (e.g., Brasser & Spear, 2004;Lariviere, Chen, & Spear, 1990), and because it has been used as a marker for the development of brain function important for memory (e.g., Pugh & Rudy, 1996;Rudy & Morledge, 1994). NIH Public AccessSeveral experiments led to the conclusion that acquisition of an aversion to a particular context paired with footshock is less effective in rats during late infancy (postnatal days 17-20, P17-20) than in weaned juvenile ...

Ontogeny of contextual fear memory formation, specificity, and persistence in mice

“…The authors speculated that this temporary suppression of contextual fear memory could serve an adaptive function, allowing adolescent mice to venture out of the nest and explore potentially threatening environments. In line with several previous studies in mice (Hefner and Holmes 2007) and rats (Pugh et al 1997;Brasser and Spear 2004;Esmoris-Arranz et al 2008;Murawski and Stanton 2010), however, we found no evidence of memory suppression in adolescents. Instead, we found that levels of conditioned fear were stable across all ages tested, from infancy to adulthood.…”

“…Although some studies report that rats fail to associate a shock with a context until 23-24 d of age (Spear 1979;Rudy 1993;Rudy and Morledge 1994;Raineki et al 2010;Schiffino et al 2011), others demonstrate that this type of learning can occur at 17-18 d of age under some training conditions (Brasser and Spear 2004;Esmoris-Arranz et al 2008;Pisano et al 2012) or following certain neonatal manipulations (i.e., injection of fibroblast growth factor-2, sensory stimulation) (Woodcock and Richardson 2000;Graham and Richardson 2010;Callaghan and Richardson 2011). Our finding that mice are able to associate a shock with a context as early as 13-14 d of age, however, suggests that brain and behavioral development is accelerated in mice compared to rats, consistent with previous proposals (Pellis and Iwaniuk 2000;Whishaw et al 2001).…”

Limbic system development underlies the emergence of classical fear conditioning during the third and fourth weeks of life in the rat.

“…Additionally, contextual learning may emerge earlier than suggested by the “traditional view” (Brasser & Spear, 1998; Brasser & Spear, 2004; Esmorís-Arranz, Méndez, & Spear, 2008; Foster & Burman, 2010). Thus, it seems likely that several structures, and the connectivity between them, are continuing to emerge during the periweaning time period, making a strict dissociation between auditory and contextual fear conditioning somewhat unlikely.…”

Contextual and Auditory Fear Conditioning Continue to Emerge during the Periweaning Period in Rats

“…For example, when examining extinction of fear conditioning, Rick Richardson and colleagues report giving twice as many CS-US pairings to PD 16 subjects than to PD 23 subjects in order to achieve equivalent initial freezing, suggesting that PD 23 subjects otherwise demonstrate greater conditioning [32], [33]. Although they did not directly compare across ages, another study found that there is an almost 3-fold increase in freezing between PD 17 and 28 to a CS-context compound [25]. No such increase was found to the context alone, suggesting that CS-elicited freezing accounted for this effect.…”