Dendritic Spikes Induce Ripples in Parvalbumin Interneurons during Hippocampal Sharp Waves

Abstract

Sharp-wave ripples are transient oscillatory events in the hippocampus that are associated with the reactivation of neuronal ensembles within specific circuits during memory formation. Fast-spiking, parvalbumin-expressing interneurons (FS-PV INs) are thought to provide fast integration in these oscillatory circuits by suppressing regenerative activity in their dendrites. Here, using fast 3D two-photon imaging and a caged glutamate, we challenge this classical view by demonstrating that FS-PV IN dendrites can generate propagating Ca(2+) spikes during sharp-wave ripples. The spikes originate from dendritic hot spots and are mediated dominantly by L-type Ca(2+) channels. Notably, Ca(2+) spikes were associated with intrinsically generated membrane potential oscillations. These oscillations required the activation of voltage-gated Na(+) channels, had the same frequency as the field potential oscillations associated with sharp-wave ripples, and controlled the phase of action potentials. Furthermore, our results demonstrate that the smallest functional unit that can generate ripple-frequency oscillations is a segment of a dendrite.

The Effects of Realistic Synaptic Distribution and 3D Geometry on Signal Integration and Extracellular Field Generation of Hippocampal Pyramidal Cells and Inhibitory Neurons

“…The parameters and subthreshold behavior of our models were consistent with those in more detailed conductance-based models (Káli and Freund, 2005; Chiovini et al, 2014), and we believe that most of our conclusions are qualitatively and, in many details, quantitatively robust.…”

“…Dendritic patch-clamp and multiphoton imaging and manipulation techniques have revealed the complexity and importance of dendritic processing in cortical pyramidal neurons. Much less is currently known about dendritic integrative processes in interneurons, although some results do suggest that their dendrites may also have non-linear properties and may have roles beyond the faithful transmission of synaptically evoked signals to the axosomatic output region (Saraga et al, 2003; Chiovini et al, 2014). Meanwhile, a set of studies examined the interactions of specific cell types in cortical networks, with the aim of understanding the generation of different kinds of population dynamics such as coherent oscillations and transient synchrony (Butler and Paulsen, 2015; Gulyás and Freund, 2015).…”

Nonlinear dendritic integration of electrical and chemical synaptic inputs drives fine-scale correlations

“…A prediction would be that directional-selective LGN neurons that receive input from cRGCs will maintain robust direction selectivity over a wider range of stimulus conditions than LGN neurons coding other directions (as directionally selective RGCs coding other directions are not gap junction coupled in the mature retina 13 ). Moreover, given the prevalence of dendritic electrical coupling 3–11 and active dendritic properties 46–49 in neural circuits throughout the CNS, it is likely that mechanisms similar to those presented here may be a general solution to the problem of reliably transmitting weak signals in noisy neural systems.…”

Tasks for inhibitory interneurons in intact brain circuits

“…Activating PV+ cells with moderate light intensity reduced the activity of pyramidal cells but induced fast network oscillations between pyramidal cells and PV+ interneurons, suggesting the critical role of PV-PV interneuron interactions in setting fast oscillation frequency. A combined multi-photon imaging, electrophysiological study showed that dendrites of PV neurons have resonant properties at ripple frequency (Chiovini et al , 2014). …”