Elsevier

Behavioural Brain Research

Volume 153, Issue 1, 12 August 2004, Pages 217-231
Behavioural Brain Research

Research report
Abilities in tactile discrimination of textures in adult rats exposed to enriched or impoverished environments

https://doi.org/10.1016/j.bbr.2003.12.002Get rights and content

Abstract

In previous studies, we have shown that housing in enriched environment for about 3 months after weaning improved the topographic organization and decreased the size of the receptive fields (RFs) located on the glabrous skin surfaces in the forepaw maps of the primary somatosensory cortex (SI) in rats [Exp. Brain Res. 121 (1998) 191]. In contrast, housing in impoverished environment induced a degradation of the SI forepaw representation, characterized by topographic disruptions, a reduction of the cutaneous forepaw area and an enlargement of the glabrous RFs [Exp. Brain Res. 129 (1999) 518]. Based on these two studies, we postulated that these representational alterations could underlie changes in haptic perception. Therefore, the present study was aimed at determining the influence of housing conditions on the rat’s abilities in tactile texture discrimination. After a 2-month exposure to enriched or impoverished environments, rats were trained to perform a discrimination task during locomotion on floorboards of different roughness. At the end of every daily behavioral session, rats were replaced in their respective housing environment. Rats had to discriminate homogeneous (low roughness) from heterogeneous floorboards (combination of two different roughness levels). To determine the maximum performance in texture discrimination, the roughness contrast of the heterogeneous texture was gradually reduced, so that homogeneous and heterogeneous floorboards became harder to differentiate. We found that the enriched rats learned the first steps of the behavioral task faster than the impoverished rats, whereas both groups exhibited similar performances in texture discrimination. An individual “predilection” for either homogeneous or heterogeneous floorboards, presumably reflecting a behavioral strategy, seemed to account for the absence of differences in haptic discrimination between groups. The sensory experience depending on the rewarded texture discrimination task seems to have a greater influence on individual texture discrimination abilities than the sensorimotor experience related to housing conditions.

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.

References (113)

  • C.A. Frye

    Estrus-associated decrements in a water maze task are limited to acquisition

    Physiol. Behav.

    (1995)
  • L.A. Galea et al.

    High levels of estradiol disrupt conditioned place preference learning, stimulus response learning and reference memory but have limited effects on working memory

    Behav. Brain Res.

    (2001)
  • E.B. Gardner et al.

    Environmental enrichment and deprivation: effects on learning memory and exploration

    Physiol. Behav.

    (1975)
  • R.B. Gibbs et al.

    Effects of estrogen and fimbria/fornix transection on p75NGFR and ChAT expression in the medial septum and diagonal band of Broca

    Exp. Neurol.

    (1992)
  • W.T. Greenough et al.

    Pattern of dendritic branching in occipital cortex of rats reared in complex environments

    Exp. Neurol.

    (1973)
  • W.T. Greenough et al.

    Effects of rearing complexity on dendritic branching in frontolateral and temporal cortex of the rat

    Exp. Neurol.

    (1973)
  • E. Guic-Roblès et al.

    Rats can learn a roughness discrimination using only their vibrissal system

    Behav. Brain Res.

    (1989)
  • E. Guic-Roblès et al.

    Vibrissal roughness discrimination is barrel cortex-dependent

    Behav. Brain Res.

    (1992)
  • R.R. Gupta et al.

    Estrogen modulates sexually dimorphic contextual fear conditioning and hippocampal long-term potentiation (LTP) in rats

    Brain Res.

    (2001)
  • J.R. Hoffman et al.

    Rats recovering from unilateral barrel-cortex ischemia are capable of completing a whisker-dependent task using only their affected whiskers

    Brain Res.

    (2003)
  • M. Hollins et al.

    Vibrotaction and texture perception

    Behav. Brain Res.

    (2002)
  • C.R. Kelche et al.

    Effets de l’environnement sur la restauration fonctionnelle après lésions hippocampiques chez des rats adultes

    Physiol. Behav.

    (1978)
  • F. Larsson et al.

    Psychological stress and environmental adaptation in enriched vs. impoverished housed rats

    Pharmacol. Biochem. Behav.

    (2002)
  • R. Loy et al.

    Autoradiographic localization of estradiol-binding neurons in the rat hippocampal formation and entorhinal cortex

    Brain Res.

    (1988)
  • V.N. Luine

    Estradiol increases choline acetyltransferase activity in specific basal forebrain nuclei and projection areas of female rats

    Exp. Neurol.

    (1985)
  • A.K. Mohammed et al.

    Selective lesioning of forebrain noradrenaline neurons at birth abolishes the improved maze learning performance induced by rearing in complex environment

    Brain Res.

    (1986)
  • A.K. Mohammed et al.

