Periaqueductal gray and emotions: the complexity of the problem and the light at the end of the tunnel, the magnetic resonance imaging

Open access

Abstract

The periaqueductal gray (PAG) is less referred in relationship with emotions than other parts of the brain (e.g. cortex, thalamus, amygdala), most probably because of the difficulty to reach and manipulate this small and deeply lying structure. After defining how to evaluate emotions, we have reviewed the literature and summarized data of the PAG contribution to the feeling of emotions focusing on the behavioral and neurochemical considerations. In humans, emotions can be characterized by three main domains: the physiological changes, the communicative expressions, and the subjective experiences. In animals, the physiological changes can mainly be studied. Indeed, early studies have considered the PAG as an important center of the emotions-related autonomic and motoric processes. However, in vivo imaging have changed our view by highlighting the PAG as a significant player in emotions-related cognitive processes. The PAG lies on the crossroad of networks important in the regulation of emotions and therefore it should not be neglected. In vivo imaging represents a good tool for studying this structure in living organism and may reveal new information about its role beyond its importance in the neurovegetative regulation.

If the inline PDF is not rendering correctly, you can download the PDF file here.

  • Abbadie C Pan YX Pasternak GW. Differential distribution in rat brain of mu opioid receptor carboxy terminal splice variants MOR-1C-like and MOR-1-like immunoreactivity: evidence for region-specific processing. J Comp Neurol 419 244-256 2000.

  • Adametz J O’Leary JL. Experimental mutism resulting from periaqueductal lesions in cats. Neurology 9 636-642 1959.

  • Adolphs R. The neurobiology of social cognition. Curr Opin Neurobiol 11 231-239 2001.

  • Anderzhanova E Kirmeier T Wotjak CT. Animal models in psychiatric research: The RDoC system as a new framework for endophenotype-oriented translational neuroscience. Neurobiol Stress 7 47-56 2017.

  • Apfelbach R Blanchard CD Blanchard RJ Hayes RA McGregor IS. The effects of predator odors in mammalian prey species: a review of field and laboratory studies. Neurosci Biobehav Rev 29 1123-1144 2005.

  • Asan E Steinke M Lesch KP. Serotonergic innervation of the amygdala: targets receptors and implications for stress and anxiety. Histochem Cell Biol 139 785-813 2013.

  • Bales KL. Parenting in Animals. Curr Opin Psychol 15 93-98 2017.

  • Bandler R Shipley MT. Columnar organization in the midbrain periaqueductal gray: modules for emotional expression? Trends Neurosci 17 379-389 1994.

  • Bandler R Keay KA Floyd N Price J. Central circuits mediating patterned autonomic activity during active vs. passive emotional coping. Brain Res Bull 53 95-104 2000.

  • Barba-Muller E Craddock S Carmona S Hoekzema E. Brain plasticity in pregnancy and the postpartum period: links to maternal caregiving and mental health. Arch Womens Ment Health 2018.

  • Bartsch T Knight YE Goadsby PJ. Activation of 5-HT(1B/1D) receptor in the periaqueductal gray inhibits nociception. Ann Neurol 56 371-381 2004.

  • Basbaum AI Fields HL. Endogenous pain control systems: brainstem spinal pathways and endorphin circuitry. Annu Rev Neurosci 7 309-338 1984.

  • Baslow MH. Evidence supporting a role for N-acetyl-L-aspartate as a molecular water pump in myelinated neurons in the central nervous system. An analytical review. Neurochem Int 40 295-300 2002.

  • Beckett S Marsden CA. The effect of central and systemic injection of the 5-HT1A receptor agonist 8-OHDPAT and the 5-HT1A receptor antagonist WAY100635 on periaqueductal grey-induced defence behaviour. J Psychopharmacol 11 35-40 1997.

  • Benarroch EE. Periaqueductal gray: an interface for behavioral control. Neurology 78 210-217 2012.

  • Benedetti F Carlino E Pollo A. How placebos change the patient’s brain. Neuropsychopharmacology 36 339-354 2011.

  • Bindra D. Emotion and behavior theory: current research in historical perspective. In Physiological Correlates of Emotion Reed Elsevier. ed. Perry Black. Academic Press USA 1970.

