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Rhinal Cortex Removal Produces Amnesia for Preoperatively The Journal of Neuroscience, November 1, 1997, 17(21):8536–8549 Rhinal Cortex Removal Produces Amnesia for Preoperatively Learned Discrimination Problems But Fails to Disrupt Postoperative Acquisition and Retention in Rhesus Monkeys Jennifer A. Thornton,1,2 Lawrence A. Rothblat,2 and Elisabeth A. Murray1 1Laboratory of Neuropsychology, National Institute of Mental Health, Bethesda, Maryland 20892, and 2Department of Psychology, The George Washington University, Washington, DC 20052 To test whether the rhinal cortex (i.e., entorhinal and perirhinal sets (i.e., no temporal gradient). In addition, the monkeys with cortex) plays a time-limited role in information storage, eight rhinal cortex lesions subsequently learned three new sets of 10 rhesus monkeys were trained to criterion on two sets of 60 object discrimination problems as quickly as the controls did, object discrimination problems, one set at each of two different thus ruling out the possibility of a gross impairment in visual time periods separated by 15 weeks. After the monkeys had perception or discrimination abilities. Furthermore, they re- learned both sets, two groups balanced for preoperative acqui- tained these postoperatively learned object discriminations as sition rates were formed. One group received bilateral ablation well as the controls did. The findings indicate that the rhinal of the rhinal cortex (n 5 4), and the other was retained as an cortex is critical for the storage and/or retrieval of object dis- unoperated control group (n 5 4). After a 2 week rest period, crimination problems that were learned up to 16 weeks before monkeys were assessed for retention of the object discrimina- rhinal cortex ablation; however, in the absence of the rhinal tion problems. Retention was significantly poorer in monkeys cortex, efficient learning and retention of new discrimination with removals of the rhinal cortex relative to the controls (68 vs problems can still occur. 91%). Although both groups showed slightly better retention of Key words: visual discrimination; stimulus memory; retro- problems from the more recently learned set, there was no grade amnesia; entorhinal cortex; perirhinal cortex; rhesus evidence of a differential effect of the cortical removal across monkey Bilateral damage to the medial temporal lobe in humans typically for at least some types of information, a picture that is consistent results in a temporally graded retrograde amnesia, in which with clinical findings. However, it has recently been established in recent memories are lost although remote memories are spared, monkeys that the rhinal cortex (i.e., entorhinal and perirhinal as well as severe anterograde amnesia, which is characterized by cortex) and the hippocampal formation have dissociable roles in rapid forgetting of new information (e.g., Scoville and Milner, memory (Meunier et al., 1993; Murray et al., 1993; O’Boyle et al., 1957). The phenomenon of temporally graded retrograde amne- 1993; Eacott et al., 1994; Gaffan, 1994a; Murray and Mishkin, sia is consistent with the idea of memory consolidation (see 1996). If the rhinal cortex and the hippocampal formation have McGaugh and Herz, 1972) and with the idea that the role of dissociable roles in the acquisition of information, as the forego- medial temporal lobe structures is only temporary. Presumably, as ing studies suggest, they may also make independent contribu- time passes after the original learning episode, memories that tions to the long-term storage of information. These consider- were initially dependent on these areas are eventually consoli- ations suggest that the role of the rhinal cortex in the retention of dated into a more permanent state elsewhere (for review, see information should be evaluated separately from that of the Squire and Alvarez, 1995). hippocampus. Zola-Morgan and Squire (1990) found that monkeys with dam- Accordingly, in Experiment 1 we examined the effect of rhinal age to the hippocampal formation, entorhinal cortex, and para- cortex ablation on the retention of two sets of object discrimina- hippocampal cortex exhibited temporally graded retrograde am- tion problems learned at two different time periods [16 and 1 nesia, and they concluded that the hippocampal formation has a week(s)] before surgery. The 16 week training–surgery interval time-limited role in memory. Furthermore, similar findings have was chosen, in part, because it exceeds that at which hip- now been reported in rats (Winocur, 1990; Kim and Fanselow, pocampectomized monkeys have been found to have intact re- 1992; cf. Bolhuis et al., 1994; Cho et al., 1995) and rabbits (Kim tention of preoperatively learned discriminations (Zola-Morgan et al., 1995) after lesions of the hippocampal formation. Thus, it and Squire, 1990). If the rhinal cortex is critical for information seems that the hippocampal formation acts as a temporary store storage or retrieval for only a limited period of time, as hypoth- esized, then the operated monkeys would exhibit good