Extensive Cytotoxic Lesions Involving Both the Rhinal Cortices and Area TE Impair Recognition But Spare Spatial Alternation in the Rat

https://doi.org/10.1016/S0361-9230(97)00007-5Get rights and content

Abstract

Rats with cytotoxic lesions of the perirhinal, postrhinal, and TE cortices (Rh+TE, n = 7) were compared with surgical control animals (n = 7) on a series of spontaneous object recognition tests. The Rh+TE group was associated with a failure to select the novel object. This recognition deficit contrasted with the apparently normal ability of the same animals to learn and perform a spatial working memory test (T-maze alternation). The animals were also tested on the acquisition of an automated visual discrimination task in which the stimuli were presented on a visual display unit (VDU) equipped with a touch screen. The animals with Rh+TE lesions showed only a borderline deficit on this task. These findings are consistent with other evidence implicating the rhinal region in recognition memory. More importantly, they also provide a dissociation between spatial working memory and object recognition and, hence, show that extensive rhinal lesions are not sufficient to disconnect the hippocampus functionally.

Introduction

A fundamental reevaluation of the relative contributions of the hippocampus and the adjacent temporal cortical regions to memory has occurred over the last few years. This has been prompted by lesion studies in monkeys that have demonstrated that cortex lateral to the hippocampus, most especially the perirhinal cortex, is vital for visual recognition [13, 16, 35]. Further support has come from electrophysiological studies, which have found cells in the same (perirhinal) region that consistently change their firing rate when visual stimuli are repeated, i.e., become familiar [3, 22]. In the light of these findings and the plentiful connections between the perirhinal cortex and the hippocampus [6, 25, 31] it has been proposed that in the primate brain these two regions function conjointly to form a medial temporal lobe memory system [7, 24]. Within this system, hippocampal function is thought to be heavily dependent upon inputs from the perirhinal cortex, while the perirhinal cortex retains some independent mnemonic functions [7, 14, 24].

It has more recently become evident that the perirhinal cortices of the rat are also involved in recognition memory. Lesions in this region can impair tests of object recognition [11, 15, 27] and olfactory recognition [[19]]. Furthermore, single-unit recordings have revealed the presence of cells in the perirhinal cortex and area TE that change their responses to familiar stimuli in a manner very similar to that found in monkeys [[32]]. Other evidence has come from the expression of the immediate early gene c-fos, a marker of neuronal activity. When rats are shown novel objects an increase in c-fos expression occurs in a number of sites, including the perirhinal cortex and area TE but not the hippocampus [[33]]. In a subsequent experiment, novel objects were placed in the visual field of one eye of the rat while only familiar objects were visible to the other eye [[34]]. This “paired viewing” procedure, which helped to ensure that any differential c-fos expression was not a result of changes in activity or arousal, led to a greater expression of c-fos in both the perirhinal cortex and area TE in the hemisphere receiving inputs from the eye exposed to novel stimuli [[34]].

The consistent involvement of area TE in electrophysiological and c-fos expression studies indicates that this region, along with the perirhinal cortex, might be involved in object recognition. This evidence led to the present study, which examined the effects of cytotoxic lesions that were intended to involve both the perirhinal cortex and area TE. The lesions were also intended to extend caudally so as to involve the recently described “postrhinal” region [[4]], which receives many visual inputs. It was predicted that this extensive lesion might produce more robust object recognition deficits than those observed after relatively selective cytotoxic lesions centred in the perirhinal cortex [[11]]. To examine recognition we measured the differential exploration of novel and familiar objects by rats, a procedure that takes advantage of their spontaneous preference for novelty [[10]].

This study also provided the opportunity to assess whether the loss of these cortical regions (rhinal plus TE) functionally disconnects the hippocampus. In a previous experiment it was found that neurotoxic lesions of the perirhinal cortex, which spared much of the postrhinal cortex, did not disrupt tests of spatial memory that are sensitive to hippocampal damage [9, 11]. This dissociation was reexamined in the present study as the cortical lesions were more extensive and so might provide a more complete disconnection of entorhinal/hippocampal afferents. For this reason the rats were tested on a spatial alternation task, known to be sensitive to hippocampal dysfunction [1, 21]. Finally, the rats were tested on a visual discrimination task in which the stimuli were displayed on a computer touch screen [[5]]. This arrangement made it possible to present stimuli of matched luminance, to better assess the nature of any visual deficits.

Section snippets

Subjects

The study involved 14 male rats of the pigmented DA strain (Bantin and Kingman, Hull). Throughout the period of the experiment the animals were housed in pairs under diurnal conditions (14 h light/10 h dark). At the time of surgery they were aged 8 months and weighed between 252 g and 318 g. Three months prior to surgery all rats had been used in a study that assessed the effects of lorazepam (IM) on spontaneous object recognition.

Surgical and Histological Procedures

The rats were divided into two groups; rhinal and TE lesions (Rh

Histological Analysis

The Rh+TE lesions consistently removed all of the perirhinal tissue at the levels depicted in Fig. 1 and Fig. 2. As intended, the lesions extended caudally and involved virtually all of the postrhinal area and that portion of area TE dorsal and rostral to the rhinal region. Within the extent of the lesion there was little or no evidence of neuronal sparing. At more rostral levels the lesions consistently encroached ventrally to include the most lateral parts of the piriform cortex, while more

Discussion

The present study examined the behavioural effects of cytotoxic lesions of the rhinal cortices (perirhinal plus postrhinal) and the adjacent area TE. The principal goals were to determine if the loss of this tissue would produce a severe visual recognition deficit and whether a functional disconnection of the hippocampus would result. Previous studies have indicated that damage to perirhinal cortex can disrupt recognition in rats [11, 15, 27], but in those studies using spontaneous exploration

Acknowledgements

This research was supported by a grant from the Wellcome Trust.

References (35)

  • K.A Wiig et al.

    The effects of perirhinal cortical lesions on spatial reference memory in the rat

    Behav. Brain Res.

    (1994)
  • X.O Zhu et al.

    Effects of the novelty or familiarity of visual stimuli on the expression of the immediate early gene c-fos in rat brain

    Neuroscience

    (1995)
  • R.D Burwell et al.

    Perirhinal and postrhinal cortices of the rat: A review of the neuroanatomical literature and comparison with findings from the monkey brain

    Hippocampus

    (1995)
  • T.J Bussey et al.

    A novel automated touchscreen procedure for assessing learning in the rat using computer graphic stimuli

    Neurosci. Res. Commun.

    (1994)
  • T.W Deacon et al.

    Afferent connections of the perirhinal cortex in the rat

    J. Comp. Neurol.

    (1983)
  • H Eichenbaum et al.

    Two functional components of the hippocampal memory system

    Behav. Brain Sci.

    (1994)
  • A Ennaceur et al.

    Spontaneous recognition of object configurations in rats: Effects of fornix lesions

    Exp. Brain Res.

    (1994)
  • Cited by (153)

    • Effects of perirhinal cortex and hippocampal lesions on rats’ performance on two object-recognition tasks

      2020, Behavioural Brain Research
      Citation Excerpt :

      Nonetheless, upon closer inspection of the within-subjects results from several studies, there are discrepancies in terms of whether or not PRh lesions consistently abolish novel-object preferences. For example, some studies have shown that rats with PRh lesions, or combined postrhinal lesions, fail to exhibit statistically significant novelty preferences on the test [20,21,34–36]. Ennaceur and colleagues [20] found that rats with PRh lesions exhibited a statistically significant novelty preference following a 1-min delay but not a 15-min delay.

    View all citing articles on Scopus
    View full text