Object and spatial memory after neonatal perirhinal lesions in monkeys

Abstract

The contribution of the perirhinal cortex (PRh) to recognition memory is well characterized in adults, yet the same lesions have limited effect on recognition of spatial locations. Here, we assessed whether the same outcomes will follow when perirhinal lesions are performed in infancy. Monkeys with neonatal perirhinal (Neo-PRh) lesions and control animals were tested in three operant recognition tasks as they reached adulthood: Delayed Nonmatching-to-Sample (DNMS) and Object Memory Span (OMS), measuring object recognition, and Spatial Memory Span (SMS), measuring recognition of spatial locations. Although Neo-PRh lesions did not impact acquisition of the DNMS rule, they did impair performance when the delays were extended from 30s to 600s. In contrast, the same neonatal lesions had no impact on either the object or spatial memory span tasks, suggesting that the lesions impacted the maintenance of information across longer delays and not memory capacity. Finally, the magnitude of recognition memory impairment after the Neo-PRh lesions was similar to that previously observed after adult-onset perirhinal lesions, indicating minimal, or no, functional compensation after the early PRh lesions. Overall, the results indicate that the PRh is a cortical structure that is important for the normal development of mechanisms supporting object recognition memory. Its contribution may be relevant to the memory impairment observed with human cases of temporal lobe epilepsy without hippocampal sclerosis, but not to the memory impairment found in developmental amnesia cases.

Keywords: Developmental amnesia; Excitotoxic lesion; Medial temporal lobe epilepsy; Memory span; Recognition; Rhesus macaque.

Figure 1

Coronal MR images from a representative case (Neo-PRh-2). Pre-surgical structural T1-weighed images (left column) at three rostro-caudal levels through the perirhinal cortex. Post-surgical coronal FLAIR images (right column) show the extent of hypersignals (white areas) indicative of edema and cell damage caused by injection of ibotenic acid. Arrows point to the rhinal sulcus on the left and to the hypersignals on the right.

Figure 2

Average percent correct (± SEM) on DNMS at delays of 30s, 60s, 120s, and 600s for animals with neonatal perirhinal lesions (open squares, dashed line) and controls (filled circles, solid line). Chance is at 50%.

Figure 3

Average percent correct (± SEM) on DNMS at delays of 30s, 60s, and 120s for animals with early-onset perirhinal lesions (Neo-PRh: open squares, dashed line) and their controls (Neo-C: filled circles, solid line) and those with late-onset perirhinal lesions (Adult-PRh: open diamonds, dashed line) and their controls (Adult-C: filled triangles, solid line). Chance is at 50%.