Progressive postnatal assembly of limbic-autonomic circuits revealed by central transneuronal transport of pseudorabies virus

Journal of Neuroscience

Volumn 20, Issue 7, 2000, Pages 2731-2741

  Rinaman, Linda ^a   Levitt, Pat ^a   Card, J Patrick ^a  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

Central nucleus of the amygdala, bed nucleus of the stria terminalis; Development; Dorsal motor nucleus of the vagus; Gastrointestinal; Insular cortex; Lateral hypothalamic area; Medial prefrontal cortex; Nucleus of the solitary tract; Parasympathetic; Paraventricular nucleus of the hypothalamus; Stomach; Sympathetic

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTONOMIC NERVE; AUTONOMIC NERVOUS SYSTEM; BRAIN DEVELOPMENT; BRAIN STEM; CONTROLLED STUDY; FOREBRAIN; LIMBIC SYSTEM; NERVE PROJECTION; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PSEUDORABIES HERPETOVIRUS; RAT; SPINAL CORD; SYNAPSE;

EID: 0034175614     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.20-07-02731.2000     Document Type: Article

References (65)

1. Abercrombie M (1946) Estimation of nuclear populations from microtome sections. Anat Rec 94:239-247.
2. Aleksandrov VG, Bagaev VA, Nozdrachev AD, Panteleev SS (1996) Identification of gastric related neurones in the rat insular cortex. Neurosci Lett 216:5-8.
3. Bartha A (1961) Experimental reduction of virulence of Aujeszky's disease virus. Magy Allotorv Lapja 16:42-45.
4. Bernston GG, Sarter M, Cacioppo JT (1998) Anxiety and cardiovascular reactivity: the basal forebrain cholinergic link. Behav Brain Res 94:225-248.
5. Card JP (1995) Pseudorabies virus replication and assembly in the rodent central nervous system. In: Viral vectors (Kaplitt MG, Loewy AD, eds), pp 319-347. Orlando, FL: Academic.
6. Card JP (1998) Practical considerations for the use of pseudorabies virus in transneuronal studies of neural circuitry. Neurosci Biobehav Rev 22:685-694.
7. Card JP, Enquist LW (1995) Neurovirulence of pseudorabies virus. Crit Rev Neurobiol 9:137-162.
8. Card JP, Rinaman L, Schwaber JS, Miselis RR, Whealy ME, Robbins AK, Enquist LW (1990) Neurotropic properties of pseudorabies virus: uptake and transneuronal passage in the rat central nervous system. J Neurosci 10:1974-1994.
9. Card JP, Rinaman L, Lynn RB, Lee B-H, Meade RP, Miselis RR, Enquist LW (1993) Pseudorabies virus infection of the rat central nervous system: ultrastructural characterization of viral replication, transport, and pathogenesis. J Neurosci 13:2515-2539.
10. Card JP, Dubin JR, Whealy ME, Enquist LW (1995) Influence of infectious dose upon productive replication and transynaptic passage of pseudorabies virus in rat central nervous system. J Neurovirol 1:349-358.
11. Card JP, Enquist LW, Moore RY (1999) Neuroinvasiveness of pseudorabies virus injected intracerebrally is dependent on viral concentration and terminal field density. J Comp Neurol 407:438-452.
12. Crestani F, Lorez M, Baer K, Essrich C, Benke D, Laurent JP, Belzung C, Fritschy JM, Luscher B, Mohler H (1999) Decreased GABAA-receptor clustering results in enhanced anxiety and a bias for threat cues. Nat Neurosci 2:833-839.
13. Cunningham MG, McKay RDG (1993) A hypothermic miniaturized stereotaxic instrument for surgery in newborn rats. J Neurosci Methods 47:105-114.
14. Danielsen EH, Magnuson DJ, Gray TS (1989) The central amygdaloid nucleus innervation of the dorsal vagal complex in rat: a Phaseolus vulgaris leucoagglutinin lectin anterograde tracing study. Brain Res Bull 22:705-715.
15. Enquist LW, Card JP (1996) Pseudorabies virus: a tool for tracing neuronal connections. In: Protocols for gene transfer in neuroscience: towards gene therapy of neurological disorders (Lowenstein PR, Enquist LW, eds), pp 333-348. Chichester, UK: Wiley.
16. Enquist LW, Husak PJ, Banfield BW, Smith GA (1999) Infection and spread of alphaherpesviruses in the nervous system. Adv Virus Res 51:237-347.
17. Ferguson AV, Marcus P, Spencer J, Wallace JL (1988) Paraventricular nucleus stimulation causes gastroduodenal mucosal necrosis in the rat. Am J Physiol 255:R861-R865.
