Rapid neocortical acquisition of long-term arbitrary associations independent of the hippocampus

Abstract

Anterograde amnesia following hippocampal damage involves the loss of the capacity to form new declarative memories but leaves nondeclarative memory processes intact. Current theories of declarative memory suggest the existence of two complementary memory systems: a hippocampal-based system that specializes in rapid acquisition of specific events and a neocortical system that slowly learns through environmental statistical regularities and requires the initial support of the hippocampal system. Contrary to this notion, we demonstrate a neurocognitive mechanism that enables rapid acquisition of novel arbitrary associations independently of the hippocampus. This mechanism has been dubbed "fast mapping" (FM) and is believed to support the rapid acquisition of vocabulary in children as young as 16 mo of age. We used FM to teach novel word-picture associations to four profoundly amnesic patients with hippocampal system damage. Patients were able to acquire arbitrary associations through FM normally, despite profound impairment on a matched standard associative memory task. Most importantly, they retained what they learned through FM after a week's delay, when they were around chance level on the standard task. By contrast, two patients with unilateral damage to the left polar temporal neocortex were impaired on FM, suggesting that this cortical region is critical for associative learning through FM. Left perirhinal and entorhinal cortices might also play a role in learning through FM. Contrary to current theories, these findings indicate that rapid acquisition of declarative-like (relational) memory can be accomplished independently of the hippocampus and that neocortical plasticity can be induced rapidly to support novel arbitrary associations.