Abstract
Recent studies have shown that the dendrites of several neurons are not simple translators but are crucial facilitators of excitatory postsynaptic potential (EPSP) propagation and summation of synaptic inputs to compensate for inherent voltage attenuation. Granule cells (GCs)are located at the gateway for valuable information arriving at the hippocampus from the entorhinal cortex. However, the underlying mechanisms of information integration along the dendrites of GCs in the hippocampus are still unclear. In this study, we investigated the input integration around dendritic branches of GCs in the rat hippocampus. We applied differential spatiotemporal stimulations to the dendrites using a high-speed glutamate-uncaging laser. Our results showed that when two sites close to and equidistant from a branching point were simultaneously stimulated, a nonlinear summation of EPSPs was observed at the soma. In addition, nonlinear summation (facilitation) depended on the stimulus location and was significantly blocked by the application of a voltage-dependent Ca2+ channel antagonist. These findings suggest that the nonlinear summation of EPSPs around the dendritic branches of hippocampal GCs is a result of voltage-dependent Ca2+ channel activation and may play a crucial role in the integration of input information.
This is a preview of subscription content, access via your institution.







References
Alonso A, Klink R (1993) Differential electro responsiveness of stellate and pyramidal-like cells of medial entorhinal cortex layer II. J Neurophysiol 70(1):128–143
Amaral DG, Scharfman HE, Lavenex P (2007) The dentate gyrus: fundamental neuroanatomical organization (dentate gyrus for dummies). Prog Brain Res 163:3–22. doi:10.1016/S0079-6123(07)63001-5
Aradi I, Holmes WR (1999) Role of multiple calcium and calcium-dependent conductances in regulation of hippocampal dentate granule cell excitability. J Comput Neurosci 6(3):215–235
Branco T, Häusser M (2010) The single dendritic branch as a fundamental functional unit in the nervous system. Curr Opin Neurobiol 20(4):494–502. doi:10.1016/j.conb.2010.07.009
Branco T, Häusser M (2011) Synaptic integration gradients in single cortical pyramidal cell dendrites. Neuron 69(5):885–892. doi:10.1016/j.neuron.2011.02.006
Branco T, Clark BA, Häusser M (2010) Dendritic discrimination of temporal input sequences in cortical neurons. Science 329(5999):1671–1675. doi:10.1126/science.1189664
Buckmaster PS, Strowbridge BW, Kunkel DD, Schmiege DL, Schwartzkroin PA (1992) Mossy cell axonal projections to the dentate gyrus molecular layer in the rat hippocampal slice. Hippocampus 2(4):349–362. doi:10.1002/hipo.450020403
Buckmaster PS, Wenzel HJ, Kunkel DD, Schwartzkroin PA (1996) Axon arbors and synaptic connections of hippocampal mossy cells in the rat in vivo. J Comp Neurol 366(2):271–292
Claiborne BJ, Amaral DG, Cowan WM (1990) Quantitative, three-dimensional analysis of granule cell dendrites in the rat dentate gyrus. J Comp Neurol 302(2):206–219. doi:10.1002/cne.903020203
Fyhn M, Molden S, Witter MP, Moser EI, Moser MB (2004) Spatial representation in the entorhinal cortex. Science 305(5688):1258–1264. doi:10.1126/science.1099901
Hargreaves EL, Rao G, Lee I, Knierim JJ (2005) Major dissociation between medial and lateral entorhinal input to dorsal hippocampus. Science 308(5729):1792–1794. doi:10.1126/science.1110449
Hayman RM, Jeffery KJ (2008) How heterogeneous place cell responding arises from homogeneous grids—a contextual gating hypothesis. Hippocampus 18(12):1301–1313. doi:10.1002/hipo.20513