    Environmental influence on behaviour and nerve growth factor in the brain

    Brain Res.

    (1990)
  • A.H. Mohammed et al.

    Environmental influences on the central nervous system and their implications for the aging rat

    Behav. Brain Res.

    (1993)
  • M.J. Morgan

    Effects of post-weaning environment on learning in the rat

    Anim. Behav.

    (1973)
  • M.J. Morgan et al.

    Incentive motivation and behavioural inhibition in socially isolated rats

    Physiol. Behav.

    (1975)
  • T.M. Pham et al.

    Effects of environmental enrichment on cognitive function and hippocampal NGF in the non-handled rats

    Behav. Brain Res.

    (1999)
  • T. Prigg et al.

    Texture discrimination and unit recordings in the rat whisker/barrel system

    Physiol. Behav.

    (2002)
  • T.W. Robbins et al.

    Neurobehavioural mechanisms of reward and motivation

    Curr. Opin. Neurobiol.

    (1996)
  • F.D. Rose et al.

    Differential reinforcement effects in rats reared in enriched and impoverished environments

    Physiol. Behav.

    (1986)
  • M.R. Rosenzweig et al.

    Psychobiology of plasticity: effects of training and experience on brain and behavior

    Behav. Brain Res.

    (1996)
  • N.C. Schrijver et al.

    Dissociable effects of isolation rearing and environmental enrichment on exploration, spatial learning and HPA activity in adult rats

    Pharmacol. Biochem. Behav.

    (2002)
  • M. Singh et al.

    Ovarian steroid deprivation results in a reversible learning impairment and compromised cholinergic function in female Sprague–Dawley rats

    Brain Res.

    (1994)
  • A.M. Sirevaag et al.

    Differential rearing effects on rat visual cortex synapses. III. Neuronal and glial nuclei, boutons, dendrites, and capillaries

    Brain Res.

    (1987)
  • A.M. Sirevaag et al.

    A multivariate statistical summary of synaptic plasticity measures in rats exposed to complex, social and individual environments

    Brain Res.

    (1988)
  • R.W. Stackman et al.

    Stability of spatial working memory across the estrous cycle of Long–Evans rats

    Neurobiol. Learn. Mem.

    (1997)
  • M. Torasdotter et al.

    Expression of neurotrophin-3 mRNA in the rat visual cortex and hippocampus is influenced by environmental conditions

    Neurosci. Lett.

    (1996)
  • A.M. Turner et al.

    Differential rearing effects on rat visual cortex synapses. I. Synaptic and neuronal density and synapses per neuron

    Brain Res.

    (1985)
  • G.B. Varty et al.

    Environmental enrichment and isolation rearing in the rat: effects on locomotor behavior and startle response plasticity

    Biol. Psychiatry

    (2000)
  • S.G. Warren et al.

    LTP varies across the estrous cycle: enhanced synaptic plasticity in proestrus rats

    Brain Res.

    (1995)
  • S. Bao et al.

    Cortical remodelling induced by activity of ventral tegmental dopamine neurons

    Nature

    (2001)
  • S. Bao et al.

    Suppression of cortical representation through backward conditioning

    Proc. Natl. Acad. Sci. U.S.A.

    (2003)
  • E.L. Bennett et al.

    Chemical and anatomical plasticity of brain

    Science

    (1964)
  • Bennett EL, Rosenzweig MR, Diamond MC. Time courses of effects of differential experience on brain measures and...
  • B. Berry et al.

    Spatial learning and memory at defined points of the estrous cycle: effects on performance of a hippocampal-dependent task

    Behav. Neurosci.

    (1997)
  • D.T. Blake et al.

    Neural correlates of instrumental learning in primary auditory cortex

    Proc. Natl. Acad. Sci. U.S.A.

    (2002)
  • Cited by (21)

    • Tactile learning in rodents: Neurobiology and neuropharmacology

      2016, Life Sciences
      Citation Excerpt :

      Previous studies have investigated the role of the environment in tactile learning, although with some conflicting results. Bourgeon et al., evaluated the influence of housing conditions on the ability of rats to perform tactile discriminations using their paws [17]. Their study showed that rats which were exposed to an enriched environment learned faster than those which were exposed to an impoverished environment, and performed better at the beginning of the experiment.

    • Have studies of the developmental regulation of behavioral phenotypes revealed the mechanisms of gene-environment interactions?

      2012, Physiology and Behavior
      Citation Excerpt :

      Persistence of the effects of enrichment is observed for behavioral consequences as well [38]. These changes in cortical structure and chemistry are associated with improved learning in a variety of tasks [30,39–43]. However, many of these comparisons have been between EC and IC rats, so at least some of these differences may be attributed to isolation-induced differences, discussed in more detail in a later section.

    View all citing articles on Scopus
    View full text