Lifelong learning: ocular dominance plasticity in mouse visual cortex

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Ocular dominance plasticity has long served as a successful model for examining how cortical circuits are shaped by experience. In this paradigm, altered retinal activity caused by unilateral eye-lid closure leads to dramatic shifts in the binocular response properties of neurons in the visual cortex. Much of the recent progress in identifying the cellular and molecular mechanisms underlying ocular dominance plasticity has been achieved by using the mouse as a model system. In this species, monocular deprivation initiated in adulthood also causes robust ocular dominance shifts. Research on ocular dominance plasticity in the mouse is starting to provide insight into which factors mediate and influence cortical plasticity in juvenile and adult animals.

Introduction

Since the 1960s, when Wiesel and Hubel [1] discovered that the binocular representation in primary visual cortex is particularly susceptible to changes in visual experience, ocular dominance (OD) has served as an important model system for exploring the cellular and molecular mechanisms underlying the plasticity of cortical circuits. Their groundbreaking studies in kittens demonstrated fast and strong adaptive changes of neuronal circuits in response to the imbalanced binocular input caused by transient lid closure of one eye (referred to as monocular deprivation, MD), leading to a shift in the preference of cortical neurons for the eye that remained open [1]. This shift in OD is associated with degraded vision through the deprived eye after reopening [2].

Although the phenomenology of OD shifts has been described in detail in several species [3, 4, 5], the underlying cellular and molecular mechanisms are still largely unresolved and merit further study. In this context, the mouse, which shows OD shifts that are comparable to those of higher mammals [4, 6], has emerged as a valuable experimental model because of its amenability to genetic manipulation. In this review we summarise the relevant, and at times contradictory, findings on OD plasticity from the past few years, focusing on the underlying mechanisms and the recent discovery of plasticity in the visual cortex of adult mice.

Section snippets

Ocular dominance plasticity in juvenile animals

In cats, ferrets and primates, thalamic afferents from eye-specific layers in the lateral geniculate nucleus (LGN) segregate in the visual cortex during early development, giving rise to OD columns of neurons that are driven more strongly by the left or the right eye [7, 8]. In rodents, the binocular region of the primary visual cortex lacks clear OD columns but contains mostly binocular cells that on average have a preference for the contralateral eye (Figure 1) [6, 9, 10]. In higher mammals,

Mechanisms of ocular dominance plasticity

Whereas a mature inhibitory network is important for enabling OD plasticity, most studies addressing the mechanisms of OD plasticity have concentrated on changes at excitatory synapses. Early, long-favoured theories postulated that inputs from the eyes concurrently compete for postsynaptic space on, and resources from, target neurons, such as neurotrophic factors [18, 19]. However, as yet no evidence has been provided for such direct competition in the binocular cortex. In fact, in rodents,

Ocular dominance plasticity in adult visual cortex

In contrast to the classic notion of a critical period for experience-dependent plasticity [11], several studies have recently reported that OD shifts in mice can also be induced in adulthood [37••, 56, 57, 58•]. Strong OD plasticity was demonstrated after MD in adult mice with several methods, including extracellular microelectrode recordings [37••], intrinsic signal imaging [37••] and visually evoked potentials (VEPs) [56] under different anaesthetic regimes and importantly also in awake

Promoting adult plasticity

The potential for large-scale plasticity in adult primary visual cortex is restricted in most mammals and even in the mouse it does not match the extent of plasticity found in juvenile animals. Rearing animals in the dark enables strong plasticity in the visual cortex of older animals by retarding the maturation of cortical circuits [66]. Recently, it has also been demonstrated that complete visual deprivation in adult rats re-established a more immature cortical state, leading to enhanced OD

Recovery from monocular deprivation

Another way of exploring visual cortex plasticity is to study the effect of re-establishing binocular vision after MD. In models of OD plasticity based solely on competition, recovery from MD is not expected to occur when the deprived eye is simply re-opened. But, in fact, full recovery of binocular responses after a period of binocular vision has been shown in different species [37••, 71, 72, 73, 74]. One might assume that the recovery from MD is simply a reversal of the initial MD effect, but

Conclusions

Ocular dominance plasticity in visual cortex has long served as a useful model for examining how cortical circuits are shaped by experience. Altered activity at deprived eye synapses initiates a sequence of cellular and molecular events such that the cortex becomes more responsive to the eye that remained open. Although progress has been made in identifying some of the underlying physiological and biochemical processes, a coherent synthesis of how experience alters cortical circuitry is, as of

Update

Two recent studies explored how different manipulations of visual environment differentially regulate the expression of genes in mouse visual cortex [78, 79]. They exposed a cohort of novel candidate molecules and molecular signalling pathways involved in the adaptive changes of cortical neurons in response to modification of visual experience, including those specifically associated with monocular deprivation.

