Impaired discrimination with intact crossmodal association in aged rats: A dissociation of perirhinal cortical-dependent behaviors

Abstract

The perirhinal cortex (PRC) supports associative memory and perception, and PRC dysfunction impairs animals' abilities to associate stimulus features across sensory modalities. PRC damage also leads to deficits in discriminating between stimuli that share features. Although PRC-dependent stimulus discrimination has been shown to be impaired with advanced age, data regarding the abilities of older adults and other animals to form PRC-dependent associations have been equivocal. Moreover, the extent to which similar neural computations within the PRC support associative memory versus discrimination abilities have not been directly examined. In the current study, young and aged rats were cross-characterized on two PRC-dependent crossmodal object recognition (CMOR) tasks to test associative memory, and a LEGO object discrimination task. In the CMOR tasks, rats were familiarized with an object with access to tactile input and then tested for recognition with visual input only. The relative exploration time of novel versus familiar objects indicated that aged rats showed preference for the novel over familiar object with and without an epoch of multimodal preexposure to the familiar object prior to the testing session. Furthermore, crossmodal recognition performance between young and aged rats was not significantly different. In contrast, for the LEGO object discrimination task, aged rats were impaired relative to young rats. Notably, aged rats that performed poorly on the LEGO object discrimination task had better performance on the CMOR tasks. The dissociation of discrimination and association abilities with age suggests that these behaviors rely on distinct neural computations within PRC-medial temporal lobe circuit. (PsycINFO Database Record

Figure 1. Experimental design

(A) Timeline of testing for all behavioral experiments. The order of object recognition conditions was pseudorandomized across animals. (B) Line drawing representing the testing apparatus for the object recognition task. The black circles indicate the location that objects were placed during all phases of recognition testing. Photographs show all objects that were used for recognition testing. Objects were made of plastic or ceramic. Triplicates of each object were obtained for testing to ensure that rodents could not use odorant cues to recognize or discriminate between objects and the novel versus familiar object within a task were counterbalanced across rats. (C) Line drawing representing the testing apparatus for the object discrimination task. The black circles indicate food wells where the food reward is placed for the rat to obtain. The blue ring in the right arm of the object discrimination apparatus represents the Froot Loop piece placed in the arm to be retrieved by the rat at the start of each trial. Photographs show the standard (top) and LEGO (bottom) objects used in the discrimination tasks.

Figure 2. Standard Crossmodal Object Recognition (CMOR) without multimodal pre-exposure performance

(A) Mean exploration time (seconds) for the novel and familiar objects in young (white) and aged (grey) rats. The main effect of object (novel versus familiar) was significant with more time spent exploring the novel object (F_[1,41] = 6.73, p < 0.05). However, the main effect of age on total exploration time was not significant (F_[1,41] = 0.57, p = 0.46). While the interaction effect between object type (novel versus familiar) and age also did not reach statistical significance (F_[1,41] = 1.18, p = 0.28), there was a trend for the young rats to explore the familiar object more than the aged rats (t_[41] = −1.76, p = 0.09). (B) Mean discrimination ratio for young (white) and aged (grey) rats. The aged rats (T_[17] = 2.39, p < 0.05), but not young (T_[24] = 1.17, p = 0.25), showed a discrimination ratio that was significantly different from 0.

Figure 3. Crossmodal Object Recognition (CMOR) with multimodal pre-exposure performance

(A) Mean exploration time (seconds) for the novel and familiar objects in young (white) and aged (grey) rats. Significantly more time was spent exploring the novel object relative to the familiar object (F_[1,41] = 11.50, p = 0.02). However, there was not a significant main effect of age (F_[1,41] = 0.20, p = 0.66), nor was the interaction between exploration time and age significant (F_[1,41] = 0.15, p = 0.70). (B) Mean discrimination ratio in young (white) and aged (grey) rats. The discrimination ratio of young and aged rats did not significantly differ between the age groups (t_[41] = 1.24, p = 0.22), but were significantly different from 0 (t_[42] = 4.52, p < 0.001).

Figure 4. Comparison of Visual and Tactile Standard Object Recognition (SOR) Performance across Age Groups

(A) Mean exploration time (seconds) for the novel and familiar objects in young (white) and aged (grey) rats for the tactile- and visual-only SOR tasks. For the tactile-only SOR task, rats spent significantly more time exploring the novel compared to the familiar objects (F_[1,39] = 11.80, p < 0.01). This did not vary as a function of age group (F_[1,39] = 0.06, p = 0.81). For the Visual-only SOR task, there were not significant effects of exploration time of novel versus familiar objects (F_[1,38] = 0.94, p = 0.34), age (F_[1,38] = 1.05, p = 0.31), or interaction between exploration time and age (F_[1,38] = 0.01, p = 0.92). (B) Mean discrimination ratios for the tactile and visual-only SOR tasks in young (white) and aged (gray) rats. Discrimination ratios of young and aged rats did not significantly differ in the tactile-only SOR task (t_[39] = 0.54, p = 0.59) or in the visual-only SOR task (t_[38] = 0.18, p = 0.86). The discrimination ratio was significantly different from 0, however, for both the tactile-only SOR task (t_[40] = 5.90, p < 0.001) and the visual-only SOR task (t_[39] = 2.69, p = 0.01).

Figure 5. Standard Object Discrimination Performance by Age Group

Standard object discrimination percent correct (%) as a function of test day in young (white) and aged (grey) rats. Performance did not significantly differ between test day (F_[1,41] = 0.16, p = 0.69), or age group (F_[1,41] = 0.07, p = 0.79). Moreover, the interaction effect between testing day and rat age was not significant (F_[1,41] = 0.36, p = 0.55).

Figure 6. LEGO Object Discrimination Performance by Age Group

(A) LEGO object discrimination percent correct (%) as a function of test day in young (white) and aged (grey) rats. The main effect of testing day on LEGO object discrimination task performance was significant (F_[7,1] = 11.48, p < 0.001). The main effect of age (F_[1,21] = 2.62, p = 0.12). Notably, the interaction of testing day and age was significant (F_[7,1] = 2.90, p = 0.007) when collapsed across test days 3 through 10. Performance was significantly different between young and aged rats on day 10 (F_[1,21] = 9.88, p = 0.005). (B) Individual performance on LEGO object discrimination on Day 10 in young and aged rats. Horizontal lines indicated group means.

Figure 7. CMOR performance within LEGO object discrimination performance subgroups

(A) Mean discrimination ratio for the standard CMOR task without multimodal pre-exposure in young and aged rats separated into good and poor performing subgroups based on mean LEGO object discrimination percent accuracy. Only the Aged Poor Performers showed a significant preference for novelty on the standard CMOR task (t_[8] = 2.60, p = 0.03). (B) Same as in A, but for the CMOR with multimodal pre-exposure task. Again, only the Aged Poor Performers showed significant preference for novelty (t_[6] = 3.99, p = 0.007).