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 ϭ 4), and the other was retained as an unoperated control group (n ϭ 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. Key words: visual discrimination; stimulus memory; retrograde amnesia; entorhinal cortex; perirhinal cortex; rhesus monkeyBilateral damage to the medial temporal lobe in humans typically results in a temporally graded retrograde amnesia, in which recent memories are lost although remote memories are spared, as well as severe anterograde amnesia, which is characterized by rapid forgetting of new information (e.g., Scoville and Milner, 1957). The phenomenon of temporally graded retrograde amnesia is consistent with the idea of memory consolidation (see McGaugh and Herz, 1972) and with the idea that the role of medial temporal lobe structures is only temporary. Presumably, as time passes after the original learning episode, memories that were initially dependent on these areas are eventually consolidated into a more permanent state elsewhere (for review, see Squire and Alvarez, 1995).Z ola-Morgan and Squire (1990) found that monkeys with damage to the hippocampal formation, entorhinal cortex, and parahippocampal cortex exhibited temporally graded retrograde amnesia, and they concluded that the hippocampal formation has a time-limited role in memory. Furthermore, similar findings have now been reported in rats (Winocur, 1990;K im and Fanselow, 1992; cf. Bolhuis et al., 1994;Cho et al., 1995) and rabbits (Kim et al., 1995) after lesions of the hippocampal formation. Thus, it seems that the ...

Visual habit formation in monkeys with neurotoxic lesions of the ventrocaudal neostriatum

“…As already noted, damage to the perirhinal͞entorhinal cortices produces a behavioral pattern that is just the opposite of the one observed here, namely an impairment in visual recognition memory but not in visual habit formation (14)(15)(16)(17)(18)(19)(20)(21)(22)(23)(24)(26)(27)(28). Further, each of these patterns differs from the one produced by damage to TE, which yields impairments in both types of visual learning and memory (31,32).…”

“…One of these targets, the inferior prefrontal convexity (1)(2)(3)(4)(5), is essential for short-term visual memory (6)(7)(8), whereas the second, the perirhinal͞ entorhinal cortices in the medial temporal lobe (9)(10)(11)(12)(13), is critical for the long-term recognition of visual stimuli and of their associations with other stimuli (14)(15)(16)(17)(18)(19)(20)(21)(22). Neither of these areas, however, seems to contribute substantially to still another type of visual learning known as visual habit formation (23)(24)(25)(26)(27)(28). Unlike the various forms of short-and long-term memory that allow cognitive retention of stimuli and of stimulus-stimulus associations, often after only a single presentation and on the basis of visual observation alone, habits are considered to be stimulus-response connections formed gradually through trial and error on the basis of differential reinforcement of the instrumental response (29,30).…”

DNA targeting of rhinal cortex D2 receptor protein reversibly blocks learning of cues that predict reward

“…Thus, the monkeys had no difficulty discriminating the visual cues from one another. Third, previous studies have shown that monkeys with bilateral rhinal cortex removals can learn visual discrimination problems at the same rate as intact controls (36)(37)(38)(39). Therefore, it is likely that the deficit we observed is specific to learning the associations between visual cues and workload, as opposed to a visual perceptual impairment.…”

The effects of lesions to the rat hippocampus or rhinal cortex on olfactory and spatial memory: Retrograde and anterograde findings

“…Recent work has shown that RA can follow lesions of the perirhinal cortex (Eacott, 1998;Myhrer & Wangen, 1996;Wiig, Cooper, & Bear, 1996), the entorhinal cortex (Cho et al, 1993;Cho & Kesner, 1996), and the PRER (Thornton, Rothblat, & Murray, 1997), in addition to lesions of the hippocampus (Bolhuis, Stewart, & Forrest, 1994;Kim, Clark, & Thompson, 1995;Kim & Fanselow, 1992;Salmon, Zola-Morgan, & Squire, 1987;Winocur, 1990;Zola-Morgan & Squire, 1990). However, few studies have directly compared the contribution of these different hippocampal components (but see Bolhuis et al, 1994;Wiig et al, 1996).…”

“…This prediction follows from the straightforward reasoning that lesions of the hippocampus do not disrupt postoperative acquisition of discrimination learning (Vnek & Rothblat, 1996;Zola-Morgan et al, 1982). Given the recent studies implicating the perirhinal and/or the entorhinal cortex in retrograde and anterograde recognition memory (e.g., Cho et al, 1993;Cho & Kesner, 1996;Myhrer, 1992;Myhrer & Johannesen, 1995;Thornton et al, 1997), it is tenable that only damage including the rhinal cortex will interfere with memories formed prior to a lesion. Furthermore, inasmuch as the hippocampus is largely uninvolved in the processing of such nonrelational information, we may thus expect it to have no significant role in the consolidation of simple discriminations.…”