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

First evidence of neuronal connections between specific parts of the periaqueductal gray (PAG)... 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. http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Brain Structure and Function Springer Journals

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

20 pages
Read Article

Loading next page...
 
/lp/springer_journal/first-evidence-of-neuronal-connections-between-specific-parts-of-the-0OhI5PF7Ss
Publisher
Springer Berlin Heidelberg
Copyright
Copyright © 2018 by Springer-Verlag GmbH Germany, part of Springer Nature
Subject
Biomedicine; Neurosciences; Cell Biology; Neurology
ISSN
1863-2653
eISSN
1863-2661
D.O.I.
10.1007/s00429-018-1689-y
Publisher site
See Article on Publisher Site

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.

Journal

Brain Structure and Function – Springer Journals

Published: Jun 4, 2018

References

  • Prefrontal cortical projections to longitudinal columns in the midbrain periaqueductal gray in macaque monkeys
    An, X; Bandler, R; Öngür, D; Price, JL
  • The efferent projections of the rat lateral habenular nucleus revealed by the PHA-L anterograde tracing method
    Araki, M; McGeer, PL; Kimura, H
  • Columnar organization in the midbrain periaqueductal gray: modules for emotional expression ?
    Bandler, R; Shipley, MT
  • Ventral tegmental area subcircuits process rewarding and aversive experiences
    Bariselli, S; Glangetas, C; Tzanoulinou, S; Bellone, C
  • Afferent projections to the preoptic area and hypothalamic regions in the rat brain
    Berk, ML; Finkelstein, JA
  • Direct projections from the periaqueductal gray to the pontine micturition center (M-region). An anterograde and retrograde tracing study in the cat
    Blok, BFM; Holstege, G
  • Contribution of the ventromedial hypothalamus to generation of the affective dimension of pain
    Borszcz, GS
  • Fear reactions of domestic sheep confronted with either a human or a human-like model
    Bouissou, M-F; Vandenheede, M
  • NeuroNames 2002
    Bowden, DM; Dubach, MF
  • Increased BDNF and trk-B mRNA expression in cortical and limbic regions following formation of a social recognition memory
    Broad, KD; Mimmack, ML; Keverne, EB; Kendrick, KM
  • Peut-on prouver la spécificité d’un marquage immunohistochimique ?
    Calas, A
  • The periaqueductal gray and defensive behavior: Functional representation and neuronal organization
    Carrive, P
  • The supraocculomotor cap: a region revealed by NADPH diaphorase histochemistry
    Carrive, P; Paxinos, G
  • Dietary shift of an invasive predator: rats, seabirds and sea turtles
    Caut, S; Angulo, E; Courchamp, F
  • Comparisons of terminal densities of cardiovascular function-related projections from the amygdala subnuclei
    Chiou, R-J; Kuo, C-C; Yen, C-T
  • Effect of short-term and prolonged stress on the biosynthesis of gonadotropin-releasing hormone (GnRH) and GnRH receptor (GnRHR) in the hypothalamus and GnRHR in the pituitary of ewes during various physiological states
    Ciechanowska, M; Łapot, M; Antkowiak, B
  • Oxytocin and prolactin suppress cortisol responses to acute stress in both lactating and non-lactating sheep
    Cook, CJ
  • Measuring of extracellular cortisol and corticotropin-releasing hormone in the amygdala using immunosensor coupled microdialysis
    Cook, CJ
  • Stress induces CRF release in the paraventricular nucleus, and both CRF and GABA release in the amygdala
    Cook, CJ
  • Face pictures reduce behavioural, autonomic, endocrine and neural indices of stress and fear in sheep
    Costa, AP; Leigh, AE; Man, M-S; Kendrick, KM
  • Quiescence and hyporeactivity evoked by activation of cell bodies in the ventrolateral midbrain periaqueductal gray of the rat
    Depaulis, A; Keay, KA; Bandler, R
  • Long-term exposure to unpredictable and uncontrollable aversive events alters fearfulness in sheep
    Destrez, A; Deiss, V; Leterrier, C
  • Projections from bed nuclei of the stria terminalis, posterior division: Implications for cerebral hemisphere regulation of defensive and reproductive behaviors
    Dong, H-W; Swanson, LW
  • Projections from bed nuclei of the stria terminalis, dorsomedial nucleus: Implications for cerebral hemisphere integration of neuroendocrine, autonomic, and drinking responses
    Dong, H-W; Swanson, LW
  • Projections from bed nuclei of the stria terminalis, anteromedial area: Cerebral hemisphere integration of neuroendocrine, autonomic, and behavioral aspects of energy balance
