Age, Experience and the Changing Brain

https://doi.org/10.1016/S0149-7634(97)00008-0Get rights and content

Abstract

KOLB, B., M. FORGIE, R. GIBB, G. GORNY, S. ROWNTREE. Age, experience and the changing brain. NEUROSCI BIOBEHAV REV 22(2), 143-159, 1998.—In this review, various aspects of how environmental experience affects the structure of the cortex at different times in the age of the animal are summarized. The interactions of brain injury and sex on the age-dependent plastic changes in the cortex are also considered. Finally, we have attempted to reach some general conclusions that describe the effects of age, experience, sex, and injury on the cortex.

Introduction

In principle, there are two ways that experience could alter the brain: either by modifying existing circuitry or by creating novel circuitry [63]. It is reasonable to suppose that the brain makes use of both strategies, although the details of the particular strategy will likely vary with the age of the animal. Indeed, during development of the brain all circuitry is, by definition, novel. One way to examine the experience-dependent changes in the brain is to look at the effects of different experiences on neuronal structure and function. For psychologists, this rationale usually means adopting one of two approaches: either animals are placed in differential environments such as so-called “enriched environments” versus “impoverished environments”; or animals are trained in specific types of tasks, such as mazes. In either paradigm, the experience is correlated with some measure of structure such as brain weight or dendritic extent (e.g. [17]). These experiments generally show that particular experiences embellish circuitry relative to the absence of experience, which fails to do so. Although this type of experimental psychological approach would appear to have considerable appeal in understanding experience-dependent changes in the brain, the impact of this type of research has been surprisingly limited. Indeed, Purves [63]noted that for reasons that are as much sociological as scientific, the experimental neuropsychological perspective has not been embraced generally by most neurobiologists and that these psychological experiments are rarely referred to in the mainstream literature. Oddly, again for reasons that are both sociological as much as scientific, the importance of studies of enriched experience also have had limited impact in mainstream psychology where there has been a long-standing bias against structural interpretations of psychological phenomena. Nevertheless, the study of experience-dependent changes in experiments that manipulate external experiences has provided a rich broth of information that is relevant both to basic neurobiological theories of brain function as well as to general theories of behavioral organization. The goal of the current review is to illustrate some of principles that have emerged. The review will begin with a summary of some of experience-dependent changes in the intact brain followed by a consideration of the effects of manipulating factors such as gonadal hormones or neurotrophins and the effects of cortical injury.

Section snippets

Assumptions

As we begin, we must first admit to several biases. Firstly, we assume that the structural properties of the brain are important in understanding its function. Although such an assumption is self-evident to most neuroscientists, it is not as ubiquitously assumed by psychologists who do not study the brain (e.g. 69, 83). An important corollary of this assumption is that changes in the structural properties of the brain reflect changes in the function of neural circuits.

Secondly, we assume both

Historical context

Although the idea that experience can modify brain structure can probably be traced back at least to Ramon y Cajal [70], it was Hebb who made this a central feature of his neuropsychological theory [25]. Hebb did the first experiments on the consequences of enriched rearing on the behavior of the rat [24], but it was not until the group at Berkeley began to demonstrate changes in brain weight, cortical thickness, acetylcholine levels, and dendritic structure that there was any structural

Analysis of dendritic material

We indicated earlier that there is a high correlation between the extent of dendritic arborization and the number of synapses. Although synapses can only be studied (and counted) directly with EM procedures, an estimate of synapse number can be made by calculating the total dendritic length. Cells can be stained using one of two different procedures. The oldest procedure was devised by Golgi in the late 19th century and it involves depositing a heavy metal, such as gold or silver, on cell

Analysis of glia

There are three main types of glia in the cortex: astrocytes, microglia, and oligodendroctyes. The oligodendroctyes form the myelin and have not been studied with respect to experience. The astrocytes are large glia that are found both in the white matter as well as the grey matter of the cortex. Many astrocytes have processes that resemble dendrites and these processes expand in response to various events, including experience. Microglia are normally visible only when the brain is injured and

Experience-dependent change in the intact brain

As we began our studies of experience-dependent changes in the brain, we used the logic of those before us who had compared animals in laboratory cages to others in “enriched environments” (e.g. 25, 18, 74). Thus, we placed animals in same-sex groups of 4–6 in rat condominiums, which are 1 m×0.6 m×1.8 m high enclosures (Fig. 2). The condominiums feature sawdust floors to allow digging and three hardware cloth walls to allow climbing. The enclosures contain numerous objects, tree branches, and

Plasticity in the injured adult brain

When the cortex is damaged there are changes in the remaining cortex that are correlated with functional outcome. For example, when we removed the frontal cortex in adult rats, we found an initial drop in dendritic arborization in proximal cortical regions such as parietal cortex. This atrophy slowly resolved and 4 months later there was a significant increase in dendritic morphology, which was correlated with partial restitution of function (e.g. 39, 40, 77). This morphological plasticity may

Plasticity in injured developing brain

One of our consistent findings over the past decade has been that the anatomical sequelae of cortical injury vary with precise developmental stage. In brief, when the brain of rats is damaged in the first few days of life, which corresponds to a time just after neural proliferation is complete but neural migration and differentiation are still ongoing, there is a marked generalized atrophy of dendritic arborization and a decrease in spine density in neurons throughout the cortical mantle 43, 49

Sex and experience-dependent changes in the brain

There is accumulating evidence that the male and female brain differ in their structure, respond differently to environmental events, and respond differently to injury. We consider each aspect in turn.

Conclusions

One of the most intriguing questions in behavioral neuroscience concerns the manner in which the brain, and especially the neocortex, can modify its structure and ultimately its function throughout one's lifetime. As the review has suggested, the cortex can be changed dramatically by experience and this change is modulated by various factors. Several basic conclusions can be extracted regarding the nature of the relationship between experience, brain plasticity, and behavior.

