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Interneurons, tau and amyloid-β in the piriform cortex in Alzheimer’s disease

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Abstract

Impaired olfaction has been described as an early symptom of Alzheimer’s disease. Neuroanatomical changes underlying this deficit in the olfactory system are largely unknown. Interestingly, neuropathology begins in the transentorhinal cortex and extends to the neighboring limbic system and basal telencephalic structures that mediate olfactory processing, including the anterior olfactory nucleus and olfactory bulb. The human piriform cortex has been described as a crucial area in odor quality coding; disruption of this region mediates early olfactory deficits in Alzheimer’s disease. Most neuropathological investigations have focused on the entorhinal cortex and hippocampus, whereas the piriform cortex has largely been neglected. This work aims to characterize the expression of the neuropathological amyloid-β peptide, tau protein and interneuron population markers (calretinin, parvalbumin and somatostatin) in the piriform cortex of ten Alzheimer-diagnosed (80.4 ± 8.3 years old) and five control (69.6 ± 11.1) cases. Here, we examined the distribution of different interneuronal markers as well as co-localization of interneurons and pathological markers. Results indicated preferential vulnerability of somatostatin- (p = 0.0001 < α = 0.05) and calretinin-positive (p = 0.013 < α = 0.05) cells that colocalized with amyloid-β peptide, while the prevalence of parvalbumin-positive cells was increased (p = 0.045 < α = 0.05) in the Alzheimer’s cases. These data may help to reveal the neural basis of olfactory deficits linked to Alzheimer’s disease as well as to characterize neuronal populations preferentially vulnerable to neuropathology in regions critically involved in early stages of the disease.

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Abbreviations

Aβ:

Amyloid beta

Ac:

Accumbens nucleus

AD:

Alzheimer’s disease

AON:

Anterior olfactory nucleus

API:

Area piriformis insulae

CaBPs:

Calcium binding proteins

Cd:

Caudate nucleus

CSF:

Cerebrospinal fluid

CR:

Calretinin

Ent:

Entorhinal cortex

lo:

Lateral olfactory tract

LV:

Lateral ventricle

NFTs:

Neurofibrillary tangles

OB:

Olfactory bulb

olf:

Olfactory tract

OlfA:

Olfactory area

ox:

Optic chiasm

PAM:

Periamygdaloid cortex

PACI:

Periamygdalar claustrum

Pir:

Piriform cortex

PirF:

Piriform cortex (frontal lobe)

PirT:

Piriform cortex (temporal lobe)

PD:

Parkinson’s disease

Pu:

Putamen

PV:

Parvalbumin

SOM:

Somatostatin

SPs:

Senile plaques

Tu:

Olfactory tubercle

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Acknowledgments

The authors thank the Banco de Tejidos/Fundación para Investigaciones Neurológicas de la Universidad Complutense de Madrid and the Banc de Teixits Neurològics de la Universitat de Barcelona-Hospital Clínic for kindly providing the human tissue. The authors acknowledge Lucia Medina Prado and the precious help in the laboratory. The assistance of International Science Editing in revising the English grammar is also acknowledged. Authors are indebted to Dr. Mimi Halpern for reading and commenting on the manuscript. This work constitutes part of the Doctoral Thesis of Daniel Saiz-Sanchez. This study was supported by the Spanish Ministry of Economy and Competitiveness (BFU2010-15729).

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Correspondence to Alino Martinez-Marcos.

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Saiz-Sanchez, D., De la Rosa-Prieto, C., Ubeda-Banon, I. et al. Interneurons, tau and amyloid-β in the piriform cortex in Alzheimer’s disease. Brain Struct Funct 220, 2011–2025 (2015). https://doi.org/10.1007/s00429-014-0771-3

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  • DOI: https://doi.org/10.1007/s00429-014-0771-3

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