Rhinal cortex removal produces amnesia for preoperatively learned discrimination problems but fails to disrupt postoperative acquisition and retention in rhesus monkeys

Abstract

To test whether the rhinal cortex (i.e., entorhinal and perirhinal cortex) plays a time-limited role in information storage, eight rhesus monkeys were trained to criterion on two sets of 60 object discrimination problems, one set at each of two different time periods separated by 15 weeks. After the monkeys had learned both sets, two groups balanced for preoperative acquisition rates were formed. One group received bilateral ablation of the rhinal cortex (n = 4), and the other was retained as an unoperated control group (n = 4). After a 2 week rest period, monkeys were assessed for retention of the object discrimination problems. Retention was significantly poorer in monkeys with removals of the rhinal cortex relative to the controls (68 vs 91%). Although both groups showed slightly better retention of problems from the more recently learned set, there was no evidence of a differential effect of the cortical removal across sets (i.e., no temporal gradient). In addition, the monkeys with rhinal cortex lesions subsequently learned three new sets of 10 object discrimination problems as quickly as the controls did, thus ruling out the possibility of a gross impairment in visual perception or discrimination abilities. Furthermore, they retained these postoperatively learned object discriminations as well as the controls did. The findings indicate that the rhinal cortex is critical for the storage and/or retrieval of object discrimination problems that were learned up to 16 weeks before rhinal cortex ablation; however, in the absence of the rhinal cortex, efficient learning and retention of new discrimination problems can still occur.

Fig. 1.

Shaded regions indicate the location and extent of the intended lesions of the rhinal cortex.A, Ventral view of a rhesus monkey brain.B, Coronal sections from levels through the temporal lobe in a rhesus monkey brain. C, Medial aspect of both hemispheres. The numerals indicate the distance in millimeters from the interaural plane.

Fig. 2.

Extent of the rhinal cortex lesion in Rh-1.A, Ventral view (reversed to aid in matching to coronal sections). B, Coronal sections; thick black lines indicate the line along which the lesion was made.C, Medial aspect of both hemispheres. In bothA and C, shaded areasindicate the extent of the lesion reconstructed from individual sections. The numerals indicate the distance in millimeters from the interaural plane. Compare and contrast with Figure1.

Fig. 3.

Extent of the rhinal cortex lesion in Rh-2.A, Ventral view (reversed to aid in matching to coronal sections). B, Coronal sections; thick black lines indicate the line along which the lesion was made.C, Medial aspect of both hemispheres. In bothA and C, shaded areasindicate the extent of the lesion reconstructed from individual sections. The numerals indicate the distance in millimeters from the interaural plane. Compare and contrast with Figure1.

Fig. 4.

Extent of the rhinal cortex lesion in Rh-3.A, Ventral view (reversed to aid in matching to coronal sections). B, Coronal sections; thick black lines indicate the line along which the lesion was made.C, Medial aspect of both hemispheres. In bothA and C, shaded areasindicate the extent of the lesion reconstructed from individual sections. The numerals indicate the distance in millimeters from the interaural plane. Compare and contrast with Figure1.

Fig. 5.

Extent of the rhinal cortex lesion in Rh-4.A, Ventral view (reversed to aid in matching to coronal sections). B, Coronal sections; thick black lines indicate the line along which the lesion was made.C, Medial aspect of both hemispheres. In bothA and C, shaded areasindicate the extent of the lesion reconstructed from individual sections. The numerals indicate the distance in millimeters from the interaural plane. Compare and contrast with Figure1.

Fig. 6.

Photomicrographs of Nissl-stained coronal sections from a monkey with a bilateral rhinal cortex lesion (Rh-2). SectionsA, B, and C are approximately +20, +16, and +13 mm from the interaural plane, respectively. Compare and contrast with Figure 3.

Fig. 7.

Photomicrographs of Nissl-stained coronal sections from a monkey with a bilateral rhinal cortex lesion (Rh-3). SectionsA, B, and C are approximately +20, +16, and +13 mm from the interaural plane, respectively. Compare and contrast with Figure 4.

Fig. 8.

Mean rates of original (preoperative) learning of each set of object discrimination problems. The dashed line denotes chance performance. Con, Unoperated controls; Rh, monkeys assigned to receive bilateral ablations of the rhinal cortex. Remote, Object discrimination problems learned 16 weeks before surgery or rest;Recent, object discrimination problems learned 1 week before surgery or rest.

Fig. 9.

Mean percent correct responses on critical trials as a function of training period. Con, Unoperated controls; Rh, monkeys with bilateral ablations of the rhinal cortex; Remote, object discrimination problems learned 16 weeks before surgery or rest; and Recent, object discrimination problems learned 1 week before surgery or rest.Open triangle, Rh1; open diamond, Rh2;open circle, Rh3; open square, Rh4;filled triangle, Con1; filled diamond, Con2; filled circle, Con3; and filled square, Con4.

Fig. 10.

Average percent savings in the total number of incorrect responses during relearning of each set. Vertical bars represent the range of scores in each group.Con, Unoperated controls; Rh, monkeys with bilateral ablations of the rhinal cortex; Remote, object discrimination problems learned 16 weeks before surgery or rest; and Recent, object discrimination problems learned 1 week before surgery or rest.

Fig. 11.

Mean number of errors for each group during acquisition and retention of 10 object discrimination problems presented at 24 hr intertrial intervals. Vertical barsrepresent the range of scores in each group. Con, Unoperated controls; Rh, monkeys with bilateral ablations of the rhinal cortex.

Fig. 12.

Average number of errors (including the criterion run) for each group during acquisition and retention of 10 object discrimination problems presented with massed trials.Con, Unoperated controls; Rh, monkeys with bilateral ablations of the rhinal cortex. Open triangle, Rh1; open diamond, Rh2; open circle, Rh3; open square, Rh4; filled triangle, Con1; filled diamond, Con2;filled circle, Con3; and filled square, Con4.

Fig. 13.

Average number of errors (including the criterion run) for each group during acquisition and retention (reversals) of 10 object discrimination problems presented with massed trials. Con, Unoperated controls; Rh, monkeys with bilateral ablations of the rhinal cortex. Open triangle, Rh1; open diamond, Rh2; open circle, Rh3; open square, Rh4; filled triangle, Con1; filled diamond, Con2;filled circle, Con3; and filled square, Con4.