Elsevier

Neuroscience

Volume 283, 26 December 2014, Pages 4-16
Neuroscience

Review
Adult cortical plasticity following injury: Recapitulation of critical period mechanisms?

https://doi.org/10.1016/j.neuroscience.2014.04.029Get rights and content

Highlights

  • A significant measure of neuronal plasticity exists at every stage of the lifespan.

  • Adult deprivation-induced cortical plasticity displays ∼50% the magnitude of juvenile.

  • A biphasic response characterizes cortical plasticity after injury and deprivation.

Abstract

A primary goal of research on developmental critical periods (CPs) is the recapitulation of a juvenile-like state of malleability in the adult brain that might enable recovery from injury. These ambitions are often framed in terms of the simple reinstatement of enhanced plasticity in the growth-restricted milieu of an injured adult brain. Here, we provide an analysis of the similarities and differences between deprivation-induced and injury-induced cortical plasticity, to provide for a nuanced comparison of these remarkably similar processes. As a first step, we review the factors that drive ocular dominance plasticity in the primary visual cortex of the uninjured brain during the CP and in adults, to highlight processes that might confer adaptive advantage. In addition, we directly compare deprivation-induced cortical plasticity during the CP and plasticity following acute injury or ischemia in mature brain. We find that these two processes display a biphasic response profile following deprivation or injury: an initial decrease in GABAergic inhibition and synapse loss transitions into a period of neurite expansion and synaptic gain. This biphasic response profile emphasizes the transition from a period of cortical healing to one of reconnection and recovery of function. Yet while injury-induced plasticity in adult shares several salient characteristics with deprivation-induced plasticity during the CP, the degree to which the adult injured brain is able to functionally rewire, and the time required to do so, present major limitations for recovery. Attempts to recapitulate a measure of CP plasticity in an adult injury context will need to carefully dissect the circuit alterations and plasticity mechanisms involved while measuring functional behavioral output to assess their ultimate success.

Introduction

Critical periods (CPs) in mammalian cortical development comprise temporal windows when neuronal physiology and morphology are most sensitive to changes in afferent sensory input or experience (Lorenz, 1935, Hubel and Wiesel, 1963). A central goal of research on developmental CPs is the recapitulation of a juvenile-like state of malleability in the adult brain that might confer enhanced learning and/or recovery from injury. Considered within this framework, investigations into the underlying mechanisms for this robust period of early postnatal plasticity seek to uncover the key components that differentiate a relatively ‘plastic’ CP brain from a relatively ‘static’ mature brain. The hope is that these same plastic processes might be reinstated following adult cortical injury to allow better recovery, effectively replacing synaptic connections lost following brain damage with new functional connections.

Developing such interventions requires a thorough understanding of the differences between CP and adult cortical plasticity, as a first step in teasing out the key factors that drive or restrict plasticity in the uninjured brain. Cortical plasticity is sometimes framed as a privileged event, where a brain is either capable of altering its physiology and connectivity or is not, depending on the developmental state. We will argue that the cortex displays a significant measure of plasticity at every stage of an animal’s lifespan, and that the direction of change, as well as the mechanisms that underlie the induction/expression of a particular form of plasticity, are the appropriate metrics for understanding changes in cortical malleability across ages. This view of developmental plasticity emphasizes the role of overlapping plasticity mechanisms with a continuum of modes and strengths that shift as an animal matures.

Despite the existence of this continuum of plasticity mechanisms during development, ample evidence exists linking short temporal windows in early postnatal development with a greater magnitude of plasticity and more permanent alterations of both cortical anatomy and physiology than in the adult brain (Hubel and Wiesel, 1970, Shatz and Stryker, 1978, Antonini et al., 1999, Prusky and Douglas, 2003, Sawtell et al., 2003, Pham et al., 2004, Hofer et al., 2006, Heimel et al., 2007). Interestingly, after an acute injury or stroke in the adult brain, maximal neuronal plasticity and recovery occur during a sensitive period that follows the cortical insult (Nudo et al., 1996, Kolb et al., 2000, Villablanca and Hovda, 2000, Coq and Xerri, 2001, Biernaskie et al., 2004, Barbay et al., 2006, Salter et al., 2006, Rushmore et al., 2008, Nielsen et al., 2013), and as we will explore below, the cascade of events that reconfigure cortical circuitry following deprivation-induced plasticity and plasticity following cortical injury are strikingly similar (see these excellent reviews on plasticity following cortical injury/stroke (Wieloch and Nikolich, 2006, Cramer, 2008, Murphy and Corbett, 2009, Overman and Carmichael, 2014).

As both deprivation-induced plasticity and injury-induced plasticity show sensitive periods where changes are maximally expressed, and both processes have similar “trademark” effects on cortical circuits, comparisons between these two forms of plasticity seem to hold merit in the search for interventions that can reinstitute a measure of developmental plasticity in the mature injured brain. Here we aim to provide an analysis of the similarities and differences between deprivation-induced CP and injury-induced plasticity by reviewing the literature detailing specific assays for cortical plasticity in juvenile, adult and mature injured brain. We will highlight the major effects of these parallel processes on cortical circuitry, with an emphasis on the correlations between anatomical alterations, functional circuit output and the age/state of the primary visual cortex.

Section snippets

Ocular dominance plasticity (ODP) during the CP

Following the landmark studies by Hubel and Wiesel in kittens and adult cats that first delineated the notion of developmental CPs in the sensory cortex (Hubel and Wiesel, 1963, Hubel and Wiesel, 1970), the study of deprivation-induced plasticity is now mostly performed in rodents, in large part due to the powerful mechanistic questions that can be addressed through microcircuit analysis in these animals, as well as the use of transgenic mouse lines. In this review, we will primarily discuss

CP for injury-induced adult cortical plasticity

After a focal ischemic stroke or acute injury to the cortex, a CP for maximal recovery exists during which early intervention seems to have most beneficial effects in both rats and humans (Nudo et al., 1996, Coq and Xerri, 2001, Biernaskie et al., 2004, Lee et al., 2004, Barbay et al., 2006, Salter et al., 2006, Nielsen et al., 2013). The onset and closure of this optimal period for rehabilitation after injury are correlated with a sequence of molecular and anatomical changes that progress from

Recapitulation of developmental mechanisms?

A conspicuous pattern emerges from a comparison of deprivation-induced CP plasticity and plasticity following focal injury in adult. In both model paradigms an initial decrease in GABAergic inhibition and synapse loss transitions into a period of neurite expansion and synaptic gain. This biphasic response profile highlights how the cortex transitions from a period of protection and healing to one of reconnection and recovery of function. Intriguingly, this pattern of decreased activity and

Conclusions

Although not an absolute predictor of functional recovery (Kolb et al., 2000, Giza and Prins, 2006, Dennis, 2010), it has long been appreciated that juvenile brains are often more resilient to injury than mature brains (Broca, 1865, Kennard, 1936), however the underlying mechanisms for these profound differences in neuronal plasticity and functional recovery are just beginning to be understood.

Deprivation-induced plasticity during the CP and injury-induced plasticity in adults both appear to

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