Skip to main content
Top
Published in: Brain Structure and Function 7/2018

01-09-2018 | Original Article

First evidence of neuronal connections between specific parts of the periaqueductal gray (PAG) and the rest of the brain in sheep: placing the sheep PAG in the circuit of emotion

Authors: Ophélie Menant, Marie-Caroline Prima, Mélody Morisse, Fabien Cornilleau, Christian Moussu, Adeline Gautier, Hélène Blanchon, Maryse Meurisse, Philippe Delagrange, Yves Tillet, Elodie Chaillou

Published in: Brain Structure and Function | Issue 7/2018

Login to get access

Abstract

The periaqueductal gray (PAG) is a mesencephalic brain structure organised in subdivisions with specific anatomical connections with the rest of the brain. These connections support the different PAG functions and especially its role in emotion. Mainly described in territorial and predatory mammals, examination of the PAG connections suggests an opposite role of the ventral and the dorsal/lateral PAG in passive and active coping style, respectively. In mammals, the organisation of PAG connections may reflect the coping style of each species. Based on this hypothesis, we investigated the anatomical connections of the PAG in sheep, a gregarious and prey species. Since emotional responses expressed by sheep are typical of active coping style, we focused our interest on the dorsal and lateral parts of the PAG. After injection of fluorogold and fluororuby, the most numerous connections occurred with the anterior cingulate gyrus, the anterior hypothalamic region, the ventromedial hypothalamic nucleus and the PAG itself. Our observations show that the sheep PAG belongs to the neuronal circuit of emotion and has specific parts as in other mammals. However, unlike other mammals, we observed very few connections between PAG and either the thalamic or the amygdalar nuclei. Interestingly, when comparing across species, the PAG connections of sheep were noticeably more like those previously described in other social species, rabbits and squirrel monkeys, than those in territorial species, rats or cats.
Literature
go back to reference An X, Bandler R, Öngür D, Price JL (1998) Prefrontal cortical projections to longitudinal columns in the midbrain periaqueductal gray in macaque monkeys. J Comp Neurol 401:455–479. (10.1002/(SICI)1096-9861(19981130)401:4<455::AID-CNE3>3.0.CO;2-6)CrossRef An X, Bandler R, Öngür D, Price JL (1998) Prefrontal cortical projections to longitudinal columns in the midbrain periaqueductal gray in macaque monkeys. J Comp Neurol 401:455–479. (10.1002/(SICI)1096-9861(19981130)401:4<455::AID-CNE3>3.0.CO;2-6)CrossRef
go back to reference Borszcz GS (2006) Contribution of the ventromedial hypothalamus to generation of the affective dimension of pain. Pain 123:155–168CrossRef Borszcz GS (2006) Contribution of the ventromedial hypothalamus to generation of the affective dimension of pain. Pain 123:155–168CrossRef
go back to reference Bouissou M-F, Vandenheede M (1995) Fear reactions of domestic sheep confronted with either a human or a human-like model. Behav Processes 34:81–92CrossRef Bouissou M-F, Vandenheede M (1995) Fear reactions of domestic sheep confronted with either a human or a human-like model. Behav Processes 34:81–92CrossRef
go back to reference Calas A (2010) Peut-on prouver la spécificité d’un marquage immunohistochimique ? Rev Fr Histotechnol 23:73–80 Calas A (2010) Peut-on prouver la spécificité d’un marquage immunohistochimique ? Rev Fr Histotechnol 23:73–80
go back to reference Carrive P, Paxinos G (1994) The supraocculomotor cap: a region revealed by NADPH diaphorase histochemistry. NeuroReport 5:2257–2260CrossRef Carrive P, Paxinos G (1994) The supraocculomotor cap: a region revealed by NADPH diaphorase histochemistry. NeuroReport 5:2257–2260CrossRef
go back to reference Cook CJ (1997) Oxytocin and prolactin suppress cortisol responses to acute stress in both lactating and non-lactating sheep. J Diary Res 64:327–339CrossRef Cook CJ (1997) Oxytocin and prolactin suppress cortisol responses to acute stress in both lactating and non-lactating sheep. J Diary Res 64:327–339CrossRef
