Review
Experience-dependent structural plasticity in the adult human brain

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Contrary to assumptions that changes in brain networks are possible only during crucial periods of development, research in the past decade has supported the idea of a permanently plastic brain. Novel experience, altered afferent input due to environmental changes and learning new skills are now recognized as modulators of brain function and underlying neuroanatomic circuitry. Given findings in experiments with animals and the recent discovery of increases in gray and white matter in the adult human brain as a result of learning, the old concept of cognitive reserve, that is the ability to reinforce brain volume in crucial areas and thus provide a greater threshold for age-dependent deficits, has been reinforced. The challenge we face is to unravel the exact nature of the dynamic structural alterations and, ultimately, to be able to use this knowledge for disease management. Understanding normative changes in brain structure that occur as a result of environmental changes and demands is pivotal to understanding the characteristic ability of the brain to adapt.

Section snippets

Structural and functional plasticity in the brain

An intrinsic property of the human central nervous system is the lifelong ability for structural and functional brain reorganization [1]. The term ‘plasticity’ refers to functional or structural changes (which may trigger each other) that occur in the adult brain to adjust to changes in the external environment or internal milieu 2, 3. The extent of plastic reorganization is conditional on the relevance of the alterations for the individual and can have either beneficial or maladaptive

The neuroanatomical basis of structural brain plasticity

During the past decade, a steadily growing number of studies in primate and nonprimate animals confirm the notion that experience, learning new skills but also damage of the nervous system, can cause functional and structural reorganization of the brain. At the functional level it has been convincingly demonstrated that even loss of sensory input due to peripheral nerve lesion can induce reorganization of cortical representation fields 17, 18, 19, 20. At the structural level, these studies

Cross-sectional differences: the hen or the egg?

A vast number of cross-sectional morphometric studies (Box 1) have demonstrated neuroanatomical correlates of learning and experience in different cognitive domains. For example, navigational experience has been reported to be correlated with posterior hippocampus size [14] and musical proficiency to be associated with volume enlargement of motor and auditory areas and their anatomical connections 10, 26, 46. More recent studies discussed morphological enlargement in the cerebellar vermian

Dynamic changes in human brain structure

Longitudinal studies in which imaging data are acquired at multiple time points during experimental intervention have the potential to unveil dynamic properties of learning-related plastic changes. The first longitudinal studies investigated a specific learning paradigm, namely 3-ball cascade juggling [7]. Juggling represents a complex visuomotor task, where perception and anticipation of moving targets determine the planning of subsequent motor action. Daily training for three months assured

Learning and experience shaping the brain

Several studies have built on and extended the findings in procedural learning 45, 58, 59, 60, 61 by studying longitudinally morphometric changes related to memory and learning. The first study of this type investigated a ‘real-life’ situation: the German basic medical exam, called ‘Physikum’ [8], which includes both oral and written tests in biology, chemistry, biochemistry, physics, social sciences, psychology, human anatomy and physiology demanding a high level of encoding, retrieval and

Physical exercise: shaping the brain or the mind or both?

Physical activity and an enriched environment have been shown to improve the rate of adult neurogenesis and maintenance of these new neurons 37, 66. A recent study demonstrating in vivo correlates of physical exercise-induced changes in the hippocampus confirms the theoretical possibility of angiogenesis/neurogenesis underlying plasticity processes [67]. Interestingly, these findings have been replicated in older and aged animals [68], suggesting that age is not per se a limiting factor for

Maladaptive plasticity: the flip side of the coin

Maladaptive plasticity can be defined as behavioral loss or even the development of disease symptoms resulting from plasticity changes in the adult human brain. Recent studies provide sufficient evidence that faulty practice or excessive demand could pose a risk of maladaptive plasticity depending on individual predisposition [73]. Animal models demonstrate that repetitive somatosensory stimulation of the fingers in primates results in abnormal hand postures similar to the clinical picture of

Cellular events underlying experience-dependent structural plasticity

The first study describing subtle anatomical changes using morphometry (in this case VBM) in patients was published in 1999 [84] and despite several hundred studies published since then, the nature of the underlying cellular events is still essentially unknown. In some respects, this situation resembles that in the functional MRI-field some years ago, when its use for our understanding of brain function was unquestioned, yet the long-supposed physiological correlate of the blood oxygen

Concluding remarks

Technical advances in live imaging studies and molecular approaches have contributed significantly to our current understanding of developmental plasticity and also focused our attention on plasticity exhibited by the mature brain. Neuroplasticity can be understood as the environmentally driven constant rearrangement of network homeostasis balancing the integration of neuronal activity, neurotransmitter release, neuronal (and perhaps glial) morphogenesis and changes in network formation

Acknowledgments

The author wishes to thank Gerd Kempermann, Christian Gaser and Bogdan Draganski for valuable discussion and input.