    Dong, H-W; Swanson, LW
  • Afferents of vocalization-controlling periaqueductal regions in the squirrel monkey
    Dujardin, E; Jürgens, U
  • Vocalisations between mother and young in sheep: effects of breed and maternal experience
    Dwyer, CM; McLean, KA; Deans, LA
  • Emotional processing in anterior cingulate and medial prefrontal cortex
    Etkin, A; Egner, T; Kalisch, R
  • Orbitomedial prefrontal cortical projections to distinct longitudinal columns of the periaqueductal gray in the rat
    Floyd, NS; Price, JL; Ferry, AT
  • Contributions of the insula to cognition and emotion
    Gasquoine, PG
  • Role of experience in the neuroendocrine control of ewes’ sexual behavior
    Gelez, H; Archer, E; Chesneau, D
  • Coping style in farm animals: Behavioural trait or production index
    Giles, LR; Kilgour, RJ
  • Multiple exposures to familiar conspecific withdrawal is a novel robust stress paradigm in ewes
    Guesdon, V; Ligout, S; Delagrange, P
  • Behavioral and endocrine evaluation of the stressfulness of single-pen housing compared to group-housing and social isolation conditions
    Guesdon, V; Meurisse, M; Chesneau, D
  • The neurobiology of abnormal manifestations of aggression–A review of hypothalamic mechanisms in cats, rodents, and humans
    Haller, J
  • Comprehensive Physiology
    Herman, JP; McKlveen, JM; Ghosal, S
  • Cortically projecting cells in the periaqueductal gray matter of the rat. A retrograde fluorescent tracer study
    Herrero, MT; Insausti, R; Conzalo, LM
  • The habenula: from stress evasion to value-based decision-making
    Hikosaka, O
  • Amygdaloid projections to the mesencephalon, pons and medulla oblongata in the cat
    Hopkins, DA; Holstege, G
  • The Paraventricular thalamic nucleus: Subcortical connections and innervation by serotonin, orexin, and corticotropin-releasing hormone in macaque monkeys
    Hsu, DT; Price, JL
  • Local connections between the columns of the periaqueductal gray matter: a case for intrinsic neuromodulation
    Jansen, AS; Farkas, E; Mac Sams, J; Loewy, AD
  • Parallel circuits mediating distinct emotional coping reactions to different types of stress
    Keay, KA; Bandler, R
  • Periaqueductal gray. The rat nervous system
    Keay, KA; Bandler, R
  • Cortical and medial amygdala are both involved in the formation of olfactory offspring memory in sheep
    Keller, M; Perrin, G; Meurisse, M
  • Dorsal periaqueductal gray-amygdala pathway conveys both innate and learned fear responses in rats
    Kim, EJ; Horovitz, O; Pellman, BA
  • GABAergic projection from the ventral tegmental area and substantia nigra to the periaqueductal gray region and the dorsal raphe nucleus
    Kirouac, GJ; Li, S; Mabrouk, G
  • Two parts of the nucleus prepositus hypoglossi project to two different subdivisions of the dorsolateral periaqueductal gray in cat
    Klop, EM; Mouton, LJ; Ehling, T; Holstege, G
  • Periaqueductal gray matter projections to midline and intralaminar thalamic nuclei of the rat
    Krout, KE; Loewy, AD
  • Two vocalization-related subregions in the midbrain periaqueductal gray of the guinea pig
    Kyuhou, S; Gemba, H
  • Emotion circuits in the brain
    LeDoux, JE
  • Scopolamine impairs the ability of parturient ewes to learn to recognise their lambs
    Levy, F; Richard, P; Meurisse, M; Ravel, N
  • Afferents to the rostral olfactory bulb in sheep with special emphasis on the cholinergic, noradrenergic and serotonergic connections
    Levy, F; Meurisse, M; Ferreira, G
  • Surface-based cortical parcellation of the sheep brain. Figshare
    Love, S; Auge, M; Siwiaszczyk, M
  • The course of paraventricular hypothalamic efferents to autonomic structures in medulla and spinal cord
    Luiten, PGM; Horst, GJ; Karst, H; Steffens, B
  • Afferents to the periaqueductal gray in the rat. A horseradish peroxidase study
    Marchand, JE; Hagino, N
  • Isolation- and dehydration-induced changes in neuropeptide gene expression in the sheep hypothalamus
    Matthews, SG; Parrott, RF; Sirinathsinghji, DJS
  • Afferent projections to the periaqueductal gray in the rabbit
    Meller, ST; Dennis, BJ
  • The benefits of magnetic resonance imaging methods to extend the knowledge of the anatomical organisation of the periaqueductal gray in mammals
    Menant, O; Andersson, F; Zelena, D; Chaillou, E
  • Régulation des émotions chez l’animal d’élevage: focus sur les acteurs neurobiologiques
    Menant, O; Destrez, A; Deiss, V
  • Response of Sympatho-Adrenal Axis and Adrenal Cortex to Short-Term Restraint Stress in Sheep