  • Bingel U Lorenz J Schoell E Weiller C Buchel C. Mechanisms of placebo analgesia: rACC recruitment of a subcortical antinociceptive network. Pain 120 8-15 2006.

  • Blakemore RL Rieger SW Vuilleumier P. Negative emotions facilitate isometric force through activation of prefrontal cortex and periaqueductal gray. Neuroimage 124 627-640 2016.

  • Blanchard C Blanchard R Fellous JM Guimaraes FS Irwin W Ledoux JE McGaugh JL Rosen JB Schenberg LC Volchan E Da Cunha C. The brain decade in debate: III. Neurobiology of emotion. Braz J Med Biol Res 34 283-293 2001.

  • Bodnar RJ. Endogenous opiates and behavior: 2011. Peptides 38 463-522 2012.

  • Boissy A Arnould C Chaillou E Desire L Duvaux-Ponter C Greiveldinger L Leterrier C Richard S Roussel S Saint-Dizier H Meunier-Salaun MC Valance D Veissier I. Emotions and cognition: A new approach to animal welfare. Anim Welf 16 37-43 2007.

  • Bombardi C. Neuronal localization of the 5-HT2 receptor family in the amygdaloid complex. Front Pharmacol 5 68 2014.

  • Brent LJ Chang SW Gariepy JF Platt ML. The neuroethology of friendship. Ann N Y Acad Sci 1316 1-17 2014.

  • Buhle JT Kober H Ochsner KN Mende-Siedlecki P Weber J Hughes BL Kross E Atlas LY McRae K Wager TD. Common representation of pain and negative emotion in the midbrain periaqueductal gray. Soc Cogn Affect Neurosci 8 609-616 2013.

  • Buonanotte F Schurrer C Carpinella M Surur A Marangoni A Palacio S Forteza M Fernandez R Enders J. [Alteration of the antinociceptive systems in chronic daily headaches]. Rev Neurol 43 263-267 2006.

  • Campos AC de Paula Soares V Carvalho MC Ferreira FR Vicente MA Brandao ML Zuardi AW Zangrossi H Jr Guimaraes FS. Involvement of serotonin-mediated neurotransmission in the dorsal periaqueductal gray matter on cannabidiol chronic effects in panic-like responses in rats. Psychopharmacology (Berl) 226 13-24 2013.

  • Cannon WB. The James-Lange theory of emotions: A critical examination and an alternative theory. Am J Psychol 39 106-124 1927.

  • Carrive P Leung P Harris J Paxinos G. Conditioned fear to context is associated with increased Fos expression in the caudal ventrolateral region of the midbrain periaqueductal gray. Neuroscience 78 165-177 1997.

  • Carstens E Hartung M Stelzer B Zimmermann M. Suppression of a hind limb flexion withdrawal reflex by microinjection of glutamate or morphine into the periaqueductal gray in the rat. Pain 43 105-112 1990.

  • Chiou RJ Kuo CC Yen CT. Comparisons of terminal densities of cardiovascular function-related projections from the amygdala subnuclei. Auton Neurosci 181 21-30 2014.

  • Clements JR Beitz AJ Fletcher TF Mullett MA. Immunocytochemical localization of serotonin in the rat periaqueductal gray: a quantitative light and electron microscopic study. J Comp Neurol 236 60-70 1985.

  • Coutinho MR Menescal-de-Oliveira L. Role of homocysteic acid in the guinea pig (Cavia porcellus) anterior cingulate cortex in tonic immobility and the influence of NMDA receptors on the dorsal PAG. Behav Brain Res 208 237-242 2010.

  • Dampney R. Emotion and the cardiovascular system: Postulated role of inputs from the medial prefrontal cortex to the dorsolateral periaqueductal gray. Front Neurosci 12 343 2018.

  • Dantzer R. Les emotions. Presses Universitaires de France”Que sais-je?” 2002a.

  • Dantzer R. Can farm animal welfare be understood without taking into account the issues of emotion and cognition? J Anim Sci 80 E1-E9 2002b.

  • Darwin C. The Expression of the Emotions in Man and Animals. 1872.

