Ontogeny of object-in-context recognition in the rat

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.

Keywords: Context; Hippocampus; Incidental learning; Long–Evans rat; Ontogeny; Short-term memory.

Figure 1

Testing apparatuses. Contexts A (A) and B (B) were used in Experiments 1, 2, and 3, whereas Context C (C) was used only in Experiment 2. Two different object configurations (Configurations 1 and 2) for object placements during the OiC task are shown in red.

Figure 2

Stimulus Objects. Objects displayed in A and B were used in Experiments 1 and 3. Objects displayed in A and C-E were used in Experiment 2.

Figure 3

A schematic diagram of the object-in-context (OiC) task. Objects are shown in configuration 1. During the training phase, rats are exposed to two different pairs of objects within distinct contexts (Sample 1 and Sample 2), separated by a short delay (Delay 1). After a retention interval of 5 min (Delay 2), rats are replaced into one of the sample contexts with a copy of both previously-encountered objects present.

Figure 4

Exploration times for each age group during Sample 1 (A) and Sample 2 (B) of Experiment 1. Mean exploration times (±SEM) are given. In general, mean exploration times increased with age until PD26. Mean exploration times only differed between sample phases in the PD17 age group. Significant differences between age groups for congruent sample phases are indicated (**p<.01).

Figure 5

Mean exploration ratios (±SEM) during the OiC test phase for Experiment 1. Exploration ratios were calculated as t_novel / (t_novel + t_familiar). Dashed line represents chance performance (0.5). All age groups performed significantly above chance levels. (**p<.01, ***p<.001)

Figure 6

Mean exploration times (±SEM) for each testing condition (Same vs. Different) by age group during Sample 1 (A) and Sample 2 (B) of Experiment 2. Testing condition did not affect object exploration times during the sample phases. Exploration times were significantly lower in PD17 groups compared to PD26 groups. (***p<.001)

Figure 7

Mean exploration ratios (±SEM) during the OiC test phase by age group and test condition for Experiment 2. Exploration ratios were calculated as t_novel / (t_novel + t_familiar). Dashed line represents chance performance (0.5). Both Same groups performed significantly above chance levels. The Different group at age PD26 showed a significant familiarity preference. (*p<.05, ***p<.001)

Figure 8

Mean exploration times (±SEM) by age and sample phase (A) or context condition (B) for Experiment 3. Juvenile rats explored more overall than preweanling rats and PD17 rats in the Global group explored more than PD17 rats in the Distal group. (**p<.01, ***p<.001)

Figure 9

Mean exploration ratios (±SEM) during the OiC test phase by age group and context condition for Experiment 3. Exploration ratios were calculated as t_novel / (t_novel + t_familiar). Dashed line represents chance performance (0.5). Both Global groups performed significantly above chance levels. Only the Distal group at age PD26 showed a significant novelty preference. (*p<.05, ***p<.001)