Glossary

Adult neurogenesis
a specific case of cell-based brain plasticity where new neurons (and not only neurites and synapses) are added to the brain network in an activity-dependent way. In humans, new neurons are generated throughout life in the hippocampal region, which is thought to provide the functional backbone for learning and memory. Recent animal and human studies have proposed the hippocampus and neurogenesis a prime target in a number of diseases, most notably dementias as well as major

References (97)

  • A.K. Wagner

    Intervention with environmental enrichment after experimental brain trauma enhances cognitive recovery in male but not female rats

    Neurosci. Lett.

    (2002)
  • S. Hihara

    Extension of corticocortical afferents into the anterior bank of the intraparietal sulcus by tool-use training in adult monkeys

    Neuropsychologia

    (2006)
  • B. Lee

    White matter neuroplastic changes in long-term trained players of the game of ‘Baduk’ (GO): a voxel-based diffusion-tensor imaging study

    Neuroimage

    (2010)
  • S. Begre

    Relation of white matter anisotropy to visual memory in 17 healthy subjects

    Brain Res.

    (2007)
  • O. Granert

    Manual activity shapes structure and function in contralateral human motor hand area

    Neuroimage

    (2011)
  • A. Engvig

    Effects of memory training on cortical thickness in the elderly

    Neuroimage

    (2010)
  • T. Schmidt-Wilcke

    Distinct patterns of functional and structural neuroplasticity associated with learning Morse code

    Neuroimage

    (2010)
  • N.N. Byl

    Effect of sensory discrimination training on structure and function in patients with focal hand dystonia: a case series

    Arch. Phys. Med. Rehabil.

    (2003)
  • A. May

    Chronic pain may change the structure of the brain

    Pain

    (2008)
  • D.B. Chklovskii

    Synaptic connectivity and neuronal morphology: two sides of the same coin

    Neuron

    (2004)
  • P.R. Huttenlocher

    Dendritic and synaptic pathology in mental retardation

    Pediatr. Neurol.

    (1991)
  • A.K. McAllister

    Neurotrophins regulate dendritic growth in developing visual cortex

    Neuron

    (1995)
  • A. Pascual-Leone

    The plastic human brain cortex

    Annu. Rev. Neurosci.

    (2005)
  • G. Kempermann

    Adult neurogenesis

  • R. Kanai et al.

    The structural basis of inter-individual differences in human behaviour and cognition

    Nat. Rev. Neurosci.

    (2011)
  • R. Kanai

    Distractibility in daily life is reflected in the structure and function of human parietal cortex

    J. Neurosci.

    (2011)
  • B. Draganski

    Neuroplasticity: changes in grey matter induced by training

    Nature

    (2004)
  • B. Draganski

    Temporal and spatial dynamics of brain structure changes during extensive learning

    J. Neurosci.

    (2006)
  • C. Gaser et al.

    Brain structures differ between musicians and non-musicians

    J. Neurosci.

    (2003)
  • L. Jancke

    The architecture of the golfer's brain

    PLoS ONE

    (2009)
  • J. Boyke

    Training-induced brain structure changes in the elderly

    J. Neurosci.

    (2008)
  • J. Driemeyer

    Changes in gray matter induced by learning–revisited

    PLoS ONE

    (2008)
  • E.A. Maguire

    Navigation-related structural change in the hippocampi of taxi drivers

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

    (2000)
  • E.A. Maguire

    Navigation expertise and the human hippocampus: a structural brain imaging analysis

    Hippocampus

    (2003)
  • P.M. Thompson

    Genetic influences on brain structure

    Nat. Neurosci.

    (2001)
  • T.P. Pons

    Massive cortical reorganization after sensory deafferentation in adult macaques

    Science

    (1991)
  • N. Jain

    Growth of new brainstem connections in adult monkeys with massive sensory loss

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

    (2000)
  • L.A. Henderson

    Functional reorganization of the brain in humans following spinal cord injury: evidence for underlying changes in cortical anatomy

    J. Neurosci.

    (2011)
  • A. Holtmaat

    Experience-dependent and cell-type-specific spine growth in the neocortex

    Nature

    (2006)
  • G.W. Knott

    Spine growth precedes synapse formation in the adult neocortex in vivo

    Nat. Neurosci.

    (2006)
  • J.T. Trachtenberg

    Long-term in vivo imaging of experience-dependent synaptic plasticity in adult cortex

    Nature

    (2002)
  • N. Dancause

    Extensive cortical rewiring after brain injury

    J. Neurosci.

    (2005)
  • L. Jancke

    The plastic human brain

    Restor. Neurol. Neurosci.

    (2009)
  • E. Bates

    Voxel-based lesion-symptom mapping

    Nat. Neurosci.

    (2003)
  • J.T. Crinion et al.

    Recovery and treatment of aphasia after stroke: functional imaging studies

    Curr. Opin. Neurol.

    (2007)
  • K. Reetz

    Structural findings in the basal ganglia in genetically determined and idiopathic Parkinson's disease

    Mov. Disord.

    (2009)
  • D. Hebb

    The effects of early experience on problem-solving at maturity

    Am. Psychol.

    (1947)
  • G. Kempermann

    Why and how physical activity promotes experience-induced brain plasticity

    Front. Neurosci.

    (2010)
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