Scientific Understanding of Consciousness
Consciousness as an Emergent Property of Thalamocortical Activity

Dendritic Mechanisms in Interneurons

 

Science 1 January 2010: Vol. 327. no. 5961, pp. 52 - 58

Dendritic Mechanisms Underlying Rapid Synaptic Activation of Fast-Spiking Hippocampal Interneurons

Hua Hu,^1,2 Marco Martina,^1,3 Peter Jonas^1,4

¹ Institute of Physiology I, Universität Freiburg, Engesserstraße 4, D-79108 Freiburg, Germany.
² Department of Physiology at Institute of Basic Medical Sciences and Centre for Molecular Biology and Neuroscience (CMBN), University of Oslo, Blindern, NO-0317 Oslo, Norway.
³ Department of Physiology, The Feinberg School of Medicine of Northwestern University, 303 East Chicago Avenue, Chicago, IL 60611, USA.
⁴ Freiburg Institute for Advanced Studies, Albertstraße 19, D-79104 Freiburg, Germany.

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Fast-spiking, parvalbumin-expressing basket cells (BCs) are important for feedforward and feedback inhibition. During network activity, BCs respond with short latency and high temporal precision. It is thought that the specific properties of input synapses are responsible for rapid recruitment. However, a potential contribution of active dendritic conductances has not been addressed. We combined confocal imaging and patch-clamp techniques to obtain simultaneous somatodendritic recordings from BCs. Action potentials were initiated in the BC axon and backpropagated into the dendrites with reduced amplitude and little activity dependence. These properties were explained by a high K⁺ to Na⁺ conductance ratio in BC dendrites. Computational analysis indicated that dendritic K⁺ channels convey unique integration properties to BCs, leading to the rapid and temporally precise activation by excitatory inputs.

Fast-spiking, parvalbumin-expressing, -aminobutyric acid (GABA)–releasing (GABAergic) interneurons (BCs) play a key role in the function of neuronal networks. These neurons set a narrow time window for temporal summation in principal neurons by fast feedforward and feedback inhibition, contribute to the generation of network oscillations, and are thought to be involved in higher brain function and dysfunction. After stimulation of excitatory input synapses in vitro, BCs respond with remarkable speed, exquisite temporal precision, and preferential activity in the onset phase of a stimulus train. Similarly, during network activity in vivo, such as sharp-wave ripple or theta rhythms, BCs are activated by input from principal neurons with short latency and minimal jitter. The mechanisms underlying this rapid and precise activation are unclear. It is generally thought that synaptic factors, such as the time course of the postsynaptic conductance and the extent of depression or facilitation, play an important role. Alternatively or additionally, the electrical properties of interneuron dendrites may contribute. Whereas the dendrites of pyramidal neurons were extensively characterized, those of fast-spiking, parvalbumin-expressing BCs have not been directly examined. However, Ca2+ imaging experiments suggest that Na+, K+, and Ca2+ channels may be present in the dendrites of neocortical fast-spiking interneurons.

To study the dendrites of BCs directly, we used confocally targeted patch-clamp recording in hippocampal slices. BCs were identified on the basis of the location of the axon in the granule cell layer; the fast-spiking AP phenotype  (mean maximal frequency 104.2 ± 2.2 Hz). Detailed analysis of the axonal arbor revealed that our sample was mainly composed of classical basket cells with tangential collaterals but also included a subpopulation of cells with radial collaterals, suggestive of axo-axonic cells. We made simultaneous recordings from somata and apical dendrites of dentate gyrus BCs at distances up to 300 µm from the soma, close to the physical dendritic length.

Because the dendrites of BCs differ significantly from those of somatostatin-expressing interneurons, our results demonstrate that the diversity of GABAergic interneurons extends to the dendritic level. Thus, dendritic properties may contribute to setting the rules for routing of activity in inhibitory microcircuits.

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