1. Experience

Acknowledgements

This research was supported by an NSERC of Canada grant to Bryan Kolb.

References (98)

  • J.M. Juraska et al.

    Sex differences in the dendritic branching of dentate granule cells following differential experience

    Brain Res.

    (1985)
  • J.M. Juraska et al.

    Sex and environmental influences on the size and ultrastructure of the rat corpus callosum

    Brain Res.

    (1988)
  • B. Kolb

    Functions of the frontal cortex of the rat: a comparative review

    Brain Res. Rev.

    (1984)
  • B. Kolb et al.

    Recovery from early cortical damage in rats. II. Effects of experience on anatomy and behavior following frontal lesions at 1 or 5 days of age

    Behav. Brain Res.

    (1987)
  • B. Kolb et al.

    Sparing of function after neonatal frontal lesions correlates with increased cortical dendritic branching: a possible mechanism for the Kennard effect

    Behav. Brain Res.

    (1991)
  • B. Kolb et al.

    Neonatal frontal cortical lesions in rats alter cortical structure and connectivity

    Brain Res.

    (1994)
  • G. Prusky et al.

    Morphology of identified corticospinal cells in the rat following motor cortex injury: absence of use-dependent change

    Brain Res.

    (1996)
  • D. Purves et al.

    Imaging mammalian nerve cells and their connections over time in living animals

    Trends Neurosci.

    (1987)
  • 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.

    Plasticity of GFAP-immunoreactive astrocyte size and number in visual cortex of rats reared in complex environments

    Brain Res.

    (1991)
  • J. Stewart et al.

    The effects of neonatal gonadectomy and prenatal stress on cortical thickness and asymmetry in rats

    Behav. Neural Biol.

    (1988)
  • J. Stewart et al.

    Dendritic branching in cortical pyramidal cells in response to ovariectomy in adult female rats: suppression by neonatal exposure to testosterone

    Brain Res.

    (1994)
  • R.M. Sullivan et al.

    Early olfactory learning induces an enhanced olfactory bulb response in rats

    Dev. Brain Res.

    (1986)
  • 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)
  • R.W. West et al.

    Effect of environmental complexity on cortical synapses of rats

    Behav. Biol.

    (1972)
  • I.Q. Whishaw et al.

    The impairments in reaching and the movements of compensation in rats with motor cortex lesions: an endpoint, videorecording, and movement notation analysis

    Behav. Brain Res.

    (1991)
  • C.C. Woo et al.

    Sensitive period for neural and behavioral response development to learned odors

    Dev. Brain Res.

    (1987)
  • J.E. Black et al.

    Learning causes synaptogenesis, whereas motor activity causes angiogenesis, in cerebellar cortex of adult rats

    Proc. Natl. Acad. Sci. USA

    (1990)
  • Breedlove, S.M. Sexual differentiation of the brain and behavior. In: Becker, J.B.; Breedlove, S.M.; Crews, D., eds....
  • Capowski, J. Computer techniques in neuroanatomy. New York: Plenum Press;...
  • R. Coopersmith et al.

    Enhanced neural response to familiar olfactory cues

    Science

    (1984)
  • Diamond, J. Nerve growth factor and the reinnervation of skin after peripheral nerve lesions. In: Flohr, H., ed....
  • M.C. Diamond et al.

    Extensive cortical depth measurements and neuron size increases in the cortex of environmentally enriched rats

    J. Comp. Neurol.

    (1967)
  • T. Field et al.

    Tactile/kinesthetic stimulation effects on preterm neonates

    Pediatrics

    (1986)
  • Flohr, H. (ed.). Post-lesion neural plasticity. Berlin: Springer-Verlag,...
  • Gibb, R., Kolb, B. A method for Vibratome sectioning of Golgi-Cox stained whole brain. J. Neurosci. Methods, 1997,...
  • A. Globus et al.

    Effects of differential experience on dendritic spine counts in rat cerebral cortex

    J. Comp. Physiol. Psychol.

    (1973)
  • Gorski, R.A. Sexual differentiation of the endocrine brain and its control. In: Motta, M., ed. Brain endocrinology, 2nd...
  • W.T. Greenough et al.

    Experience and brain development

    Child Dev.

    (1987)
  • Greenough, W.T.; Chang, F.F. Plasticity of synapse structure and pattern in the cerebral cortex. In: Peters, A.; Jones,...
  • W.T. Greenough et al.

    Sub-synaptic plate perforations: changes with age and experience in the rat

    Science

    (1978)
  • K.M. Harris et al.

    Dendritic spines: cellular specializations imparting both stability and flexibility to synaptic function

    Annu. Rev. Psychol.

    (1994)
  • D.O. Hebb

    The effects of early experience on problem solving at maturity

    Am. Psychol.

    (1947)
  • Hebb, D.O. The organization of behavior. New York: Wiley;...
  • B. Jacobs et al.

    A quantitative dendritic analysis of Wernicke's area. I. Lifespan changes

    J. Comp. Neurol.

    (1993)
  • B. Jacobs et al.

    A quantitative dendritic analysis of Wernicke's area. II. Gender hemispheric, and environmental factors

    J. Comp. Neurol.

    (1993)
  • T.A. Jones et al.

    Use-dependent growth of pyramidal neurons after neocortical damage

    J. Neurosci.

    (1994)
  • Juraska, J.M. Sex differences in developmental plasticity of behavior and the brain. In: Greenough, W.T.; Juraska,...
  • Juraska, J.M. The structure of the cerebral cortex: effects of gender and the environment. In: Kolb, B.; Tees, R., eds....
  • Cited by (267)

    View all citing articles on Scopus
    View full text