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The Hippocampus and Long-Term Object Memory in the Rat The Journal of Neuroscience, April 15, 1996, 16(8):2780-2787 The Hippocampus and Long-Term Object Memory in the Rat Norbert Vnek and Lawrence A. Rothblat Department of Psychology, George Washington University, Washington, DC 20052 Animal models of amnesia have yielded many insights into the ration lesions of the dorsal hippocampus, rats with neocot-tical neural substrates of different types of memories. Some very control lesions, and normal controls were trained on three important aspects of memory, however, have been ignored in object discrimination problems and then retrained 3 weeks later research using experimental animals. For example, to examine to measure retention. All animals showed the same level of long-term memory investigators traditionally have relied on performance during the training (acquisition) phase of testing, measures of information acquisition, which stand in contrast but the performance of animals with dorsal hippocampal injury to the measures of retention commonly used in work with fell below that of controls during retraining (retention). Taken humans. We have recently developed a behavioral paradigm together, these and our earlier results suggest that the hip- that measures both the acquisition and long-term retention pocampus and anatomically related structures are particularly of object discriminations, and found a selective retention im- important for retaining visual discriminations over long delay pairment in rats with entorhinal-hippocampal disconnection intervals. These findings may clarify the role of the hippocam- (Vnek et al., 1995). pus in nonspatial memory. The present study was designed to determine whether direct damage to the hippocampus likewise would lead to a selective Key words: acquisition; retention; amnesia; nonspatial mem- deficit in the retention of visual discriminations. Rats with aspi- ory; entorhinal cortex; hippocampus The medial portion of the temporal lobe is important for memory time (i.e., 15-20 set) to study a set of pictures, H. M. can (for review, see Murray, 1992; Squire, 1992; Jarrard, 1993; Zola- perform at the level of controls on certain memory tests (e.g., Morgan and Squire, 1993; Mishkin and Murray, 1994). Evidence yes/no recognition judgments) after delay intervals of up to 1 d, of this comes from studies of human clinical populations with but his performance drops dramatically when longer intervals amnesia and known or suspected medial temporal pathology (1 week or more) are used (Huppert and Piercy, 1979; Freed (Scoville and Milner, 19.57; Zola-Morgan et al., 1986; Braak and and Corkin, 1988). These results underscore the importance of Braak, 1993). However, because of the rarity of circumscribed measuring extended delay intervals in behavioral paradigms lesions in human patients, animal models of amnesic disorders used with experimental animals. have been developed so that more precise functional neuroana- Although some animal models of amnesia have measured long- tomical studies are possible. term memory, the tasks used to do so typically depart from those Perhaps the most widely modeled amnesic patient is H. M., who administered to human clinical populations in some very impor- underwent bilateral medial temporal resection in 1953 and whose tant respects. In studies with humans, subjects are shown a list of consequent memory functions and dysfunctions have since been stimuli, a delay interval is imposed, and a test of retention (recall studied intensively (Scoville and Milner, 1957). H. M.‘s memory or recognition) follows. In contrast, with the exception of a few appears normal within the parameters of short-term memory, but early studies (Orbach et al., 1960; Correll and Scoville, 1965) is typically grossly impaired when he is called on to remember investigations of long-term memory in experimental animals have information in excess of those parameters (Wickelgren, 1968). rarely used behavioral paradigms that assess both the acquisition Impaired long-term memory in the face of normal short-term and retention of the same set of stimuli. For example, a measure memory is in fact a defining feature of medial temporal amnesia. of long-term nonspatial memory commonly used in animal models Thus, to examine medial temporal amnesia in both human patient of amnesia is the concurrent object discrimination task, in which populations and experimental animals, it is imperative to assess the dependent variable is the amount of training needed to reach long-term memory functions. criterion on several discrimination problems (Moss et al., 1981; Behavioral paradigms used to measure memory in animal Zola-Morgan and Squire, 1985). This task is to a large extent an models commonly use visual discriminations, usually objects, as index of information acquisition, and as such is more a measure of stimuli. The validity of these tasks can be assessed by compar- learning than memory. ing the performance of lesioned animals to that of human amnesics on analogous memory tests. When given extended We