Elsevier

Behavioural Brain Research

Volume 298, Part A, 1 February 2016, Pages 37-47
Behavioural Brain Research

Research report
Ontogeny of object-in-context recognition in the rat

https://doi.org/10.1016/j.bbr.2015.04.011Get rights and content

Highlights

  • Associative learning of objects and contexts develop prior to weaning in the rat.

  • Control tasks confirm that task performance requires associative learning.

  • Object-in-context learning in preweanling rats depends on salient proximal cues. When distal cues define the contexts, object-in-context learning is present in juvenile but not preweanling rats.

Abstract

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 associative 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.

Introduction

The development of contextual learning and memory has been attributed to the ontogeny of hippocampal function [1]. 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], [7], [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.

In recent decades, the novelty-preference paradigm [9], [10] has become increasingly popular in behavioral neuroscience research due to its versatility in examining multiple forms of memory and different brain memory systems. The paradigm is based on rodents’ innate preference for novel stimuli in their environments [11], and the many task variants within the paradigm can be used to assess different processes of incidental object, spatial, contextual, and temporal learning and memory [12], [13]. Novelty recognition paradigms are advantageous for studying the neurobiology of memory because they typically involve a one-trial training phase, and recognition memory has been shown to emerge during early development [14], [15], [16], [17]. In adult rats, variants of this paradigm rely on different neural systems [13], [18], which makes these tasks particularly useful for investigating neurocognitive development.

Object-in-context recognition (OiC) [19] is a variant of the standard object recognition (OR) task that relies on contextual processing. In this task, rats are consecutively exposed to two pairs of identical objects within two distinct contexts. After a delay, rats are replaced into one of the contexts with both object types present. 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].

While other forms of recognition memory such as object recognition (OR) and object location recognition (OL) have been studied ontogenetically, to our knowledge there are no studies of the ontogeny of object-in-context recognition. 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], [23], [24], ontogenetically emerges around the same time [7], [8], [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.

The present study aims to expand the developmental literature on contextual learning and novelty recognition tasks by examining OiC task performance after a short delay in PD17, PD21, PD26, and PD31 rats (Experiment 1). In addition, the present study begins to explore the determinants of object-in-context recognition during development by testing whether processing of object-context associations is necessary for OiC task performance (Experiment 2) and whether distal spatial cues are sufficient to support object-in-context learning (Experiment 3). If the OiC task recruits conjunctive (hippocampal) systems for the processing of contexts, then the ontogenetic profile of the OiC task should resemble those of the OL task [17] and the CPFE [8].

Section snippets

Experiment 1: ontogenetic profile of object-in-context recognition

In Experiment 1, we examined the ontogenetic profile of the OiC task by observing task performance in rats aged PD17, 21, 26, and 31. These ages were chosen in order to extend our recent findings on the development of the OR and OL tasks [17], [28].

Experiment 2: role of context associations in object-in-context recognition

Experiment 1 described the ontogenetic profile of the OiC task and found that preweanling rats could remember the contexts in which they previously encountered objects. Due to the OiC task's early emergence compared to other contextual learning paradigms [6], [7], Experiment 2 sought to determine whether developing rats were indeed associating the objects encountered during the sample phases with their respective contexts. Following training, PD17 and PD26 rats were either tested in a context

Experiment 3: contribution of distal spatial cues to object-in-context recognition

Results from Experiments 1 and 2 show that rats as young as 17-days-old can learn associations of object and context information. In Experiment 3, we asked whether distal spatial cues were sufficient to support OiC learning in preweanling and juvenile rats. Adult lesion and developmental literature on the contextual/spatial learning suggest that the hippocampus is specifically involved in processing the distal, but not proximal spatial environment [31], and that distal spatial processing

General discussion

The present study defines the ontogenetic profile of object-in-context recognition and begins to explore the behavioral determinants of the OiC task in developing rats. Experiment 1 demonstrated that PD17, 21, 26, and 31 rats can all display preference for the novel target in the OiC task. Experiment 2 replicated these findings in PD17 and PD26 rats and additionally showed that when rats were tested in an alternate context, novelty preference was eliminated. The inability of this group to

Acknowledgements

The authors would like to thank Hollie R. Sanders and Lauren E. Brennan for assistance with behavioral data collection. This study was supported by funding from the University of Delaware Undergraduate Research Program (to AIR), McNair Scholars Program (to AIR), and NIH grants 1-R21-HD070662-01 and 1-R01-HD075066-01A1 (to MES).

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