A primary acoustic startle pathway: Obligatory role of cochlear root neurons and the nucleus reticularis pontis caudalis

Journal of Neuroscience

Volumn 16, Issue 11, 1996, Pages 3775-3789

  Lee, Younglim ^a   López, Dolores E ^b   Meloni, Edward G ^a   Davis, Michael ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF SALAMANCA   (Spain)

Author keywords

cochlear nucleus; cochlear root neurons; compound action potential; lateral lemniscus; reticular formation; startle; ventral tegmentum

Indexed keywords

ACTION POTENTIAL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUDITORY STIMULATION; BRAIN INJURY; COCHLEA; CONTROLLED STUDY; ELECTROPHYSIOLOGY; MALE; NONHUMAN; PATHOPHYSIOLOGY; PONS RETICULAR FORMATION; PRIORITY JOURNAL; RAT; STARTLE REFLEX;

EID: 0029983622     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.16-11-03775.1996     Document Type: Article

References (83)

1. Adams LM, Geyer MA (1981) Effects of 6-hydroxydopamine lesions of locus coeruleus on startle in rats. Psychopharmacology 73:394-398.
2. Boulis NM, Kehne JH, Miserendino MID, Davis M (1990) Differential blockade of early and late components of acoustic startle following intrathecal infusion of 6-cyano-7-nitroquinoxaline-2,3-dione (CNQX) or D,L-2-amino-5-phosphonovaleric acid (AP-5). Brain Res 520:240-246.
3. Bradley MM, Lang PJ, Cuthbert BN (1993) Emotion, novelty, and the startle reflex: habituation in humans. Behav Neurosci 107:970-980.
4. Braff DL, Stone C, Callaway E, Geyer M, Click I, Bali L (1978) Prestimulus effects on human startle reflex in normals and schizophrenics. Psychophysiology 15:339-343.
5. Braff DL, Grillon C, Geyer MA (1992) Gating and habituation of the startle reflex in schizophrenic patients. Arch Gen Psychiatry 49:206-215.
6. Brown JS, Kalish HI, Farber IE (1951) Conditional fear as revealed by magnitude of startle response to an auditory stimulus. J Exp Psychol 41:317-328.
7. Cassella JV, Davis M (1986) Neural structures mediating acoustic and tactile startle reflexes and the acoustically-elicited pinna response in rats: electrolytic and ibotenic acid studies. Soc Neurosci Abstr 12:1273.
8. Cook III EW, Davis TL, Hawk LW, Spence EL, Gautier CH (1992) Fearfulness and startle potentiation during aversive stimulation. Psychophysiology 663-645.
9. Cory RN, Ison JR (1979) Persistent effect of noise on the acoustic startle reflex in the rat. Anim Learn Behav 7:367-371.
10. Davis M (1970) Effects of interstimulus length and variability on habituation of the acoustic startle reflex in the rat. J Comp Physiol Psychol 72:177-192.
11. Davis M (1974) Sensitization of the rat startle response by noise. J Comp Physiol Psychol 87:571-581.
12. Davis M (1980) Neurochemical modulation of sensory-motor reactivity: acoustic and tactile startle reflexes. Neurosci Biobehav Rev 4:241-263.
13. Davis M (1989) Sensitization of the acoustic startle reflex by footshock. Behav Neurosci 103:495-503.
14. Davis M, Astrachan DI (1978) Conditioned fear and startle magnitude: effects of different footshock or backshock intensities used in training. J Exp Psychol Anim Behav Process 4:95-103.
15. Davis M, Heninger GR (1972) Comparison of response plasticity between the eyeblink and vertex potential in humans. Electroencephalogr Clin Neurophysiol 33:283-293.
16. Davis M, Gendelman DS, Tischler MD, Gendelman PM (1982) A primary acoustic startle circuit: lesion and stimulation studies. J Neurosci 6:791-805.
17. Davis M, Falls WA, Campeau S, Kim M (1993) Fear-potentiated startle: a neural and pharmacological analysis. Behav Brain Res 58:175-198.
18. Fillon DL, Dawson ME, Schell AM (1993) Modification of the acoustic startle-reflex eyeblink: a tool for investigating early and later attentional processes. Biol Psychol 35:185-200.
19. Fox JE (1979) Habituation and prestimulus inhibition of the auditory startle reflex in decerebrate rats. Physiol Behav 23:291-297.
20. Frankland PW, Scott BW, Yeomans JS (1995) Axons and synapses mediating electrically evoked startle: collision tests and latency analysis. Brain Res 670:97-111.
21. Geyer MA, Braff DL (1987) Startle habituation and sensorimotor gating in schizophrenia and related animal models. Schizophr Bull 13:643-668.
22. Gokin AP, Karpukhina MV (1985) A study of reticular structures in cat brain involved in startle reflexes to somatic stimuli of different modalities. Neurophysiology (USSR) 17:380-390.
23. Graham F (1975) The more or less startling effects of weak prestimulus. Psychophysiology 12:238-248.
24. Grillner S, Lund S (1968) The origin of a descending pathway with monosynaptic action on flexor motoneurons. Acta Physiol Scand 74:274-284.
25. Grillner S, Honogo T, Lund S (1971) Convergent effects on alpha motoneurons from the vestibulospinal tract and a pathway descending the medial longitudinal fasciculus. Exp Brain Res 12:457-479.
