Role of corticotropin-releasing factor, vasopressin and the autonomic nervous system in learning and memory.

Learning and memory are essential requirements for every living organism in order to cope with environmental demands, which enables it to adapt to changes in the conditions of life. Research on the effects of hormones on memory has focused on hormones such as adrenocorticotropic hormone (ACTH), glucocorticoids, vasopressin, oxytocin, epinephrine, corticotropin-releasing factor (CRF) that are released into the blood and brain following arousing or stressful experiences. Most of the information have been derived from studies on conditioned behavior, in particular, avoidance behavior in rats. In these tasks, an aversive situation was used as a stimulus for learning. Aversive stimuli are associated with the release of stress hormones and neuropeptides. Many factors play a role in different aspects of learning and memory processes. Neuropeptides not only affect attention, motivation, concentration and arousal or vigilance, but also anxiety and fear. In this way, they participate in learning and memory processes. Furthermore, neuropeptides such as CRF and vasopressin modulate the release of stress hormones such as epinephrine. In turn, systemic catecholamines enhance memory consolidation. CRF and vasopressin are colocalized in neurons from the nucleus paraventricularis, which project to nuclei in the brainstem involved in autonomic regulation. The objective of this paper is to discuss the role of CRF, vasopressin, and the autonomic nervous system (ANS) in learning and memory processes. Both CRF and vasopressin have effects in the same direction on behavior, learning and memory processes and stress responses (release of catecholamines and ACTH). These neuropeptides may act synergistically or in a concerted action aimed to learn to adapt to environmental demands.

[1]  Y. Ohgami,et al.  Effect of active fragments of arginine-vasopressin on the disturbance of spatial cognition in rats , 1997, Behavioural Brain Research.

[2]  J. Verbalis,et al.  In vitro release of vasopressin and oxytocin from rat median eminence tissue. , 1986, Neuroendocrinology.

[3]  D. Wied,et al.  Neuropeptides: Effects on paradoxical sleep and theta rhythm in rats , 1978, Pharmacology Biochemistry and Behavior.

[4]  Q. Pittman,et al.  Release of vasopressin and oxytocin by paraventricular stimulation in rats. , 1990, The American journal of physiology.

[5]  M. Nijsen,et al.  The Role of the CRH Type 1 Receptor in Autonomic Responses to Corticotropin-Releasing Hormone in the Rat , 2000, Neuropsychopharmacology.

[6]  F. Luft,et al.  Vasopressin: mechanism of central cardiovascular action in conscious rats. , 1986, Journal of cardiovascular pharmacology.

[7]  M. Whitnall Stress selectively activates the vasopressin-containing subset of corticotropin-releasing hormone neurons. , 1989, Neuroendocrinology.

[8]  T. Lovenberg,et al.  Characterization of Corticotropin‐releasing Factor Receptor Subtypes a , 1996 .

[9]  M. Fanselow,et al.  Conditional and unconditional components of post-shock freezing , 1980, The Pavlovian journal of biological science.

[10]  E. Zimmerman,et al.  Magnocellular hypothalamic projections to the lower brain stem and spinal cord of the rat. Immunocytochemical evidence for predominance of the oxytocin-neurophysin system compared to the vasopressin-neurophysin system. , 1980, Neuroendocrinology.

[11]  L. Fisher Central autonomic modulation of cardiac baroreflex by corticotropin-releasing factor. , 1989, The American journal of physiology.

[12]  S. Maier,et al.  The Impact of the Nonpeptide Corticotropin-Releasing Hormone Antagonist Antalarmin on Behavioral and Endocrine Responses to Stress * , 1998 .

[13]  F. Bloom,et al.  Can aversive properties of (peripherally-injected) vasopressin account for its putative role in memory? , 1983, Behavioural Brain Research.

[14]  S. Lightman,et al.  Haemodynamic effects of arginine-vasopressin microinjections into the nucleus tractus solitarius: A comparative study of vasopressin, a selective vasopressin receptor agonist and antagonist, and oxytocin , 1984, Neuroscience Letters.

