Development and function of human cerebral cortex neural networks from pluripotent stem cells in vitro

Development. 2015 Sep 15;142(18):3178-87. doi: 10.1242/dev.123851.

Abstract

A key aspect of nervous system development, including that of the cerebral cortex, is the formation of higher-order neural networks. Developing neural networks undergo several phases with distinct activity patterns in vivo, which are thought to prune and fine-tune network connectivity. We report here that human pluripotent stem cell (hPSC)-derived cerebral cortex neurons form large-scale networks that reflect those found in the developing cerebral cortex in vivo. Synchronised oscillatory networks develop in a highly stereotyped pattern over several weeks in culture. An initial phase of increasing frequency of oscillations is followed by a phase of decreasing frequency, before giving rise to non-synchronous, ordered activity patterns. hPSC-derived cortical neural networks are excitatory, driven by activation of AMPA- and NMDA-type glutamate receptors, and can undergo NMDA-receptor-mediated plasticity. Investigating single neuron connectivity within PSC-derived cultures, using rabies-based trans-synaptic tracing, we found two broad classes of neuronal connectivity: most neurons have small numbers (<10) of presynaptic inputs, whereas a small set of hub-like neurons have large numbers of synaptic connections (>40). These data demonstrate that the formation of hPSC-derived cortical networks mimics in vivo cortical network development and function, demonstrating the utility of in vitro systems for mechanistic studies of human forebrain neural network biology.

Keywords: Cerebral cortex; Human; Networks; Neural development; Stem cells.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Cerebral Cortex / cytology
  • Cerebral Cortex / growth & development*
  • Dendritic Spines / ultrastructure
  • Humans
  • Image Processing, Computer-Assisted
  • In Vitro Techniques / methods*
  • Microscopy, Fluorescence
  • Nerve Net / cytology
  • Nerve Net / growth & development*
  • Neuronal Plasticity / physiology
  • Patch-Clamp Techniques
  • Pluripotent Stem Cells / physiology*
  • Reverse Transcriptase Polymerase Chain Reaction
  • Single-Cell Analysis
  • Video Recording