Differential inhibition onto developing and mature granule cells generates high-frequency filters with variable gain

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Abstract

Adult hippocampal neurogenesis provides the dentate gyrus with heterogeneous populations of granule cells (GC) originated at different times. The contribution of these cells to information encoding is under current investigation. Here we show that incoming spike trains activate different populations of GC determined by the stimulation frequency and GC age. Immature GC respond to a wider range of stimulus frequencies, whereas mature GC are less responsive at high frequencies. This difference is dictated by feed forward inhibition, which restricts mature GC activation. Yet, the stronger inhibition of mature GC results in a higher temporal fidelity compared to that of immature GC. Thus, hippocampal inputs activate two populations of neurons with variable frequency filters: immature cells, with wide‐range responses, that are reliable transmitters of the incoming frequency, and mature neurons, with narrow frequency response, that are precise at informing the beginning of the stimulus, but with a sparse activity.

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María Belén Pardi

Instituto de Investigación en Biomedicina de Buenos Aires - CONICET - Partner Institute of the Max Planck Society, Buenos Aires, Argentina

Competing interests
The authors declare that no competing interests exist.
Mora Belén Ogando

Instituto de Investigación en Biomedicina de Buenos Aires - CONICET - Partner Institute of the Max Planck Society, Buenos Aires, Argentina

Competing interests
The authors declare that no competing interests exist.
Alejandro F Schinder

Laboratory of Neuronal Plasticity, Leloir Institute -CONICET, Buenos Aires, Argentina

Competing interests
The authors declare that no competing interests exist.
Antonia Marin-Burgin

Instituto de Investigación en Biomedicina de Buenos Aires - CONICET - Partner Institute of the Max Planck Society, Buenos Aires, Argentina

For correspondence
aburgin@ibioba-mpsp-conicet.gov.ar

Competing interests
The authors declare that no competing interests exist.

Ethics

Animal experimentation: Experimental protocols were approved by the Institutional Animal Care and Use Committee of the Fundación Instituto Leloir (Protocols Number 2009 08 37 and 64/2015, IACUC, Leloir Institute Foundation) according to the Principles for Biomedical Research involving animals of the Council for International Organizations for Medical Sciences and provisions stated in the Guide for the Care and Use of Laboratory Animals.

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This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.