have recently developed a behavioral paradigm that mea- sures both the acquisition and long-term retention of visual dis- crimination problems in rats (Vnek et al., 1995). On this task, rats Received Oct. 26, 1995; revised Jan. 4, 1996; accepted Jan. 8, 1996. This work was supported by Alzheimer’s Association Grant PRG-94-172. with entorhinal- hippocampal disconnection from angular bundle Correspondence should be addressed to Dr. Lawrence A. Rothblat, Department transections show normal acquisition but impaired retention over of Psychology, George Washington University, Washington, DC 20052. a 2 week interval. The present study was conducted to determine Dr. Vnek’s present address: Section of Neurobiology, Yale University School of Medicine, New Haven, CT 06510. whether direct damage to the hippocampus would likewise lead to Copyright 0 1996 Society for Neuroscience 0270-6474/96/162780-08$05.00/O a selective retention deficit. Vnek and Rothblat l Hippocampus and Long-Term Memory J. Neurosci., April 15, 1996, 76(8):2780-2787 2781 MATERIALS AND METHODS positioned 13 cm behind the entrance ridge. Around the front (facing the Subjects. The subjects were 18 male Wistar rats (Charles River, ridge and runway) of the food well, five small holes were drilled into the Wilmington, MA). All animals were -120 d old at the start of the insert, each of which contained one 45 mg food pellet (Noyes, Lancaster, experiment and weighed between 400 and 500 gm. Animals were food- NH). These pellets were used to mask the smell of the food pellets used deprived to 85% of normal body weight during behavioral testing. to reward animals during object discrimination testing so that olfactory Dorsal hippocampal lesions were chosen instead of removing the entire cues could not be used to learn the discriminations. Between trials, hippocampus because recent studies have shown that the size of dorsal animals were restrained from traversing the runway with a removable 40 hippocampal lesions in rats is directly related to spatial memory impair- X 20 cm free standing door, which was placed 25 cm from the beginning ments whereas the size of ventral hippocampal lesions is not (Moser et of the runway. al., 1993, 1995). Based on the assumption that the relative importance of Procedure. On the object discrimination task, rats were trained on three the dorsal hippocampus can be extended to nonspatial memory, the successive object discrimination problems and then later retrained on lesions of the present study were intended to involve only this division of these discriminations to measure retention. The protocol for behavioral the hippocampus. Dorsal hippocampal lesions also can be achieved testing was identical to that of Vnek et al. (1995) except that a 3 week without damaging rhinal (i.e., entorhinal and perirhinal) cortex, which delay interval was used in the present study rather than the 2 week principally surrounds the ventral hippocampus in the rat. Avoiding dam- interval of our earlier study. For a given problem, each object from the age to this area is critical because lesions limited to rhinal cortex have test pair was placed on the food well of one of the goal arms of been found to lead to nonspatial memory impairments in both monkeys the Y-maze, although food pellets were placed only in the well that (Gaffan and Murray, 1992; Meunier et al., 1993) and rats (Otto and held the predetermined correct object. At this time, the animal was Eichenbaum, 1992; Bunsey and Eichenbaum, 1993; Mumby and Pine& placed at the beginning of the runway and was prevented from traversing 1994). the runway by the restraining door. To start a trial, the door was removed Surgery. Nine rats received bilateral aspiration lesions of the dorsal and the animal was allowed to navigate the runway and enter a goal arm hippocampus, 5 rats served as unoperated controls, and 4 rats received of his choosing. The rat was then allowed to displace the object covering lesions controlling for the cortical damage included in hippocampal the food well of the goal arm he chose. A choice, whether correct or lesions. incorrect, was dctcrmincd to have been made when the animal’s front During surgery, animals were anesthetized with a mixture of ketamine paws crossed the ridge demarcating the entrance of one of the goal arms. (90 mg/kg) and xylazine (15 mg/kg), administered by intraperitoneal The placement of the stimuli (both correct and incorrect objects) on the injection. Surgery utilized a stereotaxic device, with the rat’s head in a arms of the maze (i.e., the left/right arm assignment) was randomized to level position for all surgical procedures, and was visually guided using a preclude use of spatial cues in learning the problems. After a choice was surgical microscope. made, the animal was returned to the beginning of the runway, and the Under anesthesia, animals were placed in the stereotaxic device, an restraining door was replaced until the start of the next trial. The incision was made in the skin overlaying the dorsal surface of the skull, intertrial interval was -10 sec.
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