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Distribution of peptidergic populations in the human dentate gyrus (Somatostatin [SOM-28, SOM-12] and Neuropeptide Y [NPY]) during postnatal development

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Abstract

The postnatal development of the human hippocampal formation establishes the time and place at which we start autobiographical memories. However, data concerning the maturation of the neurochemical phenotypes characteristic of interneurons in the human hippocampus are scarce. We have studied the perinatal and postnatal changes of the dentate gyrus (DG) interneuron populations at three rostrocaudal levels. Immunohistochemically identified neurons and fibers for somatostatin (SOM-12 and SOM-28) and neuropeptide Y (NPY) and the co-localization of SOM-28 and NPY were analyzed. In total, 13 cases were investigated from late pregnancy (1 case), perinatal period (6 cases), first year (1 case), early infancy (3 cases), and late infancy (2 cases). Overall, the pattern of distribution of these peptides in the DG was similar to that of the adult. The distribution of cells was charted, and the cell density (number of positive cells/mm2) was calculated. The highest density corresponded to the polymorphic cell layer and was higher at pre- and perinatal periods. At increasing ages, neuron density modifications revealed a decrease from 5 postnatal months onward. In contrast, by late infancy, two immunoreactive bands for SOM-28 and NPY in the molecular layer were much better defined. Double-immunohistochemistry showed that NPY-positive neurons co-localized with SOM-28, whereas some fibers contained only one or other of the neuropeptides. Thus, this peptidergic population, presumably inhibitory, probably has a role in DG maturation and its subsequent functional activity in memory processing.

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Abbreviations

CA1:

Ammonic hippocampal field 1

CA2:

Ammonic hippocampal field 2

CA3:

Ammonic hippocampal field 3

DG:

Dentate gyrus

GW:

Gestational weeks

HF:

Hippocampal formation

LTP:

Long term potentiation

NPY:

Neuropeptide Y

SOM-12:

Somatostatin (1–12)

SOM-28:

Somatostatin 28

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Acknowledgments

This research was conducted on samples from the Andalusian Public Health System Biobank (ISCIII-Red de Biobancos RD09/0076/00085). The authors are grateful to Drs. Tuñón and García-Bragado from the Navarra Department of Health, Dr. Rábano from Alcorcón Foundation Hospital, and the Pathology Service of the University Hospital in Albacete (Dr. Atiénzar) for the provision of human infant tissue and to Dr. Tramu (Université de Bordeaux I, France) for kindly providing NPY and SOM-12 antibodies. The authors also thank the technical team of the Human Neuroanatomy Laboratory of the University of Castilla-La Mancha and the technicians of the Virgen del Rocío Hospital for their crucial contribution to the preparation of the human brain tissue. Special thanks are extended to the donors and their families.

Conflict of interest

The authors declare that they have no conflicts of interest.

Author information

Authors and Affiliations

  1. Human Neuroanatomy Laboratory, Faculty of Medicine, University of Castilla-La Mancha and CRIB (Centro Regional de Investigaciones Biomédicas), Avenida de Almansa 14, 02006, Albacete, Spain

    S. Cebada-Sánchez, R. Insausti, J. González-Fuentes, M. M. Arroyo-Jiménez, J. Martínez-Ruiz, G. Lozano & P. Marcos

  2. Cellular Neurobiology and Molecular Chemistry, Department of Health Sciences, University of Castilla-La Mancha, Schools of Medicine and Pharmacy, Albacete, Spain, Avenida de Almansa 14, 02006, Albacete, Spain

    J. González-Fuentes, M. M. Arroyo-Jiménez & P. Marcos

  3. Servicio de Anatomía Patológica, Virgen del Rocío Hospital, Avenida Manuel Siurot s/n, 41013, Sevilla, Spain

    E. Rivas-Infante

  4. Kavli Institute for Systems Neuroscience and Centre for the Neural Computation, Norwegian University of Science and Technology (NTNU), 7489, Trondheim, Norway

    M. J. Lagartos

Authors
  1. S. Cebada-Sánchez
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  2. R. Insausti
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  3. J. González-Fuentes
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  4. M. M. Arroyo-Jiménez
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  5. E. Rivas-Infante
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  6. M. J. Lagartos
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  7. J. Martínez-Ruiz
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  8. G. Lozano
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  9. P. Marcos
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Corresponding author

Correspondence to P. Marcos.

Additional information

This study was supported by the NINDS (grant 2R01NS016980) and the Junta de Comunidades de Castilla-La Mancha, Spain (grants PC108-0113 and PI-2006/14).

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Cebada-Sánchez, S., Insausti, R., González-Fuentes, J. et al. Distribution of peptidergic populations in the human dentate gyrus (Somatostatin [SOM-28, SOM-12] and Neuropeptide Y [NPY]) during postnatal development. Cell Tissue Res 358, 25–41 (2014). https://doi.org/10.1007/s00441-014-1929-2

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