  • Davis PJ Zhang SP Winkworth A Bandler R. Neural control of vocalization: respiratory and emotional influences. J Voice 10 23-38 1996.

  • de Almeida J Palacios JM Mengod G. Distribution of 5-HT and DA receptors in primate prefrontal cortex: implications for pathophysiology and treatment. Prog Brain Res 172 101-115 2008.

  • Decety J Michalska KJ Akitsuki Y. Who caused the pain? An fMRI investigation of empathy and intentionality in children. Neuropsychologia 46 2607-2614 2008.

  • Decety J Michalska KJ Akitsuki Y Lahey BB. Atypical empathic responses in adolescents with aggressive conduct disorder: a functional MRI investigation. Biol Psychol 80 203-211 2009.

  • Decety J Echols S Correll J. The blame game: the effect of responsibility and social stigma on empathy for pain. J Cogn Neurosci 22 985-997 2010.

  • de Menezes RC Zaretsky DV Fontes MA DiMicco JA. Microinjection of muscimol into caudal periaqueductal gray lowers body temperature and attenuates increases in temperature and activity evoked from the dorsomedial hypothalamus. Brain Res 1092 129-137 2006.

  • De Oca BM DeCola JP Maren S Fanselow MS. Distinct regions of the periaqueductal gray are involved in the acquisition and expression of defensive responses. J Neurosci 18 3426-3432 1998.

  • Depaulis A Bandler R Vergnes M. Characterization of pretentorial periaqueductal gray matter neurons mediating intraspecific defensive behaviors in the rat by microinjections of kainic acid. Brain Res 486 121-132 1989.

  • DeSantana JM Da Silva LF De Resende MA Sluka KA. Transcutaneous electrical nerve stimulation at both high and low frequencies activates ventrolateral periaqueductal grey to decrease mechanical hyperalgesia in arthritic rats. Neuroscience 163 1233-1241 2009.

  • Dunckley P Wise RG Fairhurst M Hobden P Aziz Q Chang L Tracey I. A comparison of visceral and somatic pain processing in the human brainstem using functional magnetic resonance imaging. J Neurosci 25 7333-7341 2005.

  • Eippert F Bingel U Schoell ED Yacubian J Klinger R Lorenz J Buchel C. Activation of the opioidergic descending pain control system underlies placebo analgesia. Neuron 63 533-543 2009.

  • Ezra M Faull OK Jbabdi S Pattinson KT. Connectivity-based segmentation of the periaqueductal gray matter in human with brainstem optimized diffusion MRI. Hum Brain Mapp 36 3459-3471 2015.

  • Fairhurst M Wiech K Dunckley P Tracey I. Anticipatory brainstem activity predicts neural processing of pain in humans. Pain 128 101-110 2007.

  • Fairhurst M Fairhurst K Berna C Tracey I. An fMRI study exploring the overlap and differences between neural representations of physical and recalled pain. PLoS One 7 e48711 2012.

  • Farmer DG Bautista TG Jones SE Stanic D Dutschmann M. The midbrain periaqueductal grey has no role in the generation of the respiratory motor pattern but provides command function for the modulation of respiratory activity. Respir Physiol Neurobiol 204 14-20 2014.

  • Faull OK Jenkinson M Clare S Pattinson KT. Functional subdivision of the human periaqueductal grey in respiratory control using 7 tesla fMRI. Neuroimage 113 356-364 2015.

  • Figueira RJ Peabody MF Lonstein JS. Oxytocin receptor activity in the ventrocaudal periaqueductal gray modulates anxiety-related behavior in postpartum rats. Behav Neurosci 122 618-628 2008.

  • Freeman SM Walum H Inoue K Smith AL Goodman MM Bales KL Young LJ. Neuroanatomical distribution of oxytocin and vasopressin 1a receptors in the socially monogamous coppery titi monkey (Callicebus cupreus). Neuroscience 273 12-23 2014.

  • Furl N. Structural and effective connectivity reveals potential network-based influences on category-sensitive visual areas. Front Hum Neurosci 9 253 2015.

  • Garcia-Larrea L Peyron R. Pain matrices and neuropathic pain matrices: a review. Pain 154 (Suppl 1) S29-S43 2013.

