Protracted development of motor cortex constrains rich interpretations of infant cognition

Abstract

Cognition in preverbal human infants must be inferred from overt motor behaviors such as gaze shifts, head turns, or reaching for objects. However, infant mammals - including human infants - show protracted postnatal development of cortical motor outflow. Cortical control of eye, face, head, and limb movements is absent at birth and slowly emerges over the first postnatal year and beyond. Accordingly, the neonatal cortex in humans cannot generate the motor behaviors routinely used to support inferences about infants' cognitive abilities, and thus claims of developmental continuity between infant and adult cognition are suspect. Recognition of the protracted development of motor cortex should temper rich interpretations of infant cognition and motivate more serious consideration of the role of subcortical mechanisms in early cognitive development.

Keywords: core knowledge; eye movements; infant cognition; motor cortex; motor maps; visual system.

Figure 1.. The implications of protracted development of cortical motor outflow for neonatal cognition.

(A) The assumption of cortical motor outflow is central to inferences about cortically mediated cognition—especially for claims of developmental continuity between infant and adult cognition. Bottom solid arrow: Researchers use overt motor behavior to draw inferences about complex cognition in young, preverbal infants. Top dashed arrow: Cortically mediated cognition, in turn, can only be expressed as motor behavior if cortical motor outflow exists. Without cortical motor outflow, infant behavior must be mediated subcortically, and thus claims that infant cognition is developmentally continuous are suspect. Indeed, cortical motor outflow is absent in early postnatal development. Photo of infant courtesy of Jaya Rachwani. (B) Highly simplified diagram of motor outflow to the limb and facial muscles and associated sensory feedback (reafference) across early development. (a) Initially, newborn limb and facial movements are produced by brainstem motor systems (solid red lines). (b) Reafference is conveyed to the brainstem and somatosensory regions in thalamus and cortex (green lines). (c) Later in development, cortical motor outflow produces movement via the corticospinal and corticobulbar tracts and also modulates brainstem motor networks (dashed blue lines). In addition, other cortical regions develop the ability to influence cortical motor outflow. A similar developmental trajectory exists for cortical control of eye movements.

Figure 2.. Protracted development of motor maps in M1.

(A) Representative motor maps in rat pups at P25 and P30, and in adult rats at P60. Each map was produced using intracortical microstimulation in the forelimb region of M1 in anesthetized animals. The legends indicate the simple (i.e., single joint) and complex (i.e., multijoint) movements evoked at each stimulation site. Rectangles around the maps demarcate identical cortical surface areas. Adapted from Singleton et al., 2021. (B) Representative motor maps in kittens at P63 and P86, and in adult cats. Each map was produced using intracortical microstimulation in the forelimb region of M1 in anesthetized animals. The legend indicates the single-joint forelimb movements (shoulder, elbow, wrist) and multi-joint movements evoked at each stimulation site. Movements of the digits occurred with movements of other joints. Colors denote the threshold electric current for movement production as indicated by the color bar at right. The black lines show the location of the cruciate sulcus. Adapted from Chakrabarty and Martin, 2000. Both figures used with permission of the American Physiological Society; permission conveyed through Copyright Clearance, Inc.

Figure I.. Sensory origins of primary motor cortex.

(A) Boundaries of primary cortical areas in rats—primary somatosensory cortex (S1, red) and primary motor cortex (M1, blue), and primary auditory (A1) and visual (V1) cortex. (B) Enlargements of red and blue regions in (A) show the somatotopic organization of S1 and M1. Adapted from Dooley et al., 2018. (C) Peri-event histogram showing sensory responsiveness of an individual neuron in the forelimb region of M1 at P20. The neuron’s firing rate is shown in relation to movement onset (vertical dashed line) for twitches (red) and wake movements (black). This neuron is representative of all M1 neurons recorded at this age. Neurons fire above baseline (0 on the y-axis) after—not before—movement onset during both sleep and wake, indicative of sensory responding. Adapted from Dooley et al., 2021.