Research reportThe effects of neurotoxic lesions of the perirhinal cortex combined to fornix transection on object recognition memory in the rat
Introduction
The last 10 years have seen an important revision of ideas concerning the contributions of temporal lobe structures to mnemonic processes. One of the most important sources of evidence has come from studies into the effects of temporal lobe lesions in monkeys performing a test of object recognition, delayed nonmatching-to-sample (DNMS). It had largely become accepted that combined lesions of the amygdala and hippocampus were responsible for the very severe DNMS deficits seen after medial temporal lobe lesions 19, 46. This view had, however, to be radically altered when it was convincingly shown that much, maybe all, of this deficit was the consequence of damage to the rhinal cortices which lie immediately lateral to the amygdala and hippocampus 21, 22, 32, 45. Further evidence for the importance of the rhinal region has come from electrophysiological studies in behaving monkeys which have identified cells in the rhinal cortex that respond differentially to familiar stimuli [6]. These findings have led to a need to understand more about the functions of the rhinal region and determine its relationship with other temporal lobe structures, most notably the hippocampus.
The present study examined the functional contributions of the rhinal cortex in the rat. The study had two principal goals. The first was to help more clearly identify those cortical regions that are necessary for recognition. The second was to further understand the functional relationship between the rhinal cortices and the hippocampus. The first goal was aided by the fact that it is now possible to make relatively discrete rhinal lesions in rats using cytotoxic agents, and so help to exclude the contribution of fibres of passage or adjacent fibre tracts. It was further aided by a recent, comprehensive description of the anatomy of the rhinal regions in the rat [7]. In this, the rhinal region has been divided into two major dorsal areas, the more rostral perirhinal cortex and the more caudal postrhinal/parahippocampal cortex [7]. Ventral to both is the entorhinal cortex. Both the perirhinal and postrhinal regions receive an array of sensory inputs from multiple neocortical association areas, and both project to the hippocampus via the entorhinal cortex 7, 40. There are however a number of differences in the connectivity of these two regions, including their connections within the entorhinal cortex [7]. In view of these anatomical distinctions we examined the effects of cytotoxic lesions centred in the perirhinal cortex, the most rostral of these rhinal regions.
These anatomical considerations lead to the second issue, the functional relationship between the rhinal cortices and the hippocampus. Although it has been popular to assume that both the rhinal cortex and the hippocampus work conjointly in a temporal lobe mnemonic system 10, 30, there is evidence that there might be a considerable degree of independence between the regions. For example, a double dissociation has been found between the effects of perirhinal lesions and fornix lesions in monkeys on a test of spatial memory and a test of scene recognition [14]. A similar result has recently been found for rats using spatial memory tasks (e.g. delayed nonmatching-to-position and T-maze delayed alternation) and object recognition [11]. For these reasons we included a second experimental group which received combined perirhinal and fornix lesions. We selected fornix transection rather than hippocampectomy as the former surgery mimics many of the effects of hippocampal damage but carries no risk of additional, unwanted damage to the rhinal cortex.
The animals were assessed with an eight arm radial maze and a spontaneous object recognition tests. Both tests involve working memory as the rats were required to retain specific information either about a place or an object that was used to determine choice behaviour for that session, but not for subsequent sessions. One of these, the radial arm maze, is a spatial test that is known to be sensitive to hippocampal and fornix damage. The other test, spontaneous object recognition, we have previously found to be affected by rhinal damage [11], but not by fornix transection 11, 12or medial septum lesions [13]. If the hippocampus comprises part of the same functional system as the perirhinal cortex, i.e. both structures form components of a temporal-hippocampal system, then adding fornix damage to a perirhinal lesion should not qualitatively change the effects of the cortical lesion, although it might accentuate the recognition deficit [5]. If, however, the two structures are involved in very different aspects of memory then the deficits following the combined lesion will differ qualitatively from those observed after just perirhinal damage.
Section snippets
Subjects
The subjects were 28 rats of a pigmented strain (DA) supplied by Bantin and Kingman (Hull, UK). Their weights at the time of surgery ranged from 230–245 g. They were housed individually and maintained on a light/dark cycle (14/10 h). During testing for the radial arm maze task they were put on a restricted diet (Labsure, ERM), but their body weights did not fall below 85% of normal. All rats were on ad lib water throughout.
Surgical and histological procedures
The rats were divided into three groups; perirhinal lesions (Prh, n=10),
Histological analysis
The fimbria/fornix lesions (Fig. 1a) produced very extensive damage to the fibre tract itself and in all cases it extended into the most rostral head of the hippocampus. In 15 rats (8 Fx and 7 Prh+Fx animals) the tract was completely severed bilaterally, while in the remainder (2 Fx and 1 Prh+Fx animals) only the most lateral tips of the fimbria were spared. In some cases the lesion also affected a small part of the corpus callosum. Slight damage was also observed in the extreme dorsal margin
Discussion
The behavioural effects of cytotoxic lesions in the perirhinal cortex (Prh) were compared with those of combined perirhinal lesions and fornix transection (Prh+Fx). All animals were tested postoperatively on a spatial (radial arm maze) and a nonspatial (spontaneous object recognition) test of working memory. Only the animals with fornix transection were impaired on the radial arm maze, a task known to be highly sensitive to hippocampal system damage 1, 24, 25. There was no evidence that
Acknowledgements
This research was supported by the Wellcome Trust M/90/3028. The authors wish to acknowledge the assistance of S. Nagle, S. Whiteley and Dr N. Neave.
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