  • Gaudin S Chaillou E Wycke MA Cornilleau F Moussu C Calandreau L Laine AL Nowak R. All bonds are not alike: A psychoendocrine evaluation of infant attachment. Dev Psychobiol 60 90-103. 2018.

  • Gregg TR Siegel A. Brain structures and neurotransmitters regulating aggression in cats: implications for human aggression. Prog Neuropsychopharmacol Biol Psychiatry. 25 91-140 2001.

  • Guesdon V Meurisse M Chesneau D Picard S Levy F Chaillou E. Behavioral and endocrine evaluation of the stressfulness of single-pen housing compared to group-housing and social isolation conditions. Physiol Behav 147 63-70 2015.

  • Harper DE Ichesco E Schrepf A Hampson JP Clauw DJ Schmidt-Wilcke T Harris RE Harte SE. Resting functional connectivity of the periaqueductal gray is associated with normal inhibition and pathological facilitation in conditioned pain modulation. J Pain 19 635 e1-635 e15 2018.

  • Holstege G Huynh HK. Brain circuits for mating behavior in cats and brain activations and de-activations during sexual stimulation and ejaculation and orgasm in humans. Horm Behav 59 702-707 2011.

  • Hopkins DA Holstege G. Amygdaloid projections to the mesencephalon pons and medulla oblongata in the cat. Exp Brain Res 32 529-547 1978.

  • Hosobuchi Y. Dorsal periaqueductal gray-matter stimulation in humans. Pacing Clin Electrophysiol 10 213-216 1987.

  • Jansen AS Farkas E Mac Sams J Loewy AD. Local connections between the columns of the periaqueductal gray matter: a case for intrinsic neuromodulation. Brain Res 784 329-336 1998.

  • Jurgens U. The role of the periaqueductal grey in vocal behaviour. Behav Brain Res 62 107-117 1994.

  • Keay KA Bandler R. Distinct central representations of inescapable and escapable pain: observations and speculation. Exp Physiol 87 275-279 2002.

  • Kelly AH Beaton LE Magoun HW. A midbrain mechanism for facio-vocal activity. J Neurophysiol 9 181-189 1946.

  • Kirouac G. Cognition et emotions. Les presses de l’universite Laval 223 1998.

  • Klein MO Cruz Ade M Machado FC Picolo G Canteras NS Felicio LF. Periaqueductal gray mu and kappa opioid receptors determine behavioral selection from maternal to predatory behavior in lactating rats. Behav Brain Res 274 62-72 2014.

  • Kyuhou S Gemba H. Two vocalization-related subregions in the midbrain periaqueductal gray of the guinea pig. Neuroreport 9 1607-1610 1998.

  • La Cesa S Tinelli E Toschi N Di Stefano G Collorone S Aceti A Francia A Cruccu G Truini A Caramia F. fMRI pain activation in the periaqueductal gray in healthy volunteers during the cold pressor test. Magn Reson Imaging 32 236-240 2014.

  • Laprairie JL Murphy AZ. Neonatal injury alters adult pain sensitivity by increasing opioid tone in the periaqueductal gray. Front Behav Neurosci 3 31 2009.

  • LeDoux JE Iwata J Cicchetti P Reis DJ. Different projections of the central amygdaloid nucleus mediate autonomic and behavioral correlates of conditioned fear. J Neurosci 8 2517-2529 1988.

  • Lei J Sun T Lumb BM You HJ. Roles of the periaqueductal gray in descending facilitatory and inhibitory controls of intramuscular hypertonic saline induced muscle nociception. Exp Neurol 257 88-94 2014.

  • Leman S Dielenberg RA Carrive P. Effect of dorsal periaqueductal gray lesion on cardiovascular and behavioural responses to contextual conditioned fear in rats. Behav Brain Res 143 169-176 2003.

  • Leventhal H Scherer K. The relationship of emotion to cognition: A functional approach to a semantic controversy. Cogn Emot 1 3-28 1987.

  • Leventhal H Patrick-Miller L. Emotions and physical illness: Causes and indicators of vulnerability. Handbook of Emotions 2nd ed. M. Lewis & J. M. Haviland-Jones New York Guilford Press 2000.