[15]  M. Brody,et al.  Regional hemodynamic responses to central administration of corticotropin-releasing factor (CRF) , 1988, Brain Research.

[16]  E. D. De Souza,et al.  Corticotropin-releasing factor receptors: an overview. , 2009, Experimental and clinical endocrinology & diabetes : official journal, German Society of Endocrinology [and] German Diabetes Association.

[17]  D. Wied,et al.  Central Vasopressin Impairs the Baroreceptor Heart Rate Reflex in Conscious Rats , 1990, Journal of cardiovascular pharmacology.

[18]  J. Koolhaas,et al.  Conditioned neuroendocrine and cardiovascular stress responsiveness accompanying behavioral passivity and activity in aged and in young rats , 1992, Physiology & Behavior.

[19]  N. Kalin,et al.  Fear-motivated behavior induced by prior shock experience is mediated by corticotropin-releasing hormone systems , 1990, Brain Research.

[20]  M. Sakanaka,et al.  Corticotropin releasing factor‐like immunoreactivity in the rat brain as revealed by a modified cobalt‐glucose oxidase‐diaminobenzidine method , 1987, The Journal of comparative neurology.

[21]  P. Sawchenko Evidence for differential regulation of corticotropin-releasing factor and vasopressin immunoreactivities in parvocellular neurosecretory and autonomic-related projections of the paraventricular nucleus , 1987, Brain Research.

[22]  F. Antoni Novel ligand specificity of pituitary vasopressin receptors in the rat. , 1984, Neuroendocrinology.

[23]  A. Steffens,et al.  University of Groningen The Hypothalamus, Intrinsic Connections and Outflow Pathways to the Endocrine System in Relation to the Control of Feeding and Metabolism Luiten, , 2002 .

[24]  S. Korte,et al.  Central Actions of Corticotropin-Releasing Hormone (CRH) on Behavioral, Neuroendocrine, and Cardiovascular Regulation: Brain Corticoid Receptor Involvement , 1993, Hormones and Behavior.

[25]  W. Young,et al.  Cellular localization of vasopressin V1a receptor messenger ribonucleic acid in adult male rat brain, pineal, and brain vasculature. , 1994, Endocrinology.

[26]  E. De Souza,et al.  Localization of novel corticotropin-releasing factor receptor (CRF2) mRNA expression to specific subcortical nuclei in rat brain: comparison with CRF1 receptor mRNA expression , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[27]  W. Vale,et al.  Corticotropin-releasing factor (CRF): central effects on mean arterial pressure and heart rate in rats. , 1982, Endocrinology.

[28]  R. Quirion,et al.  Potential neurotrophic factors in the mammalian central nervous system: functional significance in the developing and aging brain. , 1990, International review of neurobiology.

[29]  Craig W. Berridge,et al.  Physiological and behavioral responses to corticotropin-releasing factor administration: is CRF a mediator of anxiety or stress responses? , 1990, Brain Research Reviews.

[30]  E. Tribollet,et al.  Vasopressin and oxytocin receptors in the central nervous system. , 1996, Critical reviews in neurobiology.

[31]  X. Wang,et al.  Intracerebroventricular administration of corticotropin-releasing factor antagonist attenuates c-fos mRNA expression in the paraventricular nucleus after stress. , 1995, Neuroendocrinology.

[32]  P. Kamphuis,et al.  Endogenous corticotropin-releasing hormone inhibits conditioned-fear-induced vagal activation in the rat. , 2000, European journal of pharmacology.

[33]  W. Vale,et al.  Corticotropin-releasing factor: actions on the sympathetic nervous system and metabolism. , 1982, Endocrinology.

[34]  W. Vale,et al.  Corticotropin-releasing factor up-regulates its own receptor mRNA in the paraventricular nucleus of the hypothalamus. , 1996, Brain research. Molecular brain research.

[35]  L. Fisher,et al.  Corticotropin-releasing factor (CRF): mechanism to elevate mean arterial pressure and heart rate , 1983, Regulatory Peptides.

