Origins and Distribution of Cholinergically Induced β Rhythms in Hippocampal Slices

Abstract

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 ␤ waves (17.6 Ϯ 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, twodimensional current source density analyses indicated apical sinks associated with basal sources, lasting ϳ10 msec, followed by apical sources and basal sinks, lasting ϳ20 msec, in a repeating pattern with a period in the range of 15-25 Hz. (4) Carbachol-induced ␤ waves in the hippocampus were accompanied by 40 Hz (␥) oscillations in deep layers of the entorhinal cortex. (5) Cholinergically elicited ␤ and ␥ rhythms were eliminated by antagonists of either AMPA or GABA receptors. Benzodiazepines markedly enhanced ␤ activity and sometimes introduced a distinct ␥ frequency peak. (6) Twenty Hertz activity after orthodromic activation of field CA3 was distributed in the same manner as carbachol-induced ␤ waves and was generated by a current source in the apical dendrites of CA3. This source was eliminated by high concentrations of GABA A receptor blockers. It is concluded that cholinergically driven ␤ rhythms arise independently in hippocampal subfields from oscillatory circuits involving (1) bursts of pyramidal cell discharges, (2) activation of a subset of feedback interneurons that project apically, and (3) production of a GABA A -mediated hyperpolarization in the outer portions of the apical dendrites of pyramidal neurons.

Use of multi-electrode array recordings in studies of network synaptic plasticity in both time and space

“…(4) evaluation of network physiological properties and the pharmacological effects of compounds [16,22,45,46] ; (5) stable recording that is less sensitive to factors such as mechanical vibration [42,43] ; and (6) a tremendous variety of research applications involving acute brain slices [10,16,45,47] , organotypic slice cultures [38,44,46,48] and dissociated cell cultures [7,17] . It is well-suited for studying synaptic plasticity [21,[31][32][33] , single unit activity [49,50] , rhythmic activity [17,45,51] , and pharmacological drug testing [23,46,52] .…”

“…It is well-suited for studying synaptic plasticity [21,[31][32][33] , single unit activity [49,50] , rhythmic activity [17,45,51] , and pharmacological drug testing [23,46,52] . Furthermore, powerful analytical softwares (e.g.…”

Mode shifting between storage and recall based on novelty detection in oscillating hippocampal circuits

“…One component of this pathway originates from cholinergic septal cells, and targets both pyramidal and inhibitory cells in the hippocampal formation (Frotscher and Ler-anth, 1985). Although this projection enhances hippocampal and entorhinal theta (Stewart and Fox, 1990;Alonso and Klink, 1997;Tóth et al, 1997;Shimono et al, 2000), it is not crucial to its expression (Stewart and Fox, 1989a,b;Lee et al, 1999). The other component emanates from intrinsically rhythmic GABAergic neurons in the MS-DB.…”

“…The mechanisms generating these gamma oscillations involve networks of mutually inhibitory interneurons, likely basket and axo-axonic cells, that are excited by principal cells and ACh. These interneurons fire in gamma bursts, concomitant with increased principal cell activity, providing fast feedback inhibition to the perisomatic region of principal cells (Chrobak and Buzsaki, 1998;Traub et al, 1998;Shimono et al, 2000).…”

“…The model incorporates many features of this circuitry, including structural and functional properties of the subregions and connections, feedback and feedforward inhibition, and oscillatory population dynamics in the theta (4)(5)(6)(7)(8)(9)(10) and gamma (20 -40 Hz) frequency range (Shimono et al, 2000). In addition, most of the known effects of ACh at the cellular level were modeled, with realistic onset and decay time constants for the effects of ACh.…”