  • Levy F. Neurobiological mechanisms involved in recognition of olfactory signature of the young in sheep. J Soc Biol 196 77-83 2002.

  • Linnman C Borsook D. Completing the Pain Circuit: Recent Advances in Imaging Pain and Inflammation beyond the Central Nervous System. Rambam Maimonides Med J 4 e0026 2013.

  • Lonstein JS Stern JM. Somatosensory contributions to c-fos activation within the caudal periaqueductal gray of lactating rats: effects of perioral rooting and suckling stimuli from pups. Horm Behav 32 155-166 1997.

  • Lonstein JS Stern JM. Site and behavioral specificity of periaqueductal gray lesions on postpartum sexual maternal and aggressive behaviors in rats. Brain Res 804 21-35 1998.

  • Lonstein JS Simmons DA Stern JM. Functions of the caudal periaqueductal gray in lactating rats: kyphosis lordosis maternal aggression and fearfulness. Behav Neurosci 112 1502-1518 1998.

  • Loyd DR Murphy AZ. The role of the periaqueductal gray in the modulation of pain in males and females: are the anatomy and physiology really that different? Neural Plast 2009 462879 2009.

  • Maddock RJ Garrett AS Buonocore MH. Posterior cingulate cortex activation by emotional words: fMRI evidence from a valence decision task. Hum Brain Mapp 18 30-41 2003.

  • Martinez RC de Oliveira AR Brandao ML. Conditioned and unconditioned fear organized in the periaqueductal gray are differentially sensitive to injections of muscimol into amygdaloid nuclei. Neurobiol Learn Mem 85 58-65 2006.

  • Mauss IB Robinson MD. Measures of emotion: A review. Cogn Emot 23 209-237 2009.

  • McNaughton N. Biology and Emotion (Problems in the Behavioural Sciences). Cambridge Cambridge University Press 1989.

  • Menant O Andersson F Zelena D Chaillou E. The benefits of magnetic resonance imaging methods to extend the knowledge of the anatomical organisation of the periaqueductal gray in mammals. J Chem Neuroanat 77 110-120 2016a.

  • Menant O Destrez A Deiss V Boissy A Delagrange P Calandreau L Chaillou E. Regulation des emotions chez l’animal d’elevage : focus sur les acteurs neurobiologiques. INRA Prod Anim 29 241-254 2016b.

  • Menant O Prima MC Morisse M Cornilleau F Moussu C Gautier A Blanchon H Meurisse M Delagrange P Tillet Y Chaillou E. 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. Brain Struct Funct 223 3297-3316 2018.

  • Mobbs D Petrovic P Marchant JL Hassabis D Weiskopf N Seymour B Dolan RJ Frith CD. When fear is near: threat imminence elicits prefrontal-periaqueductal gray shifts in humans. Science 317 1079-1083 2007.

  • Mobbs D Yu R Rowe JB Eich H FeldmanHall O Dalgleish T. Neural activity associated with monitoring the oscillating threat value of a tarantula. Proc Natl Acad Sci U S A 107 20582-20586 2010.

  • Monassi CR Leite-Panissi CR Menescal-de-Oliveira L. Ventrolateral periaqueductal gray matter and the control of tonic immobility. Brain Res Bull 50 201-218 1999.

  • Monteillet-Agius G Fein J Anton B Evans CJ. ORL-1 and mu opioid receptor antisera label different fibers in areas involved in pain processing. J Comp Neurol 399 373-383 1998.

  • Morgan MM Whitney PK Gold MS. Immobility and flight associated with antinociception produced by activation of the ventral and lateral/dorsal regions of the rat periaqueductal gray. Brain Res 804 159-166 1998.

  • Morgan MM Carrive P. Activation of the ventrolateral periaqueductal gray reduces locomotion but not mean arterial pressure in awake freely moving rats. Neuroscience 102 905-910 2001.

  • Moskowitz AS Goodman RR. Autoradiographic analysis of mu1 mu2 and delta opioid binding in the central nervous system of C57BL/6BY and CXBK (opioid receptor-deficient) mice. Brain Res 360 108-116 1985.

