Role of Age, Spatial Processing, and NMDA Receptors in the Ontogeny of Contextual Recognition Memory

Abstract

Determining the ontogenetic emergence of contextual learning and memory remains a challenge for developmental behavioral neuroscientists (for review, see Revillo et al., 2015). Research in this area suggests that the ability to acquire context representations emerges around the time of weaning in the rat (e.g., Jablonski et al., 2012), similar to hippocampus-dependent spatial cognition. However, this work has primarily utilized contextual fear conditioning paradigms that involve long delays and require interactions between cognitive and emotional brain memory systems, making it difficult to attribute preweanling rats’ failure to express fear to contextual stimuli to the underdevelopment of memory systems supporting contextual learning per se. In addition, a key difficulty surrounds the spatial versus nonspatial nature of the contextual cues processed by preweanling rats (e.g., Pugh & Rudy, 1996), which may recruit different neural systems. The current study examined contextual learning and memory in developing rats using an incidental learning paradigm known as the object-in-context recognition (OiC) task. We demonstrate that rats as young as 17-days-old can exhibit short-term contextual memory using this paradigm (Experiment 1A), and that learning in this task is associative (Experiment 1B). To address the spatial versus nonspatial context problem, we next manipulated the contextual cues or object placements in our OiC preparation and observed delayed development of contextual recognition memory when contexts in the OiC task were distinguishable only by the distal spatial environment (Experiment 2A) or when spatial information about the objects needed to be associated with contextual stimuli (object-place-context recognition; OPC task; Experiment 2B). Finally, we explored the role of NMDA receptors in contextualrecognition memory by administering an NMDA receptor antagonist prior to the aforementioned tasks. Systemic injections of .06 mg/kg MK-801 prior to training did not impair performance in our standard OiC task (Experiment 3A), but did in the latter two spatial task variants (Experiments 3B and C). These data provide strong support for contextual learning and memory in the preweanling rat and further support the notion that the ontogeny of contextual memory is influenced by the degree of spatial processing necessary for task performance. Furthermore, spatial cognition may contribute to the neurobiology of contextual recognition memory by rendering it dependent on NMDA-receptor-related plasticity.