Research reportAbilities in tactile discrimination of textures in adult rats exposed to enriched or impoverished environments
Introduction
Many studies have attempted to describe various aspects of tactile discrimination behavior in rodents and to identify the cerebral areas involved in this behavior. Rodents explore their close environment using rhythmical movements of their facial whiskers, whose one-to-one representation in the barrel subfield cortex corresponds to about 20% of the SI area [101]. Rhythmical movements of the whiskers at frequencies ranging from 6 to 15 Hz allow rats to collect information on location, shape, size and texture of objects [13], [14], [52], [69], [81]. Guic-Roblès et al. were the first to clearly demonstrate the rat’s ability to discriminate between rough and smooth textures by whisker palpation, as well as the involvement of the barrel cortex in this discrimination task [47], [48]. While several studies have been conducted on capabilities of rats to discriminate different textures through the whisker-trigeminal system [13], [14], [15], [47], [48], [53], [74], the possible involvement of the paws in texture discrimination has been neglected in recent studies. In one of the early investigations on tactile discrimination of textures in rats, animals were trained to choose between two alleys with either rough or smooth textures in a Y-shaped apparatus [90]. In this study, Smith performed ablations in various locations of the neocortex, resulting in little or no impairment in this task, except for the lesion in the “somesthesic projection area”. However, the involvement of whiskers, hind and forepaws was not specified [90]. Zubek showed the involvement of the SI cortex in tactile discrimination, in particular the “arms area”, in a lesion paradigm study in which rats had to differentiate between two rotating cylinders covered with either a smooth surface or two grades of roughness, made of coarse or fine wire gauze [111]. Most of the studies were aimed at determining the location of somesthesic areas and their involvement in tactile perception using broadly defined lesions or ablations of large cortical/subcortical territories [30], [31], [33], [34], [90], [111], [112], [113]. In contrast, in another experiment, in which rats were trained to perform a roughness discrimination using the whiskers, the animals that underwent a SI barrel ablation reached the prelesion levels of performances when they were allowed to discriminate textures with the forepaws [48]. Such a circumscribed ablation showed undoubtedly for the first time the rat’s ability to perform a texture discrimination only using the forepaws. However, in this study whisker clipping, preserving the CNS integrity, could have been preferred to the SI barrel ablation.
In another line of study, many reports have shown a significant influence of housing conditions on cerebral neurochemistry and neuroanatomy, and cognitive capabilities in rats (see [50], [80], [97] for reviews). Enriched environment (EE) consists in rearing rats in large cages furnished with a regularly-renewed set of objects to promote both social contact and physical interactions with the objects. In contrast, in the impoverished environment (IE), rats are isolated in small cages without any object, so that they are deprived of social contact and have very limited environmental interactions. It is now well established that rats from EE have greater brain weight [3] and cortical thickness [6], [22], higher NGF concentrations [65], [66], [72] and enhanced levels of acetylcholinesterase activity [3], [80] in the neocortex than IE rats. Enrichment induces increases in dendritic branching, synapse counts and synaptic density (e.g. [12], [42], [44], [45], [46], [87], [88], [89], [94]) when compared to impoverishment. In addition, enrichment improves spatial learning and memory in a wide range of cognitive tasks, such as spatial orientation in the Morris water maze or problem-solving tasks in the Hebb–Williams tests (e.g. [4], [26], [37], [59], [64], [65], [77], [80], [82], [97]).
The first report devoted to experience-dependent capabilities in texture discrimination in rats was conducted by Finger and Fox in 1971 [32]. In this study carried out in enucleated rats, those reared in EE did not perform better than rats socially reared without objects, in a two-choice T-maze with floor arms covered with aluminum plates of different roughness. These authors pointed out the effects of practice in the task, and interindividual variations in arousal and motor activity within the two groups of rats to explain the absence of group-related differences in discrimination performances [32]. However, this lack of differences can be also attributed to the limited enrichment and the low difficulty of the task in this study. In another study, rats subjected to whisker trimming from birth were severely impaired in the discrimination of slight, but not great roughness contrasts in comparison with intact animals and rats with whiskers trimmed when adult [15]. These two reports raise the issue of how early sensory experience may alter tactile perception abilities in rodents. In previous studies, we found that the topographical organization of the SI forepaw maps was improved in young-adult rats reared in EE from weaning [16], whereas age-matched rats housed in IE exhibited maps with a disrupted topography [17]. Indeed, exploration and manipulation of the objects contained in the EE induced a specific expansion of the cortical zones serving the glabrous skin surfaces, as well as a reduction of the size of the corresponding glabrous RFs [16]. In contrast, the degradation of the SI forepaw maps of IE rats was characterized by a drastic enlargement of the glabrous forepaw RFs, a decrease in the area of the SI cutaneous forepaw maps and a breakdown of the topographic representation of contiguous cutaneous territories of the forepaw. This breakdown resulted from the emergence of non-cutaneous, presumably proprioceptive, input representations within the cutaneous map [17]. Therefore, our working hypothesis was that the experience-dependent changes in the forepaw representation promote better tactile discrimination abilities in EE rats than in IE rats. The main aim of the present study was to test this hypothesis by training rats to perform a texture discrimination with their paws during locomotion on floorboards of different roughness. Preliminary results were presented elsewhere [9].
Section snippets
Subjects
All experiments have been carried out in accordance with the UK Animals Act 1986 (Scientific Procedures) and the guidelines of the National Institute of Health Guide for the Care and Use of Laboratory animals (NIH Publication No. 86-23, revised 1985). After weaning (30 postnatal days), 20 female Long–Evans rats were reared for 2 months in two housing conditions: EE or IE. In EE, 10 rats lived together in a large cage (76 cm wide×76 cm deep×40 cm high) which contained numerous mobile and immobile
Pretraining
During pretraining sessions, rats had to learn basic associations of the task with no requirement of tactile detection. For instance, rats had to associate nose-pokes with reward while a single hole was opened in each session. Compared to IE rats (4.5±2.2 sessions) rats from EE (2.9±0.9 sessions) needed a smaller number of sessions to learn this association [F(1,18)=4.48; P<0.05]. Thus, EE rats learned the nose-pokes and reward association faster than IE rats.
Training in texture discrimination
During the training step, the
Discussion
The present study was devoted to evaluating the influence of sensory experience provided by differential housing conditions on rats’ tactile discrimination abilities. Rats had to differentiate homogeneous (low roughness) from heterogeneous (combination of different roughness) floorboards during their displacements in a Skinner box. To determine the maximum performance (Pmax) in texture discrimination, the roughness contrast of the heterogeneous floorboard was gradually decreased while the
Acknowledgements
This work was supported by CNRS and Université d’Aix-Marseille I. The authors are grateful to Drs. C. Baunez, F. Chaillan, M. Darnaudéry and R.N. Sachdev for helpful discussions and comments on the manuscript.
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