    Niezgoda, J; Bobek, S; Wronska-Fortuna, D; Wierzchos, E
  • Afferents to the central nucleus of the amygdala and functional subdivisions of the periaqueductal gray: neuroanatomical substrates for affective behavior
    Paredes, J; Winters, RW; Schneiderman, N; McCabe, PM
  • The mouse brain in stereotaxic coordinates
    Paxinos, G; Franklin, KB
  • An autoradiographic study of the projections of the central nucleus of the monkey amygdala
    Price, JL; Amaral, DG
  • Neural connectivity in the mediobasal hypothalamus of the sheep brain
    Qi, Y; Iqbal, J; Oldfield, BJ; Clarke, IJ
  • An analysis of von Economo neurons in the cerebral cortex of cetaceans, artiodactyls, and perissodactyls
    Raghanti, MA; Spurlock, LB; Robert Treichler, F
  • Demonstration of a reciprocal connection between the periaqueductal gray matter and the reticular nucleus of the thalamus
    Rinvik, E; Wiberg, M
  • Efferent connections of the hypothalamic “aggression area” in the rat
    Roeling, TAP; Veening, JG; Kruk, MR
  • Efferent connections of the prelimbic (area 32) and the infralimbic (area 25) cortices: an anterograde tracing study in the cat
    Room, P; Russchen, FT; Groenewegen, HJ; Lohman, AH
  • A cytoarchitectural study of the sheep cortex
    Rose, JE
  • Fiji: an open-source platform for biological-image analysis
    Schindelin, J; Arganda-Carreras, I; Frise, E
  • On the use of retrograde tracers for identification of axon collaterals with multiple fluorescent retrograde tracers
    Schofield, BR; Schofield, RM; Sorensen, KA; Motts, SD
  • Neuronal inputs from the hypothalamus and brain stem to the medial preoptic area of the ram: Neurochemical correlates and comparison to the ewe
    Scott, CJ; Clarke, IJ; Tilbrook, AJ
  • Motor organization of positive and negative emotional vocalization in the cat midbrain periaqueductal gray
    Subramanian, HH; Arun, M; Silburn, PA; Holstege, G
  • Immunocytochemical localization of serotonin-containing neurons in the myelencephalon, brainstem and diencephalon of the sheep
    Tillet, Y
  • Neuronal projections to the lateral retrochiasmatic area of sheep with special reference to catecholaminergic afferents: immunohistochemical and retrograde tract-tracing studies
    Tillet, Y; Batailler, M; Thiéry, J-C; Thibault, J
  • Relevance of dorsomedial hypothalamus, dorsomedial division of the ventromedial hypothalamus and the dorsal periaqueductal gray matter in the organization of freezing or oriented and non-oriented escape emotional behaviors
    Ullah, F; Anjos-Garcia, T; Santos, IR
  • Comparative Connectomics
    Heuvel, MP; Bullmore, ET; Sporns, O
  • Interpretation of behavioural reactions of sheep towards fear-eliciting situations
    Vandenheede, M; Bouissou, M-F; Picard, M
  • Induction of panic attack by stimulation of the ventromedial hypothalamus: Case report
    Wilent, WB; Oh, MY; Buetefisch, CM
  • Effects of AVP V1a and CRH receptor antagonist on psychological stress responses to frustrating condition in sheep
    Yayou, K; Nakamura, M; Ito, S
  • Flight and immobility evoked by excitatory amino acid microinjection within distinct parts of the subtentorial midbrain periaqueductal gray of the cat
    Zhang, SP; Bandler, R; Carrive, P

You’re reading a free preview. Subscribe to read the entire article.

Try 2 weeks free now

DeepDyve is your
personal research library

It’s your single place to instantly
discover and read the research
that matters to you.

Enjoy affordable access to
over 18 million articles from more than
15,000 peer-reviewed journals.

All for just $49/month

Explore the DeepDyve Library

or browse the journals available

Search

Query the DeepDyve database, plus search all of PubMed and Google Scholar seamlessly

Organize

Save any article or search result from DeepDyve, PubMed, and Google Scholar... all in one place.

Access

Get unlimited, online access to over 18 million full-text articles from more than 15,000 scientific journals.

Your journals are on DeepDyve

Read from thousands of the leading scholarly journals from SpringerNature, Elsevier, Wiley-Blackwell, Oxford University Press and more.

All the latest content is available, no embargo periods.

See the journals in your area

DeepDyve

Freelancer

DeepDyve

Pro

Price

FREE

$49/month
$360/year

Save searches from
Google Scholar,
PubMed

Create lists to
organize your research

Export lists, citations

Read DeepDyve articles

Abstract access only

Unlimited access to over
18 million full-text articles

Print

20 pages / month

PDF Discount

20% off

Sign up
for free
Start 14 day
Free Trial