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Quantitative ultrastructural analysis of basket and axo-axonic cell terminals in the mouse hippocampus

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Abstract

Three functionally different populations of perisomatic interneurons establish GABAergic synapses on hippocampal pyramidal cells: parvalbumin (PV)-containing basket cells, type 1 cannabinoid receptor (CB1)-positive basket cells both of which target somata, and PV-positive axo-axonic cells that innervate axon initial segments. Using electron microscopic reconstructions, we estimated that a pyramidal cell body receives synapses from about 60 and 140 synaptic terminals in the CA1 and CA3 area, respectively. About 60 % of these terminals were PV positive, whereas 35–40 % of them were CB1 positive. Only about 1 % (CA1) and 4 % (CA3) of the somatic boutons were negative for both markers. Using fluorescent labeling, we showed that most of the CB1-positive terminals expressed vesicular glutamate transporter 3. Reconstruction of somatic boutons revealed that although their volumes are similar, CB1-positive boutons are more flat and the total volume of their mitochondria was smaller than that of PV-positive boutons. Both types of boutons contain dense-core vesicles and frequently formed multiple release sites on their targets and innervated an additional soma or dendrite as well. PV-positive boutons possessed small, macular synapses; whereas the total synaptic area of CB1-positive boutons was larger and formed multiple irregular-shaped synapses. Axo-axonic boutons were smaller than somatic boutons, had only one synapse and their ultrastructural parameters were closer to those of PV-positive somatic boutons. Our results represent the first quantitative measurement—using a highly reliable method—of the contribution of different cell types to the perisomatic innervation of pyramidal neurons, and may help to explain functional differences in their output properties.

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Acknowledgments

We thank Dr. Kenneth G. Baimbridge for the rabbit anti-PV antibody and Dr. Ken Mackie (supported by National Institutes of Health Grant DA11322) and Dr. Masahiko Watanabe for the anti-CB1 antibodies. The excellent technical assistance of Katalin Lengyel, Emőke Szépné Simon, Katalin Iványi and Győző Goda is also gratefully acknowledged. This work was supported by the National Institutes of Health (Grant Number NS030549), National Office for Research and Technology—Hungarian Scientific Research Fund (NKTH-OTKA, Grant Number CNK77793, K83251) and European Research Council (Grant Number ERC-2011-ADG-294313, SERRACO). G.N. was supported by a János Bolyai Research Scholarship.

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  1. Laboratory of Cerebral Cortex Research, Department of Cellular and Network Neurobiology, Institute of Experimental Medicine, Hungarian Academy of Sciences, 1083, Budapest, Hungary

    Virág T. Takács, András Szőnyi, Tamás F. Freund, Gábor Nyiri & Attila I. Gulyás

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  1. Virág T. Takács
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  2. András Szőnyi
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  3. Tamás F. Freund
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Correspondence to Gábor Nyiri.

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G. Nyiri and A. I. Gulyás contributed equally to this work.

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Takács, V.T., Szőnyi, A., Freund, T.F. et al. Quantitative ultrastructural analysis of basket and axo-axonic cell terminals in the mouse hippocampus. Brain Struct Funct 220, 919–940 (2015). https://doi.org/10.1007/s00429-013-0692-6

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