Developmental changes in propagation patterns and transmitter dependence of waves of spontaneous activity in the mouse cerebral cortex

• Published in: The Journal of physiology 2011-05, Vol.589 (10), p.2529-2541
• Main Authors: Conhaim, Jay, Easton, Curtis R., Becker, Matthew I., Barahimi, Mitra, Cedarbaum, Emily R., Moore, Jennifer G., Mather, Luke F., Dabagh, Sarah, Minter, Daniel J., Moen, Samantha P., Moody, William J.
• Format: Article
• Language: English
• Subjects: Action Potentials - physiology; alpha -Amino-3-hydroxy-5-methyl-4-isoxazole propionic acid receptors; Animals; Animals, Newborn; Brain; Brain Waves - physiology; Cells, Cultured; Central nervous system; Cerebral Cortex - growth & development; Cerebral Cortex - physiology; Cortex; Dependence; Developmental stages; Embryos; Female; gamma -Aminobutyric acid; gamma-Aminobutyric Acid - physiology; Glutamic Acid - physiology; Information processing; Mice; Mice, Inbred Strains; Neonates; Neurons; Neurons - physiology; Neuroscience; Neurotransmission; Neurotransmitter Agents - physiology; Pacemakers; Propagation; Rodents; Septum; Structure-function relationships; Waves
• ISSN: 0022-3751; 1469-7793
• DOI: 10.1113/jphysiol.2010.202382

Non‐technical summary  It is not well understood how all of the connections among neurons required for the brain to process information are established during development. It has recently become apparent that waves of spontaneous electrical activity spread across large groups of neurons during early brain development and that these waves of activity are crucial for correct development of brain circuitry. In this paper, we show that waves of spontaneous electrical activity propagate across the mouse cerebral cortex, beginning on the day before birth and continuing through the first 12 postnatal days. These waves are initiated at specific locations in the cortex, which do not change during the period of wave generation. Identity of the neurons that initiate the waves, however, does change during this time. This work indicates that even though spontaneous electrical activity occurs during a short contiguous period of development, the mechanisms underlying that activity change.   Waves of spontaneous electrical activity propagate across many regions of the central nervous system during specific stages of early development. The patterns of wave propagation are critical in the activation of many activity‐dependent developmental programs. It is not known how the mechanisms that initiate and propagate spontaneous waves operate during periods in which major changes in neuronal structure and function are taking place. We have recently reported that spontaneous waves of activity propagate across the neonatal mouse cerebral cortex and that these waves are initiated at pacemaker sites in the septal nucleus and ventral cortex. Here we show that spontaneous waves occur between embryonic day 18 (E18) and postnatal day 12 (P12), and that during that period they undergo major changes in transmitter dependence and propagation patterns. At early stages, spontaneous waves are largely GABA dependent and are mostly confined to the septum and ventral cortex. As development proceeds, wave initiation depends increasingly on AMPA‐type glutamate receptors, and an ever increasing fraction of waves propagate into the dorsal cortex. The initiation sites and restricted propagation of waves at early stages are highly correlated with the position of GABAergic neurons in the cortex. The later switch to a glutamate‐based mechanism allows propagation of waves into the dorsal cortex, and appears to be a compensatory mechanism that ensures continued wave generation even as GABA transmission bec