Waking-like Brain Function in Embryos

Abstract

Experience-dependent plastic changes in the brain underlying complex forms of learning are generally initiated when organisms are awake, and this may limit the earliest developmental time at which learning about external events can take place. It is not known whether waking-like brain function is present prenatally in higher vertebrate (bird or mammal) embryos, or whether embryos have brain circuitry that can selectively turn on a waking-like state in response to salient external sensory stimulation. Combining submillimeter-resolution brain positron emission tomography (PET), structural X-ray computed tomography (CT) of the skeleton for fine-scale embryo aging, and noninvasive behavioral recording of chicken embryos in the egg revealed unexpectedly wide variation in prenatal brain activity, inversely related to behavioral activity, which developed into different sleep-like fetal brain states. Brief prenatal exposure to a salient chicken vocalization (eliciting strong postnatal behavioral responses) increased higher-brain activity significantly more than a spectrally and temporally matching "nonvocal" noise analog. Patterns of correlated activity between the brainstem and higher-brain areas resembling awake, posthatching animals were seen exclusively in chicken-stimulated embryos. Waking-like brain function is present in a latent but inducible state during the final 20% of embryonic life, selectively modulated by context-dependent monitoring circuitry. These data also reveal the developmental emergence of sleep-like behavior and its linkage to metabolic brain states and highlight problems with assigning embryo brain states based on behavioral observations.