Origins and distribution of cholinergically induced beta rhythms in hippocampal slices

Ken Shimono, Fernando Brucher, Richard Granger, Gary Lynch and Makoto Taketani
Journal of Neuroscience (2000), 20 , 8462-8473.

Regional variations and substrates of high-frequency rhythmic activity induced by cholinergic stimulation were studied in hippocampal slices with 64-electrode recording arrays. 1) Carbachol triggered beta waves (17.6 ± 5.7 Hz) in pyramidal regions of 75% of the slices. 2) The waves had phase shifts across the cell body layers and were substantially larger in the apical dendrites than in cell body layers or basal dendrites. 3) Continuous, two-dimensional current source density analyses indicated apical sinks associated with basal sources, lasting approximately 10 ms, followed byapical sources and basal sinks, lasting about 20 ms, in a repeating pattern with a period in the range 15-25 Hz. 4) Carbachol-induced beta waves in hippocampus were accompanied by 40 Hz (gamma) oscillations in deep layers of entorhinal cortex. 5) Cholinergically-elicited beta and gamma rhythms were eliminated by antagonists of either AMPA or GABA receptors. Benzodiazepines markedly enhanced beta activity and sometimes introduced a distinct gamma frequency peak. 6) 20 Hz activity following orthodromic activation of field CA3 was distributed in the same manner as carbachol-induced beta waves and was generated by a current source in the apical dendrites of CA3. This source was eliminated by high concentrations of GABAA receptor blockers. It is concluded that cholinergically driven beta rhythms arise independently in hippocampal subfields from oscillatory circuits involving i) bursts of pyramidal cell discharges, ii) activation of a subset of feedback interneurons that project apically, iii) production of a GABAA-mediated hyperpolarization in the outer portions of the apical dendrites of pyramidal neurons.