[36]  G. Kovacs,et al.  Facilitation of avoidance behavior by vasopressin fragments microinjected into limbic-midbrain structures , 1986, Brain Research.

[37]  D. Gibbs Dissociation of oxytocin, vasopressin and corticotropin secretion during different types of stress. , 1984, Life sciences.

[38]  J. L. Martínez,et al.  Modulation of memory storage by treatments affecting peripheral catecholamines , 1982 .

[39]  S. Henriksen,et al.  Effects of corticotropin-releasing factor and growth hormone-releasing factor on sleep and activity in rats. , 1986, Neuroendocrinology.

[40]  L. Fisher,et al.  Central nervous effects of CRF and angiotensin II on cardiac output in conscious rats. , 1990, Journal of applied physiology.

[41]  M. Joëls,et al.  Arginine8-vasopressin enhances the responses of lateral septal neurons in the rat to excitatory amino acids and fimbria-fornix stimuli , 1984, Brain Research.

[42]  J. Borrell,et al.  Inhibitory avoidance deficit following short-term adrenalectomy in the rat: the role of adrenal catecholamines. , 1983, Behavioral and neural biology.

[43]  H. Ohata,et al.  Non-peptidic corticotropin-releasing hormone receptor type 1 antagonist reverses restraint stress-induced shortening of sodium pentobarbital-induced sleeping time of rats: evidence that an increase in arousal induced by stress is mediated through CRH receptor type 1 , 1998, Neuroscience Letters.

[44]  A. Budzikowski,et al.  Central ANP attenuates pressor responses to central AVP in WKY and SHR , 1991, Brain Research Bulletin.

[45]  J. Burbach,et al.  Vasopressin and oxytocin. Their presence in the central nervous system and their functional significance in brain processes related to behaviour and memory. , 1986, Acta endocrinologica. Supplementum.

[46]  D. Wied,et al.  Autonomic and behavioral effects of centrally administered corticotropin-releasing factor in rats. , 1991, Endocrinology.

[47]  T. Gray,et al.  Neuropeptide neuronal efferents from the bed nucleus of the stria terminalis and central amygdaloid nucleus to the dorsal vagal complex in the rat , 1987, The Journal of comparative neurology.

[48]  J. Coote,et al.  Role of vasopressin in sympathetic response to paraventricular nucleus stimulation in anesthetized rats. , 1994, The American journal of physiology.

[49]  T. Gray,et al.  Corticotropin-releasing factor receptor antagonist: effects on the autonomic nervous system and cardiovascular function , 1986, Regulatory Peptides.

[50]  N. Ling,et al.  The antagonistic effect of corticotropin-releasing factor on pentobarbital in rats , 1986, Brain Research.

[51]  C. A. Marsan,et al.  Neuronal plasticity and memory formation , 1982 .

[52]  B. J. Cole 7 – Corticotropin-Releasing Factor, Stress, and Animal Behavior , 1991 .

[53]  T. Bliss,et al.  Long‐lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path , 1973, The Journal of physiology.

[54]  N. Murakami,et al.  The central role of corticotrophin‐releasing factor (CRF‐41) in psychological stress in rats. , 1993, The Journal of physiology.

[55]  Brown Mr.,et al.  Corticotropin-releasing factor: effects on the autonomic nervous system and visceral systems. , 1985 .

[56]  J. Slangen,et al.  Plasma catecholamine, corticosterone and glucose responses to repeated stress in rats: Effect of interstressor interval length , 1990, Physiology & Behavior.

[57]  G. Feuerstein,et al.  Cardiovascular effects of centrally administered vasopressin in conscious and anesthetized rats , 1985, Neuropeptides.

[58]  T. Lovenberg,et al.  CRF2 alpha and CRF2 beta receptor mRNAs are differentially distributed between the rat central nervous system and peripheral tissues. , 1995, Endocrinology.

[59]  Y. Taché,et al.  Intracerebroventricular CRF inhibits cold restraint-induced c-fos expression in the dorsal motor nucleus of the vagus and gastric erosions in rats , 1996, Brain Research.

