Subcortico-Cortical Functional Connectivity in the Fetal Brain: A Cognitive Development Blueprint

Abstract

Recent evidence has shown that patterns of cortico-cortical functional synchronization are consistently traceable by the end of the third trimester of pregnancy. The involvement of subcortical structures in early functional and cognitive development has never been explicitly investigated, notwithstanding their pivotal role in different cognitive processes. We address this issue by exploring subcortico-cortical functional connectivity at rest in a group of normally developing fetuses between the 25th and 32nd weeks of gestation. Results show significant functional coupling between subcortical nuclei and cortical networks related to: (i) sensorimotor processing, (ii) decision making, and (iii) learning capabilities. This functional maturation framework unearths a Cognitive Development Blueprint, according to which grounding cognitive skills are planned to develop with higher ontogenetic priority. Specifically, our evidence suggests that a newborn already possesses the ability to: (i) perceive the world and interact with it, (ii) create salient representations for the selection of adaptive behaviors, and (iii) store, retrieve, and evaluate the outcomes of interactions, in order to gradually improve adaptation to the extrauterine environment.

Keywords: brain development; cognitive control; learning; resting state fMRI; sensorimotor.

Figure 1

Functional synchronization patterns underlying the “Cognitive Development Blueprint,” a set of “cognitive tools” developed during gestation in order to allow the incoming newborn a successful interaction with the extrauterine environment (i.e. allowing for survival). (a) “Sensorimotor” (upper left) functionality synchronization, involving the maturation of a complex network of cortical, subcortical, and mesolimbic processing loci supporting environmental perception and voluntary control of movement. (b) “Decision Making” (upper right) functionality synchronization, involving the maturation of networks (i.e. salience network and DMN) underlying the management of attentional resources, supporting selection, and proper execution of survival-oriented behaviors. (c) “Learning” (bottom) functionality synchronization involving the maturation of the medial temporal lobe memory system, as well as of temporal structures supporting the ability to represent, store and retrieve gathered information at different levels of complexity.