Continuity and change in neural plasticity through embryonic morphogenesis, fetal activity‐dependent synaptogenesis, and infant memory consolidation

Abstract

There is an apparent continuity in human neural development that can be traced to venerable themes of vertebrate morphogenesis that have shaped the evolution of the reptilian telencephalon (including both primitive three‐layered cortex and basal ganglia) and then the subsequent evolution of the mammalian six‐layered neocortex. In this theoretical analysis, we propose that an evolutionary–developmental analysis of these general morphogenetic themes can help to explain the embryonic development of the dual divisions of the limbic system that control the dorsal and ventral networks of the human neocortex. These include the archicortical (dorsal limbic) Papez circuits regulated by the hippocampus that organize spatial, contextual memory, as well as the paleocortical (ventral limbic) circuits that organize object memory. We review evidence that these dorsal and ventral limbic divisions are controlled by the differential actions of brainstem lemnothalamic and midbrain collothalamic arousal control systems, respectively, thereby traversing the vertebrate subcortical neuraxis. These dual control systems are first seen shaping the phyletic morphogenesis of the archicortical and paleocortical foundations of the forebrain in embryogenesis. They then provide dual modes of activity‐dependent synaptic organization in the active (lemnothalamic) and quiet (collothalamic) stages of fetal sleep. Finally, these regulatory systems mature to form the major systems of memory consolidation of postnatal development, including the rapid eye movement (lemnothalamic) consolidation of implicit memory and social attachment in the first year, and then—in a subsequent stage—the non‐REM (collothalamic) consolidation of explicit memory that is integral to the autonomy and individuation of the second year of life.

Markov Blankets and Mirror Symmetries. Free Energy Minimization and Mesocortical Anatomy

“…These aspects have been given brief attention in regard to the growth model [63]. Integration with the details of the structural model of cerebral embryogenesis and its functional ramifications (5,6) may be possible. As the cortex emerges by differentiation from cells of limbic origin, during its growth it would be brought, by the same process of predictive error minimization, into harmony with the developing limbic and subcortical systems, while concurrently more direct exchanges of neocortex and environment via major sensory and motor pathways develop.…”

Markov Blankets and Mirror Symmetries—Free Energy Minimization and Mesocortical Anatomy

“…A further question is whether the development of mirror symmetric synaptic systems with intervening Markov blankets may be applicable more widely, to neurogenesis in general-and more particularly might be applicable to the paleo-and archicortical progenitors of the neocortex in the structural model. A wider unification by amalgamation with analyses of limbic neocortical relations [5,6] might then be possible. As the cortex emerges by differentiation from cells of limbic origin, during its growth it might be brought, by the same process of predictive error minimization, into harmony with the developing limbic and subcortical systems, while concurrently more direct exchanges of neocortex and environment via major sensory and motor pathways develop.…”

“…Embryologically the neocortex develops in accord with the "structural model" [1][2][3][4]. Neuron precursors migrate and differentiate under genetic control along radial pathways from archi-and paleocortical precursors, the pathways of migration partly determining later functional connections between neocortex and subcortical systems [5,6]. As cellular differentiations proceed, cell connectivity also undergoes modification under the distance rule [7,8] which describes inter-areal connectivity as an approximation to shortest and locally dense pathways-an arrangement facilitating metabolic efficiency and rapid interactions in a "small world".…”