[60]  M. Nijsen,et al.  Vagal Activation in Novelty-Induced Tachycardia During the Light Phase in the Rat , 1998, Physiology & Behavior.

[61]  E. Tribollet,et al.  Localization and pharmacological characterization of high affinity binding sites for vasopressin and oxytocin in the rat brain by light microscopic autoradiography , 1988, Brain Research.

[62]  E. B. Souza Corticotropin-releasing factor receptors: Physiology, pharmacology, biochemistry and role in central nervous system and immune disorders , 1995, Psychoneuroendocrinology.

[63]  D. Gallager,et al.  Autoradiographic Localization of CRF1 and CRF2 Binding Sites in Adult Rat Brain , 1997, Neuropsychopharmacology.

[64]  S. Lightman,et al.  Differential regulation of hypothalamic pituitary corticotropin releasing hormone receptors during development of adjuvant-induced arthritis in the rat. , 1997, The Journal of endocrinology.

[65]  I. Merchenthaler,et al.  Immunocytochemical localization of corticotropin releasing factor (CRF) in the rat spinal cord , 1983, Brain Research.

[66]  M. Nijsen,et al.  Conditioned fear-induced tachycardia in the rat: vagal involvement. , 1998, European journal of pharmacology.

[67]  J. Herman,et al.  Regulatory changes in neuroendocrine stress-integrative circuitry produced by a variable stress paradigm. , 1995, Neuroendocrinology.

[68]  G. Tsujimoto,et al.  Effects of Arginine-Vasopressin Fragment 4–9 on Rodent Cholinergic Systems , 1999, Pharmacology Biochemistry and Behavior.

[69]  M. Joëls,et al.  Amino acid neurotransmission between fimbria-fornix fibers and neurons in the lateral septum of the rat: A microiontophoretic study , 1984, Experimental Neurology.

[70]  Y. Du,et al.  Function and molecular basis of action of vasopressin 4-8 and its analogues in rat brain. , 1998, Progress in brain research.

[71]  B. Roozendaal,et al.  University of Groningen Differential effect of lesioning of the central amygdala on the bradycardiac and behavioral response of the rat in relation to conditioned social and solitary stress , 2017 .

[72]  R. Ader,et al.  Retention of a passive avoidance response as a function of the intensity and duration of electric shock , 1972 .

[73]  J. Haywood,et al.  Sympathetic nervous system activation by glutamate injections into the paraventricular nucleus , 1992, Brain Research.

[74]  D. Wied Peptides and behavior. , 1977 .

[75]  J. D. McGaugh Memory--a century of consolidation. , 2000, Science.

[76]  C. Kilts,et al.  Alterations in corticotropin-releasing factor-like immunoreactivity in discrete rat brain regions after acute and chronic stress , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[77]  L. Mahan,et al.  Extrapituitary expression of the rat V1b vasopressin receptor gene. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[78]  D. Wied,et al.  Time-related memory effects of vasopressin analogues in rats , 1986, Pharmacology Biochemistry and Behavior.

[79]  G. Koob,et al.  Effect of corticotropin-releasing factor antagonist on behavioral and neuroendocrine responses during exposure to defensive burying paradigm in rats , 1994, Physiology & Behavior.

[80]  D. R. Britton Stress-Related Behavioral Effects of Corticotropin-Releasing Factor , 1989 .

[81]  G. Croiset,et al.  Differential effects of DGAVP on acquisition and extinction of active avoidance behavior , 1991, Peptides.

[82]  E. Freis,et al.  Prophylactic approach to hypertensive diseases , 1979 .

[83]  L. Swanson,et al.  Organization of ovine corticotropin-releasing factor immunoreactive cells and fibers in the rat brain: an immunohistochemical study. , 1983, Neuroendocrinology.

[84]  Z. Mo,et al.  Effects of vasopressin and angiotensin II on neurones in the rat dorsal motor nucleus of the vagus, in vitro. , 1992, The Journal of physiology.