  • Motta SC Carobrez AP Canteras NS. The periaqueductal gray and primal emotional processing critical to influence complex defensive responses fear learning and reward seeking. Neurosci Biobehav Rev 76 39-47 2017.

  • Moura LM Canteras NS Sukikara MH Felicio LF. Morphine infusions into the rostrolateral periaqueductal gray affect maternal behaviors. Braz J Med Biol Res 43 899-905 2010.

  • Najafi M Kinnison J Pessoa L. Dynamics of Intersubject Brain Networks during Anxious Anticipation. Front Hum Neurosci 11 552 2017.

  • Nakamura T Tomida M Yamamoto T Ando H Takamata T Kondo E Kurasawa I Asanuma N. The endogenous opioids related with antinociceptive effects induced by electrical stimulation into the amygdala. Open Dent J 7 27-35 2013.

  • Nashold BS Jr. Slaughter DG. Effects of stimulating or destroying the deep cerebellar regions in man. J Neurosurg 31 172-186 1969.

  • Noriuchi MY Kikuchi Y Senoo A. The functional neuroanatomy of maternal love: mother’s response to infant’s attachment behaviors. Biol Psychiatry 63 415-423 2008.

  • Nunes-de-Souza V Nunes-de-Souza R Rodgers RJ Canto-de-Souza A. Blockade of 5-HT(2) receptors in the periaqueductal grey matter (PAG) abolishes the anxiolytic-like effect of 5-HT(1A) receptor antagonism in the median raphe nucleus in mice. Behav Brain Res 225 547-553 2011.

  • O’Connell LA Hofmann HA. The vertebrate mesolimbic reward system and social behavior network: a comparative synthesis. J Comp Neurol 519 3599-5639 2011.

  • Oka T Tsumori T Yokota S Yasui Y. Neuroanatomical and neurochemical organization of projections from the central amygdaloid nucleus to the nucleus retroambiguus via the periaqueductal gray in the rat. Neurosci Res 62 286-298 2008.

  • Osorio-Garcia MI Croitor Sava AR Sima DM Nielsen FU Himmelreich U Van Huffel S. Quantification Improvements of 1H MRS Signals. In: Magnetic Resonance Spectroscopy (Ed. Dong-Hyun Kim) pp. 3-28 IntechOpen London 2012.

  • Paradiso S Johnson DL Andreasen NC O’Leary DS Watkins GL Ponto LL Hichwa RD. Cerebral blood flow changes associated with attribution of emotional valence to pleasant unpleasant and neutral visual stimuli in a PET study of normal subjects. Am J Psychiatry 156 1618-1629 1999.

  • Parsons CE Young KS Stein A Kringelbach ML. Intuitive parenting: understanding the neural mechanisms of parents’ adaptive responses to infants. Curr Opin Psychol 15 40-44 2017.

  • Pereira EA Lu G Wang S Schweder PM Hyam JA Stein JF Paterson DJ Aziz TZ Green AL. Ventral periaqueductal grey stimulation alters heart rate variability in humans with chronic pain. Exp Neurol 223 574-581 2010.

  • Pesini P Pego-Reigosa R Tramu G Covenas R. Distribution of alpha-neoendorphin immunoreactivity in the diencephalon and the brainstem of the dog. J Chem Neuroanat 22 251-262 2001.

  • Phelps EA LeDoux JE. Contributions of the amygdala to emotion processing: from animal models to human behavior. Neuron 48 175-187 2005.

  • Price DD. Central neural mechanisms that interrelate sensory and affective dimensions of pain. Mol Interv 2 392- 403 339 2002.

  • Randall WL. The behavior of cats (Felis catus L.) with lesions in the caudal midbrain region. Behaviour 23 107-134 1964.

  • Rea K Roche M Finn DP. Modulation of conditioned fear fear-conditioned analgesia and brain regional c-Fos expression following administration of muscimol into the rat basolateral amygdala. J Pain 12 712-721 2011.

  • Reynolds WJ Scott B. Empathy: a crucial component of the helping relationship. J Psychiatr Ment Health Nurs 6 363-370 1999.

