Global retrograde amnesia but selective anterograde amnesia after frontal-temporal disconnection in monkeys

Prefrontal cortex and inferior temporal cortex interact in support of a wide variety of learning and memory functions. In macaque monkeys, a disconnection of prefrontal and temporal cortex produces severe new learning impairments in a range of complex learning tasks such as visuo-motor conditional learning and object-in-place scene learning. The retrograde effects of this disconnection, however, have never been fully examined. We therefore assessed the postoperative retention of 128 preoperatively learned object discrimination problems in monkeys with prefrontal-temporal disconnection using 1 trial postoperative retention tests. Because previous experiments have suggested that both spatial and temporal factors may be important in engaging frontal-temporal interaction we used object discrimination problems with a variety of spatial and temporal properties. Postoperatively, although monkeys with prefrontal-temporal disconnection displayed a retrograde amnesia for all problem types, subsequent assessments of new learning revealed selective anterograde amnesia, which was limited to problems in which objects were presented as serial compound stimuli. The pattern of broad retrograde amnesia with selective anterograde amnesia contrasts with recent data from monkeys with lesions which disrupt subcortical-cortical connectivity and which show the opposite pattern, namely no retrograde amnesia but severe anterograde amnesia. These results support the hypothesis that visual memory acquisition is supported by subcortical-cortical interactions while the retrieval of visual memories normally depends on the interaction between prefrontal cortex and inferior temporal cortex.