18. Francis J, Hernandez LL, Powell DA (1981) Lateral hypothalamic lesions: effects on Pavlovian cardiac and cyeblink conditioning in the rabbit. Brain Res Bull 6:155-163.
19. Gray TS, Magnuson DJ (1987) Neuropeptide neuronal efferents from the bed nucleus of the stria terminalis and central amygdaloid nucleus to the dorsal vagal complex in the rat. J Comp Neurol 262:365-374.
20. Hermann GE, McCann MJ, Rogers RC (1990) Activation of the bed nucleus of the stria terminalis increases gastric motility in the rat. J Auton Nerv Syst 30:123-128.
21. Jansen ASP, Hoffman JL, Loewy AD (1997) CNS sites involved in sympathetic and parasympathetic control of the pancreas: a viral tracing study. Brain Res 766:29-38.
22. Jordan D (1990) Autonomic changes in affective behavior. In: Central regulation of autonomic functions (Loewy AD, Spyer KM, eds), pp 349-365. New York: Oxford UP.
23. Lakke EA (1997) The projections to the spinal cord of the rat during development: a timetable of descent. Adv Anat Embryol Cell Biol 135:1-143.
24. Lakke EA, Hinderink JB (1989) Development of the spinal projections of the nucleus paraventricularis hypothalami of the rat: an intra-uterine WGA-HRP study. Dev Brain Res 49:115-121.
25. Landeira-Fernandez J, Grijalva CV (1999) Gastric mucosal erosion produced by NMDA microinfusions in the lateral hypothalamus: effect of selective knife cuts. Behav Brain Res 102:51-60.
26. LeDoux JE, Iwata J, Cicchetti P, Reis DJ (1988) Different projections of the central amygdaloid nucleus mediate autonomic and behavioral correlates of conditioned fear. J Neurosci 8:2517-2529.
27. Loewy AD (1991) Forebrain nuclei involved in autonomic control. Prog Brain Res 87:253-268.
28. Loewy AD, Haxhiu MA (1993) CNS cell groups projecting to pancreatic parasympathetic preganglionic neurons. Brain Res 620:323-330.
29. Loewy AD, Spyer KM, eds (1990) Central regulation of autonomic functions. New York: Oxford UP.
30. Marchand CF, Schwab ME (1987) Binding, uptake and retrograde axonal transport of herpes virus suis in sympathetic neurons. Brain Res 383:262-270.
31. McLean IW, Nakane PK (1974) Periodate-lysine-paraformldehyde fixative. A new fixative for immunoelectron microscopy. J Histochem Cytochem 22:1077-1083.
32. Miller AJ, McKoon M, Pinneau M, Silverstein R (1983) Postnatal synaptic development of the nucleus tractus solitarius (NTS) of the rat. Dev Brain Res 8:205-213.
33. Phillips RG, Le Doux JE (1994) Lesions of the dorsal hippocampal formation interfere with background but not foreground contextual fear conditioning. Learn Mem 1:34-44.
34. Pickel VM, Bockstaele EJV, Chan J, Cestari DM (1996) GABAergic neurons in rat nuclei of solitary tracts receive inhibitory-type synapses from amygdaloid efferents lacking detectable GABA-immunoreactivity. J Neurosci Res 44:446-458.
35. Pratt JA (1992) The neuroanatomical basis of anxiety. Pharmacol Ther 55:149-181.
36. Rao H, Pio J, Kessler JP (1999) Postnatal development of synaptophysin immunoreactivity in the rat nucleus tractus solitarii and caudal ventrolateral medulla. Dev Brain Res 112:281-285.
37. Rassnick S, Enquist LW, Sved AF, Card JP (1998) Pseudorabies virus-induced leukocyte trafficking into the rat central nervous system. J Virol 72:9181-9191.
38. Rinaman L (1998) Oxytocinergic inputs to the nucleus of the solitary tract and dorsal motor nucleus of the vagus in neonatal rats. J Comp Neurol 399:101-109.
39. Rinaman L, Levitt P (1993) Establishment of vagal sensory-motor circuits during fetal development in rats. J Neurobiol 24:641-659.
40. Rinaman L, Card JP, Schwaber JS, Miselis RR (1989) Ultrastructural demonstration of a gastric monosynaptic vagal circuit in the nucleus of the solitary tract in rat. J Neurosci 9:1985-1996.
41. Rinaman L, Card JP, Enquist LW (1993) Spatiotemporal responses of astrocytes, ramified microglia, and brain macrophages to central neuronal infection with pseudorabies virus. J Neurosci 13:685-702.
42. Rinaman L, Roesch MR, Card JP (1999) Retrograde transynaptic pseudorabies virus infection of central autonomic circuits in neonatal rats. Dev Brain Res 114:207-216.
