Plasticity during Early Brain Development Is Determined by Ontogenetic Potential

Abstract

Two competing hypotheses address neuroplasticity during early brain development: the "Kennard principle" describes the compensatory capacities of the immature developing CNS as superior to those of the adult brain, whereas the "Hebb principle" argues that the young brain is especially sensitive to insults. We provide evidence that these principles are not mutually exclusive. Following early brain lesions that are unilateral, the brain can refer to homotopic areas of the healthy hemisphere. This potential for reorganization is unique to the young brain but available only when, during ontogenesis of brain development, these areas have been used for the functions addressed. With respect to motor function, ipsilateral motor tracts can be recruited, which are only available during early brain development. Language can be reorganized to the right after early left hemispheric lesions, as the representation of the language network is initially bilateral. However, even in these situations, compensatory capacities of the developing brain are found to have limitations, probably defined by early determinants. Thus, plasticity and adaptivity are seen only within ontogenetic potential; that is, axonal or cortical structures cannot be recruited beyond early developmental possibilities. The young brain is probably more sensitive and vulnerable to lesions when these are bilateral. This is shown here for bilateral periventricular white matter lesions that clearly have an impact on cortical architecture and function, thus probably interfering with early network building.

Plasticity in One Hemisphere, Control From Two: Adaptation in Descending Motor Pathways After Unilateral Corticospinal Injury in Neonatal Rats

“…Injury to one hemisphere alters neuronal connections in both the injured and the uninjured hemispheres, especially if the injury occurs early in life. In the case of injury to the corticospinal tract (CST), the principal pathway for voluntary motor control (Porter and Lemon, 1995 ), descending motor pathways from both hemispheres have been demonstrated to adapt to injury in neonatal rats (Umeda and Funakoshi, 2014 ) and in humans (Krägeloh-Mann et al, 2017 ). However, it is not clear which neural circuits from the injured or the uninjured hemispheres are important to mediate motor skill recovery after early brain injury.…”

Transient callosal projections of L4 neurons are eliminated for the acquisition of local connectivity

“…In order to wire selectively and stereotypically during development, cortical neurons are thought to be intrinsically instructed with wiring rules that limit their connectivity 2 . However, cortical neurons also display remarkable plasticity that enables optimization of functional circuits and alternative wiring in non-canonical scenarios, such as in the case of loss of sensory inputs or brain insults in young brains 3–6 . This latter scenario requires considerable structural re-arrangement of axons.…”

Cerebellar lesions at a young age predict poorer long-term functional recovery

“…However, as first emphasized by Kennard herself ( Dennis, 2010 ), this view has limitations. Indeed, a large body of evidence now indicates that cerebral damages can actually be more harmful when inflicted at a young age, during critical periods of neural development ( Taylor and Alden, 1997 ; Forsyth, 2010 ; Anderson et al , 2011 ; Krageloh-Mann et al , 2017 ).…”

“…To date, the impact of age on functional recovery has been mainly investigated in the context of focal and diffuse cortical injuries ( Taylor and Alden, 1997 ; Forsyth, 2010 ; Anderson et al , 2011 ; Krageloh-Mann et al , 2017 ). Much less attention has been given to the issue whether the ‘Kennard principle’ holds for cerebellar lesions.…”