Rapid Cortical Oscillations and Early Motor Activity in Premature Human Neonate

Mathieu Milh,Anna Kaminska,Alexandre Lapillonne,Catherine Huon,Rustem Khazipov,Yehezkel Ben-Ari

doi:10.1093/cercor/bhl069

Abstract

Delta-brush is the dominant pattern of rapid oscillatory activity (8-25 Hz) in the human cortex during the third trimester of gestation. Here, we studied the relationship between delta-brushes in the somatosensory cortex and spontaneous movements of premature human neonates of 29-31 weeks postconceptional age using a combination of scalp electroencephalography and monitoring of motor activity. We found that sporadic hand and foot movements heralded the appearance of delta-brushes in the corresponding areas of the cortex (lateral and medial regions of the contralateral central cortex, respectively). Direct hand and foot stimulation also reliably evoked delta-brushes in the same areas. These results suggest that sensory feedback from spontaneous fetal movements triggers delta-brush oscillations in the central cortex in a somatotopic manner. We propose that in the human fetus in utero, before the brain starts to receive elaborated sensory input from the external world, spontaneous fetal movements provide sensory stimulation and drive delta-brush oscillations in the developing somatosensory cortex contributing to the formation of cortical body maps.

Highlights

Patterns of correlated neuronal activity play an important role in cortical development by guiding neuronal differentiation, migration, synaptogenesis, and formation of neuronal networks (Van der Loos and Woolsey 1973; Komuro and Rakic 1993; Rakic and Komuro 1995; Katz and Shatz 1996; Ben Ari 2001; Holmes and McCabe 2001; Llinas 2001; Fox 2002; Cang and others 2005; Moody and Bosma 2005)
Comparing the occurrence of delta-brushes at different bipolar derivations, we found that delta-brushes can be correlated over large cortical areas, sometimes over the whole cortex, but can be spatially confined (Fig. 1B,F)
We provide evidence that during the fetal stage of human development, spontaneous movements provide, Page 6 of 13 Twitches and Delta-Brushes in Premature Neonate d Milh and others via feedback signaling, sensory stimulation and trigger deltabrushes in the developing somatosensory cortex in a somatotopic manner

Summary

Introduction

Patterns of correlated neuronal activity play an important role in cortical development by guiding neuronal differentiation, migration, synaptogenesis, and formation of neuronal networks (Van der Loos and Woolsey 1973; Komuro and Rakic 1993; Rakic and Komuro 1995; Katz and Shatz 1996; Ben Ari 2001; Holmes and McCabe 2001; Llinas 2001; Fox 2002; Cang and others 2005; Moody and Bosma 2005). Studies in animal models have revealed that neuronal activity in the developing visual and somatosensory cortical areas is determined by 2 different yet important mechanisms: intrinsic oscillations and afferent input. During early postnatal development, both the visual and somatosensory developing systems of altricial animals possess endogenous. The role of such endogenous mechanisms of sensory stimulation should be even more important in primates. Both in human and nonhuman primates, extensive development of the somatosensory cortex takes place during the fetal stage (Molliver and others 1973; Rakic and others 1986; Zecevic and Rakic 1991, 2001; Burkhalter and others 1993; Kostovic and Judas 2002). In keeping with the findings made in the neonatal rat (Khazipov and others 2004), this raises a hypothesis that spontaneous motor activity provides sensory input and drives cortical activity in human fetus

Methods

Results

Conclusion