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    • Successful performance on the transverse

    2018-10-29

    Successful performance on the transverse patterning problem requires relational memory abilities, although there can be alternative strategies that support performance, such as in the rock-paper-scissors game or other semantic cues (Moses et al., 2008). The results of the present study show clearly that the relational learning as measured by the transverse patterning problem is late-developing. Unlike simple concurrent discriminations, which can be performed at a younger age, or the ability to use a nonmatching rule, which is present relatively early, but matures over the first year of life (see Bachevalier, 2013; Bachevalier and Vargha-Khadem, 2005 for review), the capability to use a relational rule does not seem to emerge before 12 months of age at the earliest, with animals older than 15 months of age able to solve the transverse patterning task. However, even at 24 months of age, not all naïve subjects used a relational strategy, whereas all subjects who had prior experience with the task and were retrained at 15 or 24 months did. Their performance improved with age such that at 36 months they learned at a mature level, similar to adults in our previous studies (Alvarado et al., 2002; Alvarado and Bachevalier, 2005). The only other published developmental study using transverse patterning trained similarly to ours was in children. Rudy and colleagues (1993) showed that the ability to learn the transverse patterning discriminations is developmentally delayed in humans, who are unable to solve the task until approximately 5 yr of age (Rudy et al., 1993). Interestingly, both our and Rudy’s results parallel the ability to perform spatial navigation tasks in children (Overman et al., 1996b) and spatial relational tasks in nursery-reared monkeys (Blue et al., 2013). Given the results from lesion and developmental neuroanatomical studies in the literature, we can speculate as to the neural basis for the prolonged maturation of relational memory abilities. Evidence that this developmental delay reflects maturational processes within the medial temporal lobe in monkeys is provided by studies in which performance on this task is severely impaired by hippocampal lesions. For example, performance was impaired in adult monkeys with either neonatal damage to the hippocampal region (Alvarado et al., 2002), or neurotoxic damage to the hippocampal formation, perirhinal carboxypeptidase a or area TH/TF sustained in adulthood (Alvarado and Bachevalier, 2005a,b). Interestingly, the animals in each of those studies performed similarly to the 12 month old groups in the present study, regardless of the age at which the lesion occurred. That is, they adopted a performance strategy that treated the individual stimuli in a linear heirarchy (i.e., A>B>C). Similar results have been shown in adult amnesic humans with hippocampal or temporal lobe damage (Rickard and Grafman, 1998; Reed and Squire, 1999), and in rats with neurotoxic damage to the hippocampal formation (Alvarado and Rudy, 1995). Although the specific structure within the medial temporal lobe supporting the development of relational memory is still under investigation, the fact that performance on tasks requiring perirhinal cortex develop early (Zeamer et al., 2015), and that the effects of early hippocampal damage to memory emerge late, suggests that the likelier candidates would be hippocampus and/or TH/TF in the medial temporal lobe. Furthermore, the finding that relational memory abilities in the spatial or nonspatial domain develop later than those for spatial recognition memory, suggests that additional late-developing structures, or protracted maturation of connections to other structures, contribute to this prolonged maturation. For example, Blue et al. (2013) traced the development of spatial memory, testing at 8, 18 and 60 months of age and found that young monkeys recognized a spatial location by 18 months, but memory for object-place relations was only present at the 60 month testing age (they were not tested on spatial tasks between 18 and 60 months). Interestingly, neonatal hippocampal damage delayed the emergence of spatial recognition, and prevented emergence of object-place relations. This finding might explain some of the differences observed among variations in the task and the effects of specific MTL damage. For example, in our hands, using 3 dimensional objects, damage to the hippocampus impacts performance on transverse patterning, however so do lesions of the parahippocampal or perirhinal cortices (Alvarado and Bachevalier, 2005a,b). Using different methods and stimuli that emphasize a strictly configural solution with perceptually complex or ambiguous stimuli (e.g. Saksida et al., 2007; see Alvarado and Bachevalier, 2005b for similar discussion) are less (or not at all) affected by hippocampal damage, but are impaired by perirhinal cortex damage.