43. Rogers RC, Hermann GE (1985) Dorsal medullary oxytocin, vasopressin, oxytocin antagonist, and TRH effects on gastric acid secretion and heart rate. Peptides 6:1143-1148.
44. Rogers RC, Hermann GE (1987) Oxytocin, oxytocin antagonist, TRH, and hypothalamic paraventricular nucleus stimulation effects on gastric motility. Peptides 8:505-513.
45. Rogers RC, Hermann GE (1992) Central regulation of brainstem gastric vago-vagal control circuits. In: Neuroanatomy and physiology of abdominal vagal afferents (Ritter S, Ritter RC, Barnes CD, eds), pp 99-134. Boca Raton, FL: CRC.
46. Rogers RC, McTigue DM, Hermann GE (1995) Vagovagal reflex control of digestion: afferent modulation by neural and "endoneurocrine" factors. Am J Physiol 268:G1-G10.
47. Saper CB (1982) Convergence of autonomic and limbic connections in the insular cortex of the rat. J Comp Neurol 210:163-173.
48. Saper CB, Loewy AD, Swanson LW, Cowan WM (1976) Direct hypothalamo-autonomic connections. Brain Res 117:305-312.
49. Sawchenko PE, Brown ER, Chan RKW, Ericsson A, Li H-Y, Roland BL, Kovacs KJ (1996) The paraventricular nucleus of the hypothalamus and the functional neuroanatomy of visceromotor responses to stress. Prog Brain Res 107:201-222.
50. Schwaber JS, Kapp BS, Higgins GA, Rapp PR (1982) Amygdaloid and basal forebrain connections with the nucleus of the solitary tract and the dorsal motor nucleus. J Neurosci 2:1424-1438.
51. Shapiro RE, Miselis RR (1985) The central organization of the vagus nerve innervating the stomach of the rat. J Comp Neurol 238:473-488.
52. Smith OA, Astley CA, DeVito JL, Stein JM, Walsh RE (1980) Functional analysis of hypothalamic control of the cardiovascular responses accompanying emotional behavior. Fed Proc 29:2487-2494.
53. Stein MB (1998) Neurobiological perspectives on social phobia: from affiliation to zoology. Biol Psychiatry 44:1277-1285.
54. Swanson LW (1992) Brain maps. Structure of the rat brain. Amsterdam: Elsevier.
55. Swanson LW, Kuypers HGJM (1980) The paraventricular nucleus of the hypothalamus: cytoarchitectonic subdivisions and the organization of projections to the pituitary, dorsal vagal complex, and spinal cord as demonstrated by retrograde fluorescence double-labeling methods. J Comp Neurol 194:555-570.
56. Tache Y, Martinez, V, Million M, Rivier J (1999) Corticotropin-releasing factor and the brain-gut motor response to stress. Can J Gastroenterol 13[Suppl A]:A18-A25.
57. Takahashi N, Okumura T, Yamada H, Kohgo Y (1999) Stimulation of gastric acid secretion by centrally administered orexin-A in conscious rats. Biochem Biophys Res Commun 254:623-627.
58. Terreberry RR, Neafsay EJ (1983) Rat medial frontal cortex: a visceral motor region with a direct projection to the solitary nucleus. Brain Res 278:245-249.
59. Thompson RH, Canteras NS, Swanson LW (1996) Organization of projections from the dorsomedial nucleus of the hypothalamus: a PHA-L study in the rat. J Comp Neurol 376:143-173.
60. Van der Kooy D, Koda LK, McGinty JF, Gerfen CR, Bloom FE (1984) The organization of projections from the cortex, amygdala, and hypothalamus to the nucleus of the solitary tract in rat. J Comp Neurol 1984:1-24.
61. Vouimba RM, Garcia R, Jaffard R (1998) Opposite effects of lateral septal LTP and lateral septal lesions on contextual fear conditioning in mice. Behav Neurosci 112:875-884.
62. Watson RE, Wiegand ST, Clough RW, Hoffman GE (1986) Use of cryoprotectant to maintain long-term peptide immunoreactivity and tissue morphology. Peptides 7:155-159.
63. Yang M, Card JP, Tirabassi RS, Miselis RR, Enquist LW (1999) Retrograde, transneuronal spread of pseudorabies virus in defined neuronal circuitry of the rat brain is facilitated by gE mutations that reduce virulence. J Virol 73:4350-4359.
64. Yasui Y, Breder CD, Saper CB, Cechetto DF (1991a) Autonomic responses and efferent pathways from the insular cortex in the rat. J Comp Neurol 303:355-374.
65. Yasui Y, Itoh K, Kaneko T, Shigemoto R, Mizuno N (1991b) Topographical projections from the cerebral cortex to the nucleus of the solitary tract in the cat. Exp Brain Res 85:75-84.