Research reportLesions of the primate rhinal cortex cause deficits in flavour–visual associative memory
Introduction
In recent years, evidence has been accumulating that the rhinal cortex has an important role in memory performance that involves visual knowledge about objects. The impairment seen after lesions of either the perirhinal cortex alone or lesions which include both perirhinal and entorhinal cortices (rhinal lesions) is noticeable both in recognition memory performance 7, 13 and in associative memory performance when memory is taxed by either increasing the number of visual objects, increasing the number of foils at choice or presenting different object views 3, 4. Both single cell recording [10] and cooling studies [11] in primates have also added evidence that this region of cortex is important in object memory performance.
As well as its role in memory for the visual properties of objects, the rhinal area is important in crossmodal tactual–visual recognition memory [9]. Crossmodal memory can also be explored with conditional associative tasks, in which the animal must learn to choose between two items in one sensory modality dependent on an instruction cue presented in a different modality. A deficit in a conditional test of auditory–visual crossmodal associative memory has been shown after lesions of the amygdala and subjacent cortex, including part of the rhinal cortex [16]. The present experiment uses a flavour–visual conditional task, in which the monkey must learn which of two stimulus objects, identified visually, are associated with the flavour of either a peanut or a raisin.
The issue of flavour–visual associative memory is of particular interest due to the marked Kluver–Bucy signs of increased orality and food preference abnormalities seen in humans with anteromedial temporal lobe damage, and in monkeys after amygdala lesions which include rhinal cortex 2, 22. It is not yet clear precisely what role the amygdala and rhinal cortex play in the abnormal behaviours seen in Kluver–Bucy syndrome. A recent series of experiments by Murray et al. [17] has compared the effects of excitotoxic amygdala lesions with the effects of anterior rhinal cortex lesions on recognition memory performance and on a test of food preference. They found a dissociation between recognition memory impairments after rhinal lesion and not after amygdalar damage, compared with unusual food preference behaviour after amygdala lesion, but not after rhinal cortex lesion [17].
Anatomical studies of the connections of the perirhinal and entorhinal cortices show that the perirhinal cortex has dense reciprocal connections with TE [20], and that the subdivision of the entorhinal cortex designated region Eo by Amaral et al. [1] receives a direct input from the olfactory bulb and a strong input from the piriform cortex. There are also extensive, reciprocal, connections between the perirhinal and entorhinal cortices. This pattern of connections, in addition to the lesion evidence of increased orality and food preference abnormalities discussed above, suggests that the rhinal cortex is a possible site for the interaction of visual and flavour memory. Research on human subjects 14, 15 has indicated that between 70% and 80% of information about the flavour of food items is olfactory in nature, with only the remaining 20–30% consisting of gustatory information. In a previous disconnection study we showed that olfactory–visual associations depend on intrahemispheric olfactory–visual interaction [19]. The present experiment examines whether crossmodal flavour–visual memories are disrupted by removal of the rhinal cortex. The behavioural task, both pre- and postoperative, was to associate the flavour of an instruction cue, a piece of free food (a peanut versus a sultana), with one of two choice stimuli, which were visually distinctive objects, one of which was always rewarded in conjunction with the sultana instruction cue, and the other in conjunction with the peanut instruction cue. Performance on a food preference test was also assessed.
Section snippets
Subjects
Three male Cynomolgus monkeys (Macaca Fascicularis) served as subjects. All three animals were experimentally naive. At the time of surgery they weighed on average 8.3 kg.
Surgery
Operations were carried out under aseptic conditions, and the monkeys were anaesthetized throughout surgery with barbiturate (thiopentone sodium) administered through an intravenous cannula. The arch of the zygoma was removed and the temporal muscle was detached from the cranium and retracted. A bone flap was raised over the
Preoperative training
The animals learned the flavour–visual conditional learning task in light in a mean of 1100 trials (range 700–1730). Then they learned the same task in the dark in a mean of 493 trials (range 450–530).
Flavour–visual conditional learning: pre- and postoperative performance tests
As shown in Table 1 and Fig. 2, following surgery severely impaired performance was observed in all three monkeys. In the preoperative retention test all three animals performed at a very high level, making an average of six errors. In contrast, in the postoperative performance test there was
Discussion
Removal of the rhinal cortex disrupted the ability to perform conditional visual discriminations which were dependent on the flavour of a non-visual instruction cue. Postoperative performance on the food preference test showed that the problems associating a flavour cue with a visual object in the conditional learning task also extended to aberrant choice of foods based on their visual appearance.
There are two possible interpretations of the impairment in the food preference test shown by the
Acknowledgments
This research was supported by the UK Medical Research Council. We thank Judi Wakeley for help in training the monkeys.
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