Malkova, L., Bachevalier, J., Webster, M., and Mishkin, M. (2000, in press.) Effects of neonatal inferior prefrontal and medial temporal lesions on learning the rule for delayed nonmatching-to-sample. Developmental Neuropsychology.
The ability of the rhesus monkeys to master the rule for delayed nonmatching-to-sample (DNMS), a measure of object recognition, has a protracted ontogenetic development, and the ability does not reach adult levels of proficiency until the animals are 4-5 years of age (Bachevalier, 1990). This slow development could be due, at least in part, to immaturity of the prefrontal component of a temporo-prefrontal circuit that is important in adult monkeys for DNMS rule-learning (Kowalska et al., 1991; Weinstein et al., 1988). To test this possibility, monkeys with neonatal lesions of the inferior prefrontal convexity were compared on DNMS with both normal controls and animals given neonatal lesions of the medial temporal lobe. The three groups were tested first at the age of 3 months and then reassessed at the age of 2 years. Consistent with our previous results (Bachevalier & Mishkin, 1994; Malkova et al., 1995), the neonatal medial temporal lesions led to marked impairment at both ages in rule-learning (as well as in recognition memory with long delays and list lengths), the learning deficit being particularly severe at the earlier age. By contrast, the neonatal inferior convexity lesions yielded on impairment in rule-learning at 3 months and only a mild impairment at 2 years, a finding that also contrasts sharply with the marked effects of the same lesion made in adulthood. This pattern of sparing closely resembles the one found earlier after neonatal lesions to the cortical visual area TE (Bachevalier & Mishkin, 1994; Malkova et al., 1995). The functional sparing at 3 months probably reflects the fact that the temporoprefrontal circuit is nonfunctional at this early age, resulting in a total dependency on medial temporal contributions to rule learning. With further development, however, this circuit begins to provide an alternative route for learning, at which point the ability begins to depend less on the medial temporal region and more on the temporo-prefrontal pathway. The long-lasting sparing of rule-learning after neonatal lesions to the stations in this pathway must therefore be due to functional compensation by neighboring tissue, such as area TEO in the case of early TE lesions, and orbital frontal cortex after early inferior convexity lesions.