ReviewAdult cortical plasticity following injury: Recapitulation of critical period mechanisms?
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
References (145)
- et al.
Optogenetic countering of glial acidosis suppresses glial glutamate release and ischemic brain damage
Neuron
(2014) - et al.
Growth-associated gene expression after stroke: evidence for a growth-promoting region in peri-infarct cortex
Exp Neurol
(2005) - et al.
Sensorimotor experience modulates age-dependent alterations of the forepaw representation in the primary somatosensory cortex
Neuroscience
(2001) - et al.
Regulation of class I MHC gene expression in the developing and mature CNS by neural activity
Neuron
(1998) - et al.
Shaping plasticity to enhance recovery after injury
Prog Brain Res
(2011) - et al.
Classical MHCI molecules regulate retinogeniculate refinement and limit ocular dominance plasticity
Neuron
(2009) Margaret Kennard (1899–1975): not a ‘principle’ of brain plasticity but a founding mother of developmental neuropsychology
Cortex
(2010)- et al.
Electrophysiological changes in the surrounding brain tissue of photochemically induced cortical infarcts in the rat
Neurosci Lett
(1993) - et al.
Mechanisms of ischemic brain damage
Neuropharmacology
(2008) - et al.
Development and plasticity of the primary visual cortex
Neuron
(2012)
How monocular deprivation shifts ocular dominance in visual cortex of young mice
Neuron
Development of auditory cortical synaptic receptive fields
Neurosci Biobehav Rev
Excitatory–inhibitory balance and critical period plasticity in developing visual cortex
Progress in Brain Research
Lifelong learning: ocular dominance plasticity in mouse visual cortex
Curr Opin Neurobiol
Transient and persistent dendritic spines in the neocortex in vivo
Neuron
BDNF regulates the maturation of inhibition and the critical period of plasticity in mouse visual cortex
Cell
Tumor necrosis factor-alpha mediates one component of competitive, experience-dependent plasticity in developing visual cortex
Neuron
Synaptic scaling and homeostatic plasticity in the mouse visual cortex in vivo
Neuron
Relative contribution of feedforward excitatory connections to expression of ocular dominance plasticity in layer 4 of visual cortex
Neuron
Auditory critical periods: a review from system’s perspective
Neuroscience
Developmental neuroplasticity after cochlear implantation
Trends Neurosci
Growth-associated gene and protein expression in the region of axonal sprouting in the aged brain after stroke
Neurobiol Dis
Experience-dependent pruning of dendritic spines in visual cortex by tissue plasminogen activator
Neuron
Lesion-induced transient suppression of inhibitory function in rat neocortex in vitro
Neuroscience
Long-term cellular dysfunction after focal cerebral ischemia: in vitro analyses
Neuroscience
Critical period revisited: impact on vision
Curr Opin Neurobiol
Homeostatic regulation of eye-specific responses in visual cortex during ocular dominance plasticity
Neuron
Strength through diversity
Neuron
Morphology of single geniculocortical afferents and functional recovery of the visual cortex after reverse monocular deprivation in the kitten
J Neurosci
Anatomical correlates of functional plasticity in mouse visual cortex
J Neurosci
Behavioral and neurophysiological effects of delayed training following a small ischemic infarct in primary motor cortex of squirrel monkeys
Exp Brain Res
Efficacy of rehabilitative experience declines with time after focal ischemic brain injury
J Neurosci
The physiological effects of monocular deprivation and their reversal in the monkey’s visual cortex
J Physiol
Faculté du langage articulé
Bull Soc Anthropol
Rapid morphologic plasticity of peri-infarct dendritic spines after focal ischemic stroke
Stroke
In vivo voltage-sensitive dye imaging in adult mice reveals that somatosensory maps lost to stroke are replaced over weeks by new structural and functional circuits with prolonged modes of activation within both the peri-infarct zone and distant sites
J Neurosci
Plasticity of cortical projections after stroke
The Neuroscientist
New patterns of intracortical projections after focal cortical stroke
Neurobiol Dis
Evolution of diaschisis in a focal stroke model
Stroke
Experience and activity-dependent maturation of perisomatic GABAergic innervation in primary visual cortex during a postnatal critical period
J Neurosci
Highly specific structural plasticity of inhibitory circuits in the adult neocortex
Neuroscientist
Structural basis for the role of inhibition in facilitating adult brain plasticity
Nat Neurosci
Rapid structural remodeling of thalamocortical synapses parallels experience-dependent functional plasticity in mouse primary visual cortex
J Neurosci
Repairing the human brain after stroke: I. Mechanisms of spontaneous recovery
Ann Neurol
Early development of ocular dominance columns
Science
Critical period for monocular deprivation in the cat visual cortex
J Neurophysiol
PirB regulates a structural substrate for cortical plasticity
Proc Natl Acad Sci U S A
Observations on monocular deprivation in mice
J Neurophysiol
On the similarities and differences of non-traumatic sound exposure during the critical period and in adulthood
Front Syst Neurosci
Increased receptive field size in the surround of chronic lesions in the adult cat visual cortex
Cereb Cortex
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