We assessed visual recognition in monkeys after early damage to either the medial temporal limbic region or to cortical visual area TE, both of which are known to be critical for this mnemonic ability in adult monkeys. The results indicated substantial functional sparing after the neonatal cortical but not after the neonatal limbic removals. These findings, together with those of follow-up studies with larger extrastriate lesions, suggest that, during infancy, visual recognition functions are widely distributed throughout many visual cortical areas and that they become critically dependent on (i.e. localized to) area TE only after cortical maturation. Further evidence that functions are widely distributed at birth due to cortical immaturity comes from our studies on the development of rule learning ability (as measured by the amount of training required to learn the rule for delayed nonmatching-to-sample). Whereas the inferior prefrontal cortex is necessary for this function in adult monkeys, it is not necessary in infants. These differential findings suggested that the spared function after early inferior prefrontal damage might have been mediated by the adjacent orbital prefrontal cortex. In support of this hypothesis, we have now found that early damage to both ventral prefrontal areas in combination causes a substantial impairment in rule learning. Early combined damage to the inferior and orbital prefrontal areas produces impairment also in object recognition, yet the same damage has no effect on relational memory for objects (as assessed by the transverse patterning task, which requires the simultaneous learning of A vs. B, B vs. C, and C vs. A). By contrast, early excitotoxic damage to the hippocampus, which leaves both object recognition and rule learning unaffected, does disrupt relational memory. This is the first evidence we have obtained of a hippocampal-dependent memory process in either infant or adult monkeys, and it lends strong support to the view that the specific mnemonic role of the hippocampus is to provide for flexibility in associative memory. Our developmental studies have provided several new examples of the phenomenon wherein early brain damage causes less impairment than the same damage in adulthood, thereby reemphasizing the neuroanatomical plasticity of the immature brain. However, we have also uncovered a striking exception to this general rule, i.e. an instance in which the opposite phenomenon prevails. Thus, neonatal limbic lesions were found to yield profound and permanent socioemotional disturbances similar to those described in autistic children, abnormalities that appeared to increase in magnitude over time. By contrast, the socioemotional disturbances produced by the same damage in adult monkeys were much less severe, suggesting that the latter animals retained at least some of the socioemotional repertoire they had acquired during maturation, whereas the neonatally lesioned animals never succeeded in acquiring them. These results, indicating that medial temporal structures are more critical in infancy than in adulthood for certain functions, have important implications for socioemotional as distinct from other types of behavioral and cognitive development after medial temporal lobe damage in children. Early damage to visual area TE also results in socioemotional disturbances, but these are mild compared to those that follow early medial temporal damage, and they disappear by the time the animals reach adulthood.