  • Rizvi TA Ennis M Behbehani MM Shipley MT. Connections between the central nucleus of the amygdala and the midbrain periaqueductal gray: topography and reciprocity. J Comp Neurol 303 121-131 1991.

  • Roeling TA Veening JG Peters JP Vermelis ME Nieuwenhuys R. Efferent connections of the hypothalamic “grooming area” in the rat. Neuroscience 56 199-225 1993.

  • Roxo MR Franceschini PR Zubaran C Kleber FD Sander JW. The limbic system conception and its historical evolution. ScientificWorldJournal 11 2428-2441 2011.

  • Roy M Shohamy D Daw N Jepma M Wimmer GE Wager TD. Representation of aversive prediction errors in the human periaqueductal gray. Nat Neurosci 17 1607-1612 2014.

  • Russell J Mahrabian A. Evidence for a Three-Factor Theory of Emotions. J Res Pers 11 273-294 1977.

  • Saavedra JM Palkovits M Brownstein MJ Axelrod J. Serotonin distribution in the nuclei of the rat hypothalamus and preoptic region. Brain Res 77 157-165 1974.

  • Sampaio KN Mauad H Biancardi VC Barros JL Amaral FT Schenberg LC Vasquez EC. Cardiovascular changes following acute and chronic chemical lesions of the dorsal periaqueductal gray in conscious rats. J Auton Nerv Syst 76 99-107 1999.

  • Satpute AB Wager TD Cohen-Adad J Bianciardi M Choi JK Buhle JT Wald LL Barrett LF. Identification of discrete functional subregions of the human periaqueductal gray. Proc Natl Acad Sci U S A 110 17101-17106 2013.

  • Schachter S Singer JE. Cognitive social and physiological determinants of emotional state. Psychol Rev 69 379-399 1962.

  • Schenberg LC Brandao CA Vasquez EC. Role of periaqueductal gray matter in hypertension in spontaneously hypertensive rats. Hypertension 26 1125-1128 1995.

  • Sebe F Aubin T Boue A Poindron P. Mother-young vocal communication and acoustic recognition promote preferential nursing in sheep. J Exp Biol 211 3554-3562 2008.

  • Shepherd SV Freiwald WA. Functional networks for social communication in the Macaque Monkey. Neuron 99 413-420 e3 2018.

  • Sela VR Biesdorf C Ramos DH Zangrossi H Jr Graeff FG Audi EA. Serotonin-1A receptors in the dorsal periaqueductal gray matter mediate the panicolytic-like effect of pindolol and paroxetine combination in the elevated T-maze. Neurosci Lett 495 63-66 2011.

  • Skultety FM. The behavioral effects of destructive lesions of the periaqueductal gray matter in adult cats. J Comp Neurol 110 337-365 1958.

  • Snider RS Maiti A. Cerebellar contributions to the Papez circuit. J Neurosci Res 2 133-146 1976.

  • Stewart-Williams S Podd J. The placebo effect: dissolving the expectancy versus conditioning debate. Psychol Bull 130 324-340 2004.

  • Stone E Coote JH Allard J Lovick TA. GABAergic control of micturition within the periaqueductal grey matter of the male rat. J Physiol 589 2065-2078 2011.

  • Subramanian HH Balnave RJ Holstege G. The midbrain periaqueductal gray control of respiration. J Neurosci 28 12274-12283 2008.

  • Sukikara MH Mota-Ortiz SR Baldo MV Felicio LF Canteras NS. The periaqueductal gray and its potential role in maternal behavior inhibition in response to predatory threats. Behav Brain Res 209 226-233 2010.

  • Swanson LW McKellar S. The distribution of oxytocin- and neurophysin-stained fibers in the spinal cord of the rat and monkey. J Comp Neurol 188 87-106 1979.

  • Takasaki A Hui M Sasaki M. Is the periaqueductal gray an essential relay center for the micturition reflex pathway in the cat? Brain Res 1317 108-115 2010.

  • Tasker RR. Identification of pain processing systems by electrical stimulation of the brain. Hum Neurobiol 1 261- 272 1982.