[85]  S. Foote,et al.  Distribution of corticotropin‐releasing‐factor‐like immunoreactivity in brainstem of two monkey species (Saimiri sciureus and Macaca fascicularis): An immunohistochemical study , 1988, The Journal of comparative neurology.

[86]  G. Kovacs,et al.  Facilitation of memory consolidation by vasopressin: Mediation by terminals of the dorsal noradrenergic bundle? , 1979, Brain Research.

[87]  M. Opp,et al.  Blockade of corticotropin-releasing hormone receptors reduces spontaneous waking in the rat. , 1998, American journal of physiology. Regulatory, integrative and comparative physiology.

[88]  W. Vale,et al.  Corticotropin-releasing factor: a physiologic regulator of adrenal epinephrine secretion , 1985, Brain Research.

[89]  M. Wayner,et al.  Corticotrophin‐releasing factor produces a long‐lasting enhancement of synaptic efficacy in the hippocampus , 1998, The European journal of neuroscience.

[90]  T. Gray,et al.  The amygdala: corticotropin-releasing factor, steroids, and stress. , 1996, Critical reviews in neurobiology.

[91]  R. Wan,et al.  Changes in heart rate and body temperature during passive avoidance behavior in rats , 1990, Physiology & Behavior.

[92]  G. Kovacs,et al.  Dose-dependent action of corticosteroids on brain serotonin content and passive avoidance behavior , 1977, Hormones and Behavior.

[93]  D. Wied Long Term Effect of Vasopressin on the Maintenance of a Conditioned Avoidance Response in Rats , 1971, Nature.

[94]  J. Koolhaas,et al.  Anxiolytics and stress-induced behavioural and cardiac responses: a study of diazepam and ipsapirone (TVX Q 7821). , 1990, European journal of pharmacology.

[95]  D. Hebb Textbook of psychology , 1958 .

[96]  T. Gray,et al.  Peptide immunoreactive neurons in the amygdala and the bed nucleus of the stria terminalis project to the midbrain central gray in the rat , 1992, Peptides.

[97]  Q. Pittman,et al.  Vasopressin antagonist in nucleus tractus solitarius/vagal area reduces pressor and tachycardia responses to paraventricular nucleus stimulation in rats , 1985, Neuroscience Letters.

[98]  L. Fisher,et al.  Differentiated hemodynamic responses to central versus peripheral administration of corticotropin-releasing factor in conscious rats. , 1991, Journal of the autonomic nervous system.

[99]  T. Sugimoto,et al.  Molecular cloning and characterization of rat V1b vasopressin receptor: evidence for its expression in extra-pituitary tissues. , 1995, Biochemical and biophysical research communications.

[100]  R. F. Kirby,et al.  Central oxytocin systems may mediate a cardiovascular response to acute stress in rats. , 1989, The American journal of physiology.

[101]  C. Nemeroff,et al.  Stress, Neuropeptides, and Systemic Disease , 1991 .

[102]  P. Sawchenko,et al.  Differential regulation of corticotropin-releasing factor mRNA in rat brain regions by glucocorticoids and stress , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[103]  G. Gillies,et al.  Corticotropin releasing activity of the new CRF is potentiated several times by vasopressin , 1982, Nature.

[104]  A. Sahgal,et al.  Failure of vasopressin to enhance memory in a passive avoidance task in rats , 1982, Neuroscience Letters.

[105]  F. Bloom,et al.  Vasopressor receptor antagonist prevents behavioural effects of vasopressin , 1981, Nature.

[106]  Y. Taché,et al.  Neuropeptides and Stress , 2012, Hans Selye Symposia on Neuroendocrinology and Stress.

[107]  R. Bartus,et al.  The cholinergic hypothesis of geriatric memory dysfunction. , 1982, Science.

[108]  A. K. Johnson,et al.  Blood pressure and heart rate responses to microinjection of vasopressin into the nucleus tractus solitarius region of the rat , 1982, Neuropharmacology.