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Defensive behaviors and prosencephalic neurogenesis in pigeons (Columba livia) are affected by environmental enrichment in adulthood

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Abstract

Neurogenesis in the adult brain appears to be phylogenetically conserved across the animal kingdom. In pigeons and other adult non-oscine birds, immature neurons are observed in several prosencephalic areas, suggesting that neurogenesis may participate in the control of different behaviors. The mechanisms controlling neurogenesis and its relevance to defensive behaviors in non-oscine birds remain elusive. Herein, the contribution of the environment to behavior and neurogenesis of pigeons was investigated. Adult pigeons (Columba livia, n = 6/group), housed in standard (SE) or enriched environment (EE) for 42 days, were exposed to an unfamiliar environment (UE) followed by presentation to a novel object (NO). Video recordings of UE+NO tests were analyzed and scored for latency, duration and frequency of angular head movements, peeping, grooming, immobility and locomotion. Twenty-four hours later, pigeons were submitted to the tonic immobility test (TI) and number of trials for TI and TI duration were scored, followed by euthanasia 2 h later. Brains were immunohistochemically processed to reveal doublecortin (DCX), a marker for newborn neurons. Compared to those housed in SE, the pigeons housed in EE responded to a NO with more immobility. In addition, the pigeons housed in EE presented longer TI, more DCX-immunoreactive (DCX-ir) cells in the hippocampus and fewer DCX-ir cells in the lateral striatum than those housed in SE. There was no correlation between the number of DCX-ir cells and the scores of immobility in behavioral tests. Together, these data suggest that enrichment favored behavioral inhibition and neurogenesis in the adult pigeons through different, parallel mechanisms.

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Abbreviations

A:

Arcopallium

AHM:

Angular head movements

BSA:

Bovine serum albumin

CDL:

Area corticoidea dorsolateralis

DAB:

3,3'-Diaminobenzidine

DCX:

Doublecortin

DCX-ir:

Doublecortin immunoreactive

DG:

Dentate gyrus

DL:

Dorsolateral region of Hp

DM:

Dorsomedial region of Hp

E:

Entopallium

EE:

Enriched environment

Ep:

Ependyma

GP:

Globus pallidus

HA:

Hyperpallium apicalle

HD:

Hyperpallium densocellulare

Hp:

Hippocampus

HVC:

Higher vocal center

ief:

Intraependymal DCX-ir fascicles

ll:

Lateral layer of ‘‘V’’-shaped Hp area

LPS:

Lamina pallio-subpallialis

LSt:

Lateral striatum

ml:

Medial layer of ‘‘V’’-shaped Hp area

MSt:

Medial striatum

M:

Mesopallium

N:

Nidopallium

NO:

Novel object

PB:

Phosphate buffer

PBS:

Phosphate buffer saline solution

PBST:

PBS plus 0.25 % triton X-100

RA:

Robustus arcopallii

rmb:

Rostral migratory-like bundle of DCX-ir fibers

SE:

Standard environment

SGZ:

Subgranular layer

St:

Striatum

SVZ:

Subventricular zone

TI:

Immobility test

TPO:

Area temporoparieto-occipitalis

Tr:

Triangular part of ‘‘V’’-shaped Hp area

UE:

Unfamiliar environment test

UE+NO:

Unfamiliar environment test plus novel object test

VP:

Ventral pallidum

V:

Lateral ventricle

VZ1 or 2:

Ventricular proliferative zones 1 or 2

VZ:

Ventricular zone

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Acknowledgments

Michele Vaz Pinheiro (MVP) and Fernando Falkenburger Melleu (FFM) have contributed equally to the development, data collection and analysis of the present experiments and both should be considered the main authors of the present report. The present study was supported by FAPESC (‘‘Young Investigator Grants’’) and Alexander von Humboldt Foundation Research (‘‘Equipment Grants’’) to CLO, as well as by CNPq Research Grants to JMN (proc. 471888/03-6 and 300308/2007-8). FFM and MVP received CAPES MSc fellowships. We wish to thank the excellent and devoted technical help and animal care provided by Mr. Carlos H. Espíndola, Mrs. Joanésia M. J. Rothstein, Mr. Marco A. de Lorenzo, Mr. Emerson V. Fornalski, Mrs. Sandra R. B. de Oliveira, and Mr. Sandro M. de Jesus throughout the experiments.

Ethical statement

All authors contributed to this work and gave their consent to publish this paper. We do not have any commercial conflicts of interest. All financial support came from public agencies without any influence on study design, collection, analysis, and interpretation of data or writing of reports. We guarantee all animal procedures were conducted in compliance with “Guidelines for the Care and Use of Mammals in Neuroscience and Behavioral Research” and the protocols were approved by the Local Ethical Committee in Animal Research. We also guarantee that this work is not under simultaneous consideration in any other journal and will not be published elsewhere in any language without the consent of the copyright owners, that the rights of third parties will not be violated and that the publisher will not be held legally responsible should there be any claims for compensation.

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Authors and Affiliations

  1. Department of Physiological Sciences, CCB, Federal University of Santa Catarina, Florianópolis, SC, 88040-900, Brazil

    F. F. Melleu, M. V. Pinheiro, C. Lino-de-Oliveira & J. Marino-Neto

  2. Institute of Biomedical Engineering, EEL-CTC, Federal University of Santa Catarina, Florianópolis, SC, 88040-900, Brazil

    J. Marino-Neto

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  1. F. F. Melleu
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  2. M. V. Pinheiro
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  3. C. Lino-de-Oliveira
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  4. J. Marino-Neto
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Correspondence to F. F. Melleu.

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Melleu, F.F., Pinheiro, M.V., Lino-de-Oliveira, C. et al. Defensive behaviors and prosencephalic neurogenesis in pigeons (Columba livia) are affected by environmental enrichment in adulthood. Brain Struct Funct 221, 2287–2301 (2016). https://doi.org/10.1007/s00429-015-1043-6

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