Lifelong learning: ocular dominance plasticity in mouse visual cortex
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.
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2021, Progress in Brain ResearchCitation Excerpt :In rodents, this percentage is around 90–95%. Thus, for each eye, axonal fibers running ipsilaterally and axonal fibers running contralaterally meet at the optic chiasm and project as an optic tract to the subcortical visual stations at a mesencephalic level (in the dorsal lateral geniculate nucleus dLGN) and diencephalic levels (in the superior colliculus) (Hofer et al., 2006). About 90% of the retinal axons project to the dLGN in the thalamus where they make synapses with neurons that in turn project to the first cortical station: the primary visual cortex (V1).