References and recommended reading

Papers of particular interest, published within the annual period of review, have been highlighted as:

  • • of special interest

  • •• of outstanding interest

Acknowledgements

We thank F Sengpiel for helpful comments on the manuscript.

References (79)

  • N. Mataga et al.

    Permissive proteolytic activity for visual cortical plasticity

    Proc Natl Acad Sci USA

    (2002)
  • A.D. Huberman et al.

    Neurotrophins and visual cortical plasticity

    Prog Brain Res

    (2002)
  • G.G. Turrigiano et al.

    Homeostatic plasticity in the developing nervous system

    Nat Rev Neurosci

    (2004)
  • E.L. Bienenstock et al.

    Theory for the development of neuron selectivity: orientation specificity and binocular interaction in visual cortex

    J Neurosci

    (1982)
  • M.F. Bear

    Mechanism for a sliding synaptic modification threshold

    Neuron

    (1995)
  • C.D. Rittenhouse et al.

    Monocular deprivation induces homosynaptic long-term depression in visual cortex

    Nature

    (1999)
  • H. Markram et al.

    Regulation of synaptic efficacy by coincidence of postsynaptic APs and EPSPs

    Science

    (1997)
  • C.D. Meliza et al.

    Receptive-field modification in rat visual cortex induced by paired visual stimulation and single-cell spiking

    Neuron

    (2006)
  • M.E. Lickey et al.

    Swept contrast visual evoked potentials and their plasticity following monocular deprivation in mice

    Vision Res

    (2004)
  • Y. Tagawa et al.

    Multiple periods of functional ocular dominance plasticity in mouse visual cortex

    Nat Neurosci

    (2005)
  • A.J. Holtmaat et al.

    Transient and persistent dendritic spines in the neocortex in vivo

    Neuron

    (2005)
  • J.T. Trachtenberg et al.

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

    Nature

    (2002)
  • J. Grutzendler et al.

    Long-term dendritic spine stability in the adult cortex

    Nature

    (2002)
  • A.W. McGee et al.

    Experience-driven plasticity of visual cortex limited by myelin and Nogo receptor

    Science

    (2005)
  • T.N. Wiesel et al.

    Single cell responses in striate cortex of kittens deprived of vision in one eye

    J Neurophysiol

    (1963)
  • D.W. Muir et al.

    Visual resolution and experience: acuity deficits in cats following early selective visual deprivation

    Science

    (1973)
  • T.N. Wiesel et al.

    Comparison of the effects of unilateral and bilateral eye closure on cortical unit responses in kittens

    J Neurophysiol

    (1965)
  • U.C. Dräger

    Observations on monocular deprivation in mice

    J Neurophysiol

    (1978)
  • D.H. Hubel et al.

    Plasticity of ocular dominance columns in monkey striate cortex

    Philos Trans R Soc Lond B Biol Sci

    (1977)
  • J.A. Gordon et al.

    Experience-dependent plasticity of binocular responses in the primary visual cortex of the mouse

    J Neurosci

    (1996)
  • D.H. Hubel et al.

    Functional architecture of macaque monkey visual cortex (ferrier lecture)

    Proc R Soc Lond B Biol Sci

    (1977)
  • S. LeVay et al.

    Ocular dominance columns and their development in layer IV of the cat's visual cortex: a quantitative study

    J Comp Neurol

    (1978)
  • U.C. Dräger

    Receptive fields of single cells and topography in mouse visual cortex

    J Comp Neurol

    (1975)
  • A. Antonini et al.

    Anatomical correlates of functional plasticity in mouse visual cortex

    J Neurosci

    (1999)
  • D.H. Hubel et al.

    The period of susceptibility to the physiological effects of unilateral eye closure in kittens

    J Physiol

    (1970)
  • T.K. Hensch et al.

    Local GABA circuit control of experience-dependent plasticity in developing visual cortex

    Science

    (1998)
  • M. Fagiolini et al.

    Inhibitory threshold for critical-period activation in primary visual cortex

    Nature

    (2000)
  • M. Fagiolini et al.

    Specific GABAA circuits for visual cortical plasticity

    Science

    (2004)
  • R.W. Guillery

    Binocular competition in the control of geniculate cell growth

    J Comp Neurol

    (1972)
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