go back to reference Cook CJ (2001) Measuring of extracellular cortisol and corticotropin-releasing hormone in the amygdala using immunosensor coupled microdialysis. J Neurosci Methods 110:95–101CrossRef Cook CJ (2001) Measuring of extracellular cortisol and corticotropin-releasing hormone in the amygdala using immunosensor coupled microdialysis. J Neurosci Methods 110:95–101CrossRef
go back to reference Depaulis A, Keay KA, Bandler R (1994) Quiescence and hyporeactivity evoked by activation of cell bodies in the ventrolateral midbrain periaqueductal gray of the rat. Exp Brain Res 99:75–83CrossRef Depaulis A, Keay KA, Bandler R (1994) Quiescence and hyporeactivity evoked by activation of cell bodies in the ventrolateral midbrain periaqueductal gray of the rat. Exp Brain Res 99:75–83CrossRef
go back to reference Dwyer CM, McLean KA, Deans LA et al (1998) Vocalisations between mother and young in sheep: effects of breed and maternal experience. Appl Anim Behav Sci 58:105–119CrossRef Dwyer CM, McLean KA, Deans LA et al (1998) Vocalisations between mother and young in sheep: effects of breed and maternal experience. Appl Anim Behav Sci 58:105–119CrossRef
go back to reference Floyd NS, Price JL, Ferry AT, et al (2000) Orbitomedial prefrontal cortical projections to distinct longitudinal columns of the periaqueductal gray in the rat. J Comp Neurol 422:556–578. (10.1002/1096-9861(20000710)422:4<556::AID-CNE6>3.0.CO;2-U)CrossRef Floyd NS, Price JL, Ferry AT, et al (2000) Orbitomedial prefrontal cortical projections to distinct longitudinal columns of the periaqueductal gray in the rat. J Comp Neurol 422:556–578. (10.1002/1096-9861(20000710)422:4<556::AID-CNE6>3.0.CO;2-U)CrossRef
go back to reference Giles LR, Kilgour RJ (1999) Coping style in farm animals: Behavioural trait or production index. Recent Adv Anim Nutr Aust 12:187–192 Giles LR, Kilgour RJ (1999) Coping style in farm animals: Behavioural trait or production index. Recent Adv Anim Nutr Aust 12:187–192
go back to reference Herman JP, McKlveen JM, Ghosal S et al (2016) Regulation of the Hypothalamic-Pituitary-Adrenocortical Stress Response. In: Terjung R (ed) Comprehensive Physiology. Wiley, Hoboken, pp 603–621CrossRef Herman JP, McKlveen JM, Ghosal S et al (2016) Regulation of the Hypothalamic-Pituitary-Adrenocortical Stress Response. In: Terjung R (ed) Comprehensive Physiology. Wiley, Hoboken, pp 603–621CrossRef
go back to reference Keay KA, Bandler R (2015) Periaqueductal gray. The rat nervous system. Elsevier, New York, pp 207–221CrossRef Keay KA, Bandler R (2015) Periaqueductal gray. The rat nervous system. Elsevier, New York, pp 207–221CrossRef
go back to reference Kim EJ, Horovitz O, Pellman BA et al (2013) Dorsal periaqueductal gray-amygdala pathway conveys both innate and learned fear responses in rats. Proc Natl Acad Sci 110:14795–14800CrossRef Kim EJ, Horovitz O, Pellman BA et al (2013) Dorsal periaqueductal gray-amygdala pathway conveys both innate and learned fear responses in rats. Proc Natl Acad Sci 110:14795–14800CrossRef
go back to reference Krout KE, Loewy AD (2000) Periaqueductal gray matter projections to midline and intralaminar thalamic nuclei of the rat. J Comp Neurol 424:111–141CrossRef Krout KE, Loewy AD (2000) Periaqueductal gray matter projections to midline and intralaminar thalamic nuclei of the rat. J Comp Neurol 424:111–141CrossRef
go back to reference LeDoux JE (2000) Emotion circuits in the brain. Annu Rev Neurosci 23:155–184CrossRef LeDoux JE (2000) Emotion circuits in the brain. Annu Rev Neurosci 23:155–184CrossRef
go back to reference Levy F, Richard P, Meurisse M, Ravel N (1997) Scopolamine impairs the ability of parturient ewes to learn to recognise their lambs. Psychopharmacology 129:85–90CrossRef Levy F, Richard P, Meurisse M, Ravel N (1997) Scopolamine impairs the ability of parturient ewes to learn to recognise their lambs. Psychopharmacology 129:85–90CrossRef
go back to reference Matthews SG, Parrott RF, Sirinathsinghji DJS (1993) Isolation- and dehydration-induced changes in neuropeptide gene expression in the sheep hypothalamus. J Mol Endocrinol 11:181–189CrossRef Matthews SG, Parrott RF, Sirinathsinghji DJS (1993) Isolation- and dehydration-induced changes in neuropeptide gene expression in the sheep hypothalamus. J Mol Endocrinol 11:181–189CrossRef
