Development and plasticity of the neural circuitry underlying visual recognition memory.

Abstract

In adult monkeys, visual recognition memory, as measured by the delayed nonmatching to sample (DNMS) task, requires the interaction between inferior temporal cortical area TE and medial temporal lobe structures (mainly the entorhinal and perirhinal cortical areas). Ontogenetically, monkeys do not perform at adult levels of proficiency on the DNMS task until 2 years of age. Recent studies have demonstrated that this protracted development of visual recognition memory is due to an immaturity of the association areas of the neocortex rather than the medial temporal lobe. For example, lesions of the medial temporal lobe structures in infancy or in adulthood yield profound and permanent visual recognition loss, indicating that the medial temporal lobe structures operate early in life to sustain visual memory. In contrast, early lesions of area TE, unlike late lesions, result in a significant and long-lasting sparing of visual memory ability. Further evidence for neocortical immaturity is provided by studies of the development of opiatergic and cholinergic receptors, of the maturation of metabolic activity, and of the connectivity between inferior temporal areas TE and TEO and cortical and subcortical structures. Together these results indicate greater compensatory potential after neonatal cortical than after neonatal medial temporal removals. In support of this view, early damage to area TE leads to the maintenance of normally transient projections as well as to reorganization in cortical areas outside the temporal lobe. In addition, lesion studies indicate that, during infancy, visual recognition functions are widely distributed throughout many visual association areas but, with maturation, these functions become localized to area TE. Thus, the maintenance of exuberant projections together with reorganization in other cortical areas of the brain could account for the preservation of visual memories in monkeys that have had area TE removed in infancy.