Differential involvement of oriens/pyramidale interneurones in hippocampal network oscillations in vitro

Abstract

Using whole-cell patch-clamp recordings in conjunction with post hoc anatomy we investigated the physiological properties of hippocampal stratum oriens and stratum pyramidale inhibitory interneurones, before and following the induction of pharmacologically evoked gamma frequency network oscillations. Prior to kainate-induced transient epochs of gamma activity, two distinct classes of oriens interneurones, oriens lacunosum-moleculare (O-LM) and trilaminar cells, showed prominent differences in their membrane and firing properties, as well as in the amplitude and kinetics of their excitatory postsynaptic events. In the active network both types of neurone received a phasic barrage of gamma frequency excitatory inputs but, due to their differential functional integration, showed clear differences in their output patterns. While O-LM cells fired intermittently at theta frequency, trilaminar interneurones discharged on every gamma cycle and showed a propensity to fire spike doublets. Two other classes of fast spiking interneurones, perisomatic targeting basket and bistratified cells, in the active network discharged predominantly single action potentials on every gamma cycle. Thus, within a locally excited network, O-LM cells are likely to provide a theta-frequency patterned output to distal dendritic segments, whereas basket and bistratified cells are involved in the generation of locally synchronous gamma band oscillations. The anatomy and output profile of trilaminar cells suggest they are involved in the projection of locally generated gamma rhythms to distal sites. Therefore a division of labour appears to exist whereby different frequencies and spatiotemporal properties of hippocampal rhythms are mediated by different interneurone subtypes.

Highly Energized Inhibitory Interneurons are a Central Element for Information Processing in Cortical Networks

“…This notion has been underlined by elegant in vivo studies in mice showing that selective genetic modification of glutamate receptor subtypes in fast-spiking, PV þ interneurons strongly affects power and synchrony of gamma oscillations, together with impaired hippocampus-dependent cognitive functions. 50,51 56,86,98,112 This finding underlines the general principle of sparse coding by pyramidal cells, which has been suggested to provide an optimal trade-off between information processing and energy efficacy. 113,114 However, pyramidal cells comprise B85% of all neurons in the hippocampus proper, and even with sparse coding they are able to encode multiple representations of spatial and episodic memories.…”

“…8 Some dendritic-targeting interneurons such as bistratified and trilaminar GABAergic interneurons were reported to show fastspiking behavior during hippocampal gamma oscillations. 23,86 However, the class of perisomatic inhibitory interneurons has gained much more attention. 8,16,19,87 This class comprises two types of basket cells as well as axo-axonic (chandelier) cells.…”

“…85 However, the highly divergent axonal plexus of basket cells has a mediolateral extent of 4700 mm within the hippocampus where it contacts somata and proximal dendrites of pyramidal cells. 18,37,86,102 This connectivity feature allows synchronous inhibition of a multitude of pyramidal cells; the estimated numbers range from several hundred up to 2,500 cells. 85,103,104 Together with the dendritictargeting interneurons, the pattern of convergence and divergence in hippocampal network connectivity thus reflects the intense feed-forward and feedback control of principal cells by GABAergic inhibition.…”

“…22,35,47,91,107 These interneurons are able to generate fast series of action potentials up to several hundred Hertz (hence: 'fast-spiking'), and they are active in almost every cycle of gamma oscillations (B30 to 100 Hz) in vitro and in vivo. 35,48,52,56,86,88,108 The resulting fast periodic release of GABA induces strong rhythmic perisomatic inhibition of almost all local principal cells, 9,10,23 which is reflected by the typical gamma oscillations in local field potential recordings. 8,48,52 Thus, fastspiking interneurons are ideally suited to control both pattern and timing of the action potential generation in principal cells ('clockwork'), which has been demonstrated by experimental data and mathematical modeling.…”

Behavior-dependent specialization of identified hippocampal interneurons

“…Different domains of pyramidal cells, such as the soma, axoninitial-segment, proximal or distal dendrites 5 are innervated by distinct types of GABAergic interneuron. They also have distinct inputs and membrane properties 6-10 and show different firing patterns during network oscillations induced in vitro [11][12][13][14] or recorded in anesthetized animals 15 , indicating distinct roles for specific interneuron types. However, research on interneurons in drug-free animals that can freely change their behavior, has so far been limited to recordings from unidentified interneurons because of technical limitations.…”