Cell type‐specific and activity‐dependent dynamics of action potential‐evoked Ca2+ signals in dendrites of hippocampal inhibitory interneurons

• Published in: The Journal of physiology 2011-04, Vol.589 (8), p.1957-1977
• Main Authors: Evstratova, Alesya, Chamberland, Simon, Topolnik, Lisa
• Format: Article
• Language: English
• Subjects: Action Potentials; Analysis of Variance; Animals; Calcium Signaling; Dendrites - metabolism; Electric Stimulation; Feedback, Physiological; Hippocampus - cytology; Hippocampus - metabolism; In Vitro Techniques; Inhibitory Postsynaptic Potentials; Interneurons - metabolism; Kinetics; Mice; Mice, Inbred C57BL; Microscopy, Fluorescence, Multiphoton; Nerve Net - physiology; Neural Inhibition; Neural Pathways - metabolism; Neuronal Plasticity; Neuroscience; Patch-Clamp Techniques; Synaptic Transmission; Theta Rhythm
• ISSN: 0022-3751; 1469-7793
• DOI: 10.1113/jphysiol.2010.204255

Non‐technical summary  Action potentials generated at the level of the cell body can propagate back to neuronal dendrites, where they activate different types of voltage‐sensitive calcium channels and produce massive calcium influx. Although these calcium signals may control dendritic integration, their mechanisms, dynamic properties and role in different cell types remain largely unknown. We found that in dendrites of hippocampal interneurons, an inhibitory cell type involved in control of network excitability, specific types of calcium channels are present but are recruited in an activity‐dependent manner. Furthermore, their activation produces calcium rises spatially restricted to proximal dendritic sites, where they control the efficacy of transmission at inhibitory synapses. The pathway by which this happens appears to constitute a negative feedback loop – increased firing activity of interneurons potentiates the inhibitory drive that they receive, thus decreasing the activity of interneurons further. This may have a profound effect on the recruitment of interneurons and network activity.   In most central neurons, action potentials (APs), generated in the initial axon segment, propagate back into dendrites and trigger considerable Ca2+ entry via activation of voltage‐sensitive calcium channels (VSCCs). Despite the similarity in its underlying mechanisms, however, AP‐evoked dendritic Ca2+ signalling often demonstrates a cell type‐specific profile that is determined by the neuron dendritic properties. Using two‐photon Ca2+ imaging in combination with patch‐clamp whole‐cell recordings, we found that in distinct types of hippocampal inhibitory interneurons Ca2+ transients evoked by backpropagating APs not only were shaped by the interneuron‐specific properties of dendritic Ca2+ handling but also involved specific Ca2+ mechanisms that were regulated dynamically by distinct activity patterns. In dendrites of regularly spiking basket cells, AP‐evoked Ca2+ rises were of large amplitude and fast kinetics; however, they decreased with membrane hyperpolarization or following high‐frequency firing episodes. In contrast, AP‐evoked Ca2+ elevations in dendrites of Schaffer collateral‐associated cells exhibited significantly smaller amplitude and slower kinetics, but increased with membrane hyperpolarization. These cell type‐specific properties of AP‐evoked dendritic Ca2+ signalling were determined by distinct endogenous buffer capacities of the interneurons examine