Jackson MB, Scharfman HE (1996) Positive feedback from hilar mossy cells to granule cells in the dentate gyrus revealed by voltage-sensitive dye and microelectrode recording. J Neurophysiol 76(1):601–616
Jaffe DB, Carnevale NT (1999) Passive normalization of synaptic integration influenced by dendritic architecture. J Neurophysiol 82(6):3268–3285
Jinde S, Zsiros V, Nakazawa K (2013) Hilar mossy cell circuitry controlling dentate granule cell excitability. Front Neural Circuits 7:14. doi:10.3389/fncir.2013.00014
Kojima H (2006) Development of a system for patterned rapid photolysis and 2-photon confocal microscopy. Circuits Devices Mag IEEE 22:66–74
Krueppel R, Remy S, Beck H (2011) Dendritic integration in hippocampal dentate granule cells. Neuron 71(3):512–528. doi:10.1016/j.neuron.2011.05.043
Kubota Y, Karube F, Nomura M, Gulledge AT, Mochizuki A, Schertel A, Kawaguchi Y (2011) Conserved properties of dendritic trees in four cortical interneuron subtypes. Sci Rep 1:89. doi:10.1038/srep00089
London M, Häusser M (2005) Dendritic computation. Annu Rev Neurosci 28:503–532. doi:10.1146/annurev.neuro.28.061604.135703
McRory JE, Santi CM, Hamming KS, Mezeyova J, Sutton KG, Baillie DL, Stea A, Snutch TP (2001) Molecular and functional characterization of a family of rat brain T-type calcium channels. J Biol Chem 276(6):3999–4011. doi:10.1074/jbc.M008215200
Nishimura-Akiyoshi S, Niimi K, Nakashiba T, Itohara S (2007) Axonal netrin-Gs transneuronally determine lamina-specific subdendritic segments. Proc Natl Acad Sci USA 104(37):14801–14806. doi:10.1073/pnas.0706919104
Rall W (1962) Electrophysiology of a dendritic neuron model. Biophys J 2(2 Pt 2):145–167
Schmidt-Hieber C, Jonas P, Bischofberger J (2007) Subthreshold dendritic signal processing and coincidence detection in dentate gyrus granule cells. J Neurosci Off J Soc Neurosci 27(31):8430–8441. doi:10.1523/JNEUROSCI.1787-07.2007
Tahvildari B, Alonso A (2005) Morphological and electrophysiological properties of lateral entorhinal cortex layers II and III principal neurons. J Comp Neurol 491(2):123–140. doi:10.1002/cne.20706
Wang X, Lambert NA (2003) Membrane properties of identified lateral and medial perforant pathway projection neurons. Neuroscience 117(2):485–492. doi:10.1016/s0306-4522(02)00659-0
Yoganarasimha D, Rao G, Knierim JJ (2011) Lateral entorhinal neurons are not spatially selective in cue-rich environments. Hippocampus 21(12):1363–1374. doi:10.1002/hipo.20839
Yoneyama M, Fukushima Y, Tsukada M, Aihara T (2011) Spatiotemporal characteristics of synaptic EPSP summation on the dendritic trees of hippocampal CA1 pyramidal neurons as revealed by laser uncaging stimulation. Cogn Neurodyn 5(4):333–342. doi:10.1007/s11571-011-9158-9
Acknowledgments
We thank Dr. Fujii of Yamagata Univ., Dr. Sakai of Tamagawa Univ., and Drs. Hong and Nishiyama of New York Univ. for valuable discussions and advice on the physiological experiments. This work was supported by the Global COE Program at Tamagawa University and Strategic Research Foundation for Private Universities and by NEXT KAKENHI Grants (Numbers 19200014 and 20500278).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Kamijo, T.C., Hayakawa, H., Fukushima, Y. et al. Input integration around the dendritic branches in hippocampal dentate granule cells. Cogn Neurodyn 8, 267–276 (2014). https://doi.org/10.1007/s11571-014-9280-6
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11571-014-9280-6
Keywords
- Hippocampus
- Dendrite
- Excitatory postsynaptic potentials summation
- Uncaging
- Supralinear amplification