Oscillatory dynamics in the hippocampus support dentate gyrus–CA3 coupling

Abstract

Gamma oscillations in the dentate gyrus and hippocampal CA3 show variable coherence in vivo, but the mechanisms and relevance for information flow are unknown. We found that carbacholinduced oscillations in rat CA3 have biphasic phase-response curves, consistent with the ability to couple with oscillations in afferent projections. Differences in response to stimulation of either the intrinsic feedback circuit or the dentate gyrus were well described by varying an impulse vector in a two-dimensional dynamical system, representing the relative input to excitatory and inhibitory neurons. Responses to sinusoidally modulated optogenetic stimulation confirmed that the CA3 network oscillation can entrain to periodic inputs, with a steep dependence of entrainment phase on input frequency. CA3 oscillations are therefore suited to coupling with oscillations in the dentate gyrus over a broad range of frequencies. Many brain areas, including the dentate gyrus and hippocampal CA3, show prominent gamma oscillations whose inter-region coherence varies during awake activity 1,2 . Structures of gamma-oscillatory activity in the temporal lobe are modulated by both brain state 3 and task demands 4,5 . Such changing patterns of coherent oscillatory activity may be involved in controlling information flow among connected networks 6-8 . The dynamical mechanisms underlying the emergence of coherence among anatomically coupled networks are, however, poorly understood.During gamma oscillations, individual neurons spike irregularly 1,2,9-11 , but the collective dynamics of the local network are oscillatory. Thus, the emergence of phase coherence between regions is a process of synchronization between local network oscillators. Important determinants of the synchronization properties of systems of coupled oscillators are the phase-response curves (PRCs) of the constituents 12-14 . Synchronization through excitatory connections is strongly promoted by biphasic PRCs, in which the same input can either advance or delay the phase of oscillation depending on when the perturbation occurs during the oscillatory cycle. Such PRCs allow oscillators to entrain to periodic inputs at both higher and lower frequencies than the unperturbed oscillation frequency. Although the mechanisms generating gamma oscillations in local networks have been extensively studied 9,11,15,16 , the phase response dynamics of the resulting network oscillators have not been measured, nor have their entrainment properties in response to periodic inputs been

Tonic GABA A conductance bidirectionally controls interneuron firing pattern and synchronization in the CA3 hippocampal network

“…10). Assuming that changes in the power of oscillations and in their frequency can have different computational meanings (24), the effect of tonic GABA A conductance on pyramidal neurons can provide a mechanism enabling increases in the oscillation power without changes in their frequency.…”

Population dynamics of the modified theta model: macroscopic phase reduction and bifurcation analysis link microscopic neuronal interactions to macroscopic gamma oscillation

“…Although the PRF derived by the adjoint method is generally used to evaluate the effect of external perturbations [16,17], in our study, the macroscopic PRF was successfully applied to evaluate not only the effects of external perturbations but also how intrinsic parameter changes alter the macroscopic oscillatory dynamics. Recent experiments have used optogenetic tools to selectively drive subpopulations of neurons with periodic stimuli [12,21,36]; the adjoint method allows us to investigate the effects of such perturbations on the macroscopic gamma oscillations analytically. Many studies have used the LIF model [25,35,37] or other neuronal models [26,38] to investigate the properties of population rhythms.…”

“…The macroscopic PRF with its link to the microscopic one (equation (2.30)) enables us to understand the complicated relationships between microscopic structure and macroscopic oscillatory dynamics, and it cannot be achieved by the phase reduction of the simplified firing rate models of neuronal population [21,44].…”

Chemical–genetic attenuation of focal neocortical seizures

“…26). Ten to eleven weeks later, the animals were transcardially perfused with a room temperature solution containing (in mM): N-Methyl-D-glucamine-Cl, 92; KCl, 2.5; NaH 2 PO 4 , 1.25; Thiourea, 2; Ascorbic acid, 5; Na-Pyruvate, 3; MgCl 2 , 10; D-Glucose, 25; NaHCO 3 , 30; CaCl 2 , 0.5; Sucrose, 1 and horizontal hippocampal slices were prepared.…”