go back to reference Menant O, Destrez A, Deiss V et al (2016b) Régulation des émotions chez l’animal d’élevage: focus sur les acteurs neurobiologiques. INRA Prod Anim 29:241–254 Menant O, Destrez A, Deiss V et al (2016b) Régulation des émotions chez l’animal d’élevage: focus sur les acteurs neurobiologiques. INRA Prod Anim 29:241–254
go back to reference Niezgoda J, Bobek S, Wronska-Fortuna D, Wierzchos E (1993) Response of Sympatho-Adrenal Axis and Adrenal Cortex to Short-Term Restraint Stress in Sheep. J Vet Med Ser A 40:631–638CrossRef Niezgoda J, Bobek S, Wronska-Fortuna D, Wierzchos E (1993) Response of Sympatho-Adrenal Axis and Adrenal Cortex to Short-Term Restraint Stress in Sheep. J Vet Med Ser A 40:631–638CrossRef
go back to reference Paxinos G, Franklin KB (2001) The mouse brain in stereotaxic coordinates, 2nd edn. Academic press, San Diego Paxinos G, Franklin KB (2001) The mouse brain in stereotaxic coordinates, 2nd edn. Academic press, San Diego
go back to reference Price JL, Amaral DG (1981) An autoradiographic study of the projections of the central nucleus of the monkey amygdala. J Neurosci 1:1242–1259CrossRef Price JL, Amaral DG (1981) An autoradiographic study of the projections of the central nucleus of the monkey amygdala. J Neurosci 1:1242–1259CrossRef
go back to reference Room P, Russchen FT, Groenewegen HJ, Lohman AH (1985) Efferent connections of the prelimbic (area 32) and the infralimbic (area 25) cortices: an anterograde tracing study in the cat. J Comp Neurol 242:40–55CrossRef Room P, Russchen FT, Groenewegen HJ, Lohman AH (1985) Efferent connections of the prelimbic (area 32) and the infralimbic (area 25) cortices: an anterograde tracing study in the cat. J Comp Neurol 242:40–55CrossRef
go back to reference Rose JE (1942) A cytoarchitectural study of the sheep cortex. J Comp Neurol 76:1–55CrossRef Rose JE (1942) A cytoarchitectural study of the sheep cortex. J Comp Neurol 76:1–55CrossRef
go back to reference Tillet Y (1987) Immunocytochemical localization of serotonin-containing neurons in the myelencephalon, brainstem and diencephalon of the sheep. Neuroscience 23:501–527CrossRef Tillet Y (1987) Immunocytochemical localization of serotonin-containing neurons in the myelencephalon, brainstem and diencephalon of the sheep. Neuroscience 23:501–527CrossRef
go back to reference Vandenheede M, Bouissou M-F, Picard M (1998) Interpretation of behavioural reactions of sheep towards fear-eliciting situations. Appl Anim Behav Sci 58:293–310CrossRef Vandenheede M, Bouissou M-F, Picard M (1998) Interpretation of behavioural reactions of sheep towards fear-eliciting situations. Appl Anim Behav Sci 58:293–310CrossRef
go back to reference Wilent WB, Oh MY, Buetefisch CM et al (2010) Induction of panic attack by stimulation of the ventromedial hypothalamus: Case report. J Neurosurg 112:1295–1298CrossRef Wilent WB, Oh MY, Buetefisch CM et al (2010) Induction of panic attack by stimulation of the ventromedial hypothalamus: Case report. J Neurosurg 112:1295–1298CrossRef
go back to reference Yayou K, Nakamura M, Ito S (2009) Effects of AVP V1a and CRH receptor antagonist on psychological stress responses to frustrating condition in sheep. J Vet Med Sci 71:431–439CrossRef Yayou K, Nakamura M, Ito S (2009) Effects of AVP V1a and CRH receptor antagonist on psychological stress responses to frustrating condition in sheep. J Vet Med Sci 71:431–439CrossRef
Metadata
Title
First evidence of neuronal connections between specific parts of the periaqueductal gray (PAG) and the rest of the brain in sheep: placing the sheep PAG in the circuit of emotion
Authors
Ophélie Menant
Marie-Caroline Prima
Mélody Morisse
Fabien Cornilleau
Christian Moussu
Adeline Gautier
Hélène Blanchon
Maryse Meurisse
Philippe Delagrange
Yves Tillet
Elodie Chaillou
Publication date
01-09-2018
Publisher
Springer Berlin Heidelberg
Published in
Brain Structure and Function / Issue 7/2018
Print ISSN: 1863-2653
Electronic ISSN: 1863-2661
DOI
https://doi.org/10.1007/s00429-018-1689-y

Other articles of this Issue 7/2018

Brain Structure and Function 7/2018 Go to the issue