  • Teodorov E Bernardi MM Ferrari MF Fior-Chadi DR Felicio LF. Plasticity of opioid receptors in the female periaqueductal gray: multiparity-induced increase in the activity of genes encoding for mu and kappa receptors and a post-translational decrease in delta receptor expression. J Mol Neurosci 43 175-181 2011.

  • Turner EA. Cerebral control of respiration. Brain 77 448-486 1954.

  • van der Graaf M. In vivo magnetic resonance spectroscopy: basic methodology and clinical applications. Eur Biophys J 39 527-540 2010.

  • Veissier I Boissy A. Stress and welfare: two complementary concepts that are intrinsically related to the animal’s point of view. Physiol Behav 92 429-433 2007.

  • Vianna DML Graeff FG Landeira-Fernandez J Brandao ML. Lesion of the ventral periaqueductal gray reduces conditioned fear but does not change freezing by stimulation of the dorsal periaqueductal gray. Learn Mem 8 164-169 2001.

  • Vianna DM Brandao ML. Anatomical connections of the periaqueductal gray: specific neural substrates for different kinds of fear. Braz J Med Biol Res 36 557-566 2003.

  • Wager TD Rilling JK Smith EE Sokolik A Casey KL Davidson RJ Kosslyn SM Rose RM Cohen JD. Placeboinduced changes in FMRI in the anticipation and experience of pain. Science 303 1162-1167 2004.

  • Wager TD van Ast VA Hughes BL Davidson ML Lindquist MA Ochsner KN. Brain mediators of cardiovascular responses to social threat part II: Prefrontal-subcortical pathways and relationship with anxiety. Neuroimage 47 836-851 2009.

  • Walker P Carrive P. Role of ventrolateral periaqueductal gray neurons in the behavioral and cardiovascular responses to contextual conditioned fear and poststress recovery. Neuroscience 116 897-912 2003.

  • Wiedenmayer CP Barr GA. Mu opioid receptors in the ventrolateral periaqueductal gray mediate stress-induced analgesia but not immobility in rat pups. Behav Neurosci 114 125-136 2000.

  • Wu D Wang S Stein JF Aziz TZ Green AL. Reciprocal interactions between the human thalamus and periaqueductal gray may be important for pain perception. Exp Brain Res 232 527-534 2014.

  • Xavier CH Ianzer D Lima AM Marins FR Pedrino GR Vaz G Menezes GB Nalivaiko E Fontes MA. Excitatory amino acid receptors mediate asymmetry and lateralization in the descending cardiovascular pathways from the dorsomedial hypothalamus. PLoS One 9 e112412 2014.

  • Yoshida W Seymour B Koltzenburg M Dolan RJ. Uncertainty increases pain: evidence for a novel mechanism of pain modulation involving the periaqueductal gray. J Neurosci 33 5638-5646 2013.

  • Yoshimura R Kiyama H Kimura T Araki T Maeno H Tanizawa O Tohyama M. Localization of oxytocin receptor messenger ribonucleic acid in the rat brain. Endocrinology 133 1239-1246 1993.

  • Young RF Kroening R Fulton W Feldman RA Chambi I. Electrical stimulation of the brain in treatment of chronic pain. Experience over 5 years. J Neurosurg 62 389-396 1985.

  • Young KS Parsons CE Stein A Vuust P Craske MG Kringelbach ML. The neural basis of responsive caregiving behaviour: Investigating temporal dynamics within the parental brain. Behav Brain Res 325 105-116 2017.

  • Yu CX Li B Xu YK Ji TT Li L Zhao CJ Chen L Zhuo ZZ. Altered functional connectivity of the periaqueductal gray in chronic neck and shoulder pain. Neuroreport 28 720-725 2017.

  • Zhang SP Bandler R Carrive P. Flight and immobility evoked by excitatory amino acid microinjection within distinct parts of the subtentorial midbrain periaqueductal gray of the cat. Brain Res 520 73-82 1990.

Search
Journal information
Impact Factor


CiteScore 2018: 1.27

SCImago Journal Rank (SJR) 2018: 0.411
Source Normalized Impact per Paper (SNIP) 2018: 0.441

Metrics
All Time Past Year Past 30 Days
Abstract Views 0 0 0
Full Text Views 391 363 53
PDF Downloads 288 273 54