retention Received June 3, 1997; revised Aug. 13, 1997; accepted Aug. 15, 1997. relative to controls of the object discrimination problems learned We thank Tinera Fobbs, Wendy Hadfield, Dino Peralta, and John Sewell for their long before surgery but poor retention of the problems learned valuable technical support, Norbert Vnek for helpful comments during the initial planning of these experiments, and Mortimer Mishkin, Mark Baxter, and Robert immediately before surgery. By contrast, if the rhinal cortex is Hampton for comments on an earlier version of this manuscript. critical for storage or retrieval over a longer period of time, then Correspondence should be addressed to Dr. Elisabeth A. Murray, Laboratory of the operated monkeys would exhibit poor retention of the object Neuropsychology, National Institute of Mental Health, Building 49, Room 1B80, 49 Convent Drive, Bethesda, MD 20892-4415. discriminations learned at both time points. Copyright © 1997 Society for Neuroscience 0270-6474/97/178536-14$05.00/0 In Experiment 2 we examined the effect of rhinal cortex abla- Thornton et al. • Rhinal Cortex and Object Discrimination J. Neurosci., November 1, 1997, 17(21):8536–8549 8537 Figure 1. Shaded regions indicate the location and extent of the intended le- sions of the rhinal cortex. A, Ventral view of a rhesus monkey brain. B, Coro- nal 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. tion on acquisition and retention of postoperatively learned ob- received the rhinal cortex lesions, and the other (Con) was kept as an ject discrimination problems. There were two main goals. First, unoperated control group. we wanted to clarify the nature of the impairment, if any, that Surgery might be observed in Experiment 1. That is, if monkeys with Bilateral ablation of the rhinal cortex was performed in a single stage of rhinal cortex lesions were impaired in Experiment 1, it would be surgery and was performed under visual control with the aid of an useful to assess their postoperative learning abilities with the operating microscope. Figure 1 illustrates the extent of the intended same kinds of stimulus material to determine whether there was lesion. Monkeys were immobilized with ketamine hydrochloride (10 mg/kg, i.m.) and anesthetized with isoflurane (1.0–2.0%, to effect); they a global impairment in visual perception or discrimination. Sec- received an intravenous drip of isotonic fluids, and heart rate, respiration ond, we sought to determine whether rhinal cortex lesions would rate, body temperature, and expired CO2 were closely monitored cause abnormally rapid forgetting of postoperatively acquired throughout the procedure. After establishment of the aseptic field and object discrimination problems. skin incision, the zygoma was removed to allow access to the portion of the cranium overlying the ventrolateral surface of the frontal and tem- Parts of this paper have been published previously in abstract poral lobes. Then the temporalis muscle was reflected, and a large bone form (Thornton and Murray, 1996). flap was made; the flap extended rostrally to the orbit, ventrally to the base of the temporal fossa, and caudally to the auditory meatus. Two EXPERIMENT 1 approaches were used for the ablation. First, a dural flap was cut over the Materials and methods frontal and anterior part of the temporal lobes. Using a supraorbital approach, we gently retracted the frontal lobe from the orbit with a brain Subjects spoon, and the anterior part of the rhinal cortex was removed with a Eight experimentally naive rhesus monkeys (Macaca mulatta) weighing small-gauge sucker. This part of the lesion extended along the anterior between 3.3 and 7.2 kg at the beginning of testing were used; six of the face of the temporal pole from the lateral fissure to the floor of the monkeys were male, and two were female. They were housed in individ- temporal fossa and included the cortex lining the banks of the rhinal ual cages in rooms with regular 12 hr light/dark cycles and were fed a diet sulcus as well as ;2 mm of cortex both medial and lateral to the sulcus. of monkey chow (PMI Feeds Inc., St. Louis, MO) supplemented with After this part of the removal was completed, the dura was sewn over the fruit. The monkeys were later divided on the basis of their preoperative frontal lobe, and then an additional dural flap was cut over the lateral part performance into two groups of four animals each. One group (Rh) of the temporal lobe. A subtemporal approach was used for ablation of 8538 J. Neurosci., November 1, 1997, 17(21):8536–8549 Thornton et al. • Rhinal Cortex and Object Discrimination Table 1. Rhinal cortex damage PRh damage ERh damage Total Rh damage Case L% R% X% W% L% R% X% W% L% R% X% W% Rh-1 100 84 92 84 71 64 68 46 86 75 80 64 Rh-2 100 99 99 99 91 77 84 70 96 89 92 85 Rh-3 100 100 100 100 79 79 79 62 90 90 90 81 Rh-4 96 73 85 71 77 63 70 48 87 68 78 60 X 99 89 94 88 80 71 75 57 90 80 85 72 Estimated damage (as a percentage of normal volume) to perirhinal (PRh), entorhinal (ERh), and rhinal (Rh) cortex in each subject.
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