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The mesencephalic GCt–ICo complex and tonic immobility in pigeons (Columba livia): a c-Fos study

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Abstract

Tonic immobility (TI) is a response to a predator attack, or other inescapable danger, characterized by immobility, analgesia and unresponsiveness to external stimuli. In mammals, the periaqueductal gray (PAG) and deep tectal regions control the expression of TI as well as other defensive behaviors. In birds, little is known about the mesencephalic circuitry involved in the control of TI. Here, adult pigeons (both sex, n = 4/group), randomly assigned to non-handled, handled or TI groups, were killed 90 min after manipulations and the brains processed for detection of c-Fos immunoreactive cells (c-Fos-ir, marker for neural activity) in the mesencephalic central gray (GCt) and the adjacent nucleus intercollicularis (ICo). The NADPH-diaphorase staining delineated the boundaries of the sub nuclei in the ICo–GCt complex. Compared to non-handled, TI (but not handling) induced c-Fos-ir in NADPH-diaphorase-rich and -poor regions. After TI, the number of c-Fos-ir increased in the caudal and intermediate areas of the ICo (but not in the GCt), throughout the rostrocaudal axis of the dorsal stratum griseum periventriculare (SGPd) of the optic tectum and in the n. mesencephalicus lateralis pars dorsalis (MLd), which is part of the ascending auditory pathway. These data suggest that inescapable threatening stimuli such as TI may recruit neurons in discrete areas of ICo–GCt complex, deep tectal layer and in ascending auditory circuits that may control the expression of defensive behaviors in pigeons. Additionally, data indicate that the contiguous deep tectal SCPd (but not GCt) in birds may be functionally comparable to the mammalian dorsal PAG.

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Abbreviations

Aq:

Cerebral aqueduct

EW:

Edinger–Westphal nucleus

FLM:

Medial longitudinal fasciculus

GCt:

Griseum centralis

ICo:

Intercollicular nucleus

ICo-l:

Lateral intercollicular nucleus

ICo-m:

Medial intercollicular nucleus

Laq:

Lateral expansion of the aqueduct

MLd:

Nucleus mesencephalicus lateralis, pars dorsalis

NADPHd:

Reduced nicotinamide adenine dinucleotide phosphate-diaphorase

nIII:

Nucleus of the oculomotor nerve

SGPd:

Dorsal part of the stratum griseum periventriculare

SGPv:

Ventral part of the stratum griseum periventriculare

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Acknowledgments

The present study was supported by an Alexander von Humboldt Foundation Research (‘‘Equipment Grant’’) to CLO as well as by CNPq Research Grants to JMN (proc. 471888/03-6 and 441577/2014-8). FFM received CAPES PhD fellowships. We wish to thank the excellent and devoted technical help and animal care provided by Mr. Eduardo Henrique Gonçalves, Mrs. Joanésia M. J. Rothstein, Mr. Marco A. de Lorenzo, and Mr. Emerson V. Fornalski throughout the experiments.

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

    Fernando Falkenburger Melleu, 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. Fernando Falkenburger Melleu
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  2. C. Lino-de-Oliveira
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Correspondence to Fernando Falkenburger Melleu.

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Melleu, F.F., Lino-de-Oliveira, C. & Marino-Neto, J. The mesencephalic GCt–ICo complex and tonic immobility in pigeons (Columba livia): a c-Fos study. Brain Struct Funct 222, 1253–1265 (2017). https://doi.org/10.1007/s00429-016-1275-0

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