Fast Oscillations in Cortical Circuits

  • Roger D. Traub,
  • John G. R. Jefferys &
  • Miles A. Whittington
MIT Press: 1999. 324 pp. $57.50, £34.95

The dynamics of groups of nerve cells pose a major challenge in understanding brain function. In that context, Fast Oscillations in Cortical Circuits is a refreshing approach to unravelling one of the most intriguing phenomena displayed by the mammalian brain: the γ oscillation. This brain activity, during which neurons synchronize their firing at a rate of approximately 40 Hz, has been found during a vast variety of behavioural states, ranging from REM (rapid eye-movement) sleep to attentive behaviour in human and animal studies.

Traub, Jefferys and Whittington use a combination of neuronal modelling and electrophysiological experiments to outline their ideas on how γ oscillations are generated. This book is not for the novice. Its main focus resides at the minuscule level at which changes in the membrane potential occur in single neurons from a hippocampal slice. The authors show how these changes can be represented by compartmental modelling of neuronal networks. However, the authors also link these cellular-level descriptions to more complex phenomena such as epilepsy, opiate function and memory formation.

The central mechanism proposed to explain γ oscillations is based on the dynamics of networks of mutually coupled inhibitory interneurons. At the start of the decade, computational studies unravelled the conditions under which such networks display and sustain synchronized oscillatory activity. If the membranes of the interneurons depolarize (become activated) homogeneously and their synaptic connections hyperpolarize (become inhibitory) simultaneously, synchronized firing can occur at an oscillation period that is shorter than the duration of inhibition. In the case of hippocampal basket cells coupled through hyperpolarizing GABAA synapses, such synchronization occurs in the γ frequency range.

Traub, Jefferys and Whittington's central hypothesis is that the homogeneous depolarization necessary for the interneuron network to oscillate is brought about by the action of a single class of neurotransmitter receptor — the metabotropic glutamate receptor. Despite this uni-causal viewpoint, which is by no means universally espoused, the beauty of this book arises from the fact that such hypotheses are clearly formulated, logically argued, then tested by experiments and computational modelling.

The activities of complex neural networks are not always based on complicated rules. Using pharmacological manipulations, the authors skilfully demonstrate the straightforward relationship between the frequency of the γ oscillation and the time course and amplitude of activity at GABAA synapses. Furthermore, they use a two-site stimulation protocol in the CA1 region of a hippocampus slice as an in vitro model for long-range synchronization, and show how interneuron spike doublets are involved in this.

Overall, the book is succinct and informative, and leads the reader through difficult uncharted waters. Unfortunately, the data provided deal exclusively with the hippocampus, and it remains to be shown whether the authors' hypothesis holds true for the neocortex in general. Furthermore, the proposed role of metabotropic glutamate receptors in the generation of γ oscillations naturally invites a thorough review of the various subtypes of glutamate receptor to be found in the neuronal membrane. Finally, some parts of the book are heavy going. Facts are too often presented without being integrated into the authors' context and arguments.

Nevertheless, the interdisciplinary work summarized in the book is exactly the type of research necessary to fill the gap between mechanism and phenomenon in one of the fastest-moving fields in neuroscience.