26. Grillon C, Ameli R, Woods SW, Merikangas K, Davis M (1991) Fearpotentiated startle in humans: effects of anticipatory anxiety on the acoustic blink reflex. Psychophysiology 28:588-595.
27. Groves PM, Thompson RF (1970) Habituation: a dual process theory. Psycho] Rev 77:419-450.
28. Groves PM, Wilson CJ, Boyle RD (1974) Brain stem pathways, cortical modulation and habituation of the acoustic startle response. Behav Biol 10:391-418.
29. Hammond GR (1973) Lesions of pontine and medullary reticular formation and prestimulus inhibition of the acoustic startle in rats. Physiol Behav 10:239-243.
30. Harrison JM, Irving R (1965) The anterior ventral cochlear nucleus. J Comp Neurol 124:15-42.
31. Harrison JM, Warr WB (1962) A study of the cochlear nucleus and ascending auditory pathways of the medulla. J Comp Neurol 119:341-379.
32. Huffman HS, Ison JR (1980) Reflex modulation in the domain of startle. I. Some empirical findings and their implications for how the nervous system processes sensory input. Psychol Rev 87:175-189.
33. Huffman HS, Stitt C (1969) Behavioral factors in habituation of acoustic startle reactions. J Comp Physiol Psychol 68:276-279.
34. Hoffman HS, Marsh RR, Stein N (1969) Persistence of background acoustic stimulation in controlling startle. J Comp Physiol Psychol 68:280-283.
35. Ison JR (1982) Temporal acuity in auditory function in the rat: reflex inhibition by brief gaps in noise. J Comp Physiol Psychol 96:945-954.
36. Ison JR, Hammond G (1971) Modification of the startle reflex in the rat by changes in the auditory and visual environment. J Comp Physiol Psychol 75:435-452.
37. Ison JR, McAdam DW, Hammond GR (1973) Latency and amplitude changes in the acoustic startle reflex of the rat produced by variation in auditory prestimulation. Physiol Behav 10:1035-1039.
38. Jordan WP (1989) Mesencephalic reticular formation lesions made after habituation training abolish long-term habituation of the acoustic startle response in rats. Behav Neurosci 103:805-815.
39. Kandler K, Herbert H (1991) Auditory projections from the cochlear nucleus to pontine and mesencephalic reticular nuclei in the rat. Brain Res 562:230-242.
40. Klüver H, Barrera A (1953) A method for the combined staining of cells and fibres of the nervous system. J Neuropathol Exp Neurol 12:400.
41. Koch M, Lingenhöhl K, Pilz PKD (1992) Loss of the acoustic startle response following neurotoxic lesions of the caudal pontine reticular formation: possible role of giant neurons. Neuroscience 49:617-625.
42. Koch M, Kungel M, Herbert H (1993) Cholinergic neurons in the pedunculopontine tegmental nucleus are involved in the mediation of prepulse inhibition of the acoustic startle response in the rat. Exp Brain Res 97:71-82.
43. Kokkinidis L (1986) Sensitization to amphetamine and tolerance to cocaine and phenycyclidine stimulation in mice. Pharmacol Biochem Behav 25:1175-1180.
44. Korn JH, Moyer KE (1965) The effects of pre-shock and handling on the startle response in the rat. Psychon Sci 3:409-410.
45. Krase W, Koch M, Schnitzler HU (1993) Glutamate antagonists in the reticular formation reduce the acoustic startle reflex. NeuroReport 4:13-16.
46. Krase W, Koch M, Schnitzler HU (1994) Substance P is involved in the sensitization of the acoustic startle response by footshock in rats. Behav Brain Res 63:81-88.
47. Landis C, Hunt W (1939) The startle paradigm. New York: Farrar and Rinehart.
48. Lang PJ, Bradley MM, Cuthbert BN (1990) Emotion, attention, and the startle reflex. Psychol Rev 97:377-395.
49. Leaton RN (1976) Long-term retention of the habituation of lick suppression and startle response produced by a single auditory stimulus. J Exp Psychol Anim Behav Process 3:248-259.
50. Leaton RN, Supple WF (1986) Cerebellar vermis: essential for long-term habituation of the acoustic startle response. Science 232:513-515.
51. Lee Y, Davis M (1992) A primary acoustic startle circuit: lesion and anatomical tracing studies. Soc Neurosci Abstr 18:1563.
52. Leitner DS, Powers AS, Huffman HS (1980) The neural substrate of the startle response. Physiol Behav 25:291-297.
53. Lingenhöhl K, Friauf E (1992) Giant neurons in the caudal pontine reticular formation receive short latency acoustic input: an intracellular recording and HRP study in the rat. J Comp Neurol 325:473-492.
54. Lingenhöhl K, Friauf E (1994) Giant neurons in the rat reticular formation: a sensorimotor interface in the elementary acoustic startle circuit? J Neurosci 14:1176-1194.
55. Lipp OV, Sheridan J, Siddle DA (1994) Human blink startle during aversive and nonaversive Pavlovian conditioning. J Exp Psychol Anim Behav Process 20:380-389.
56. López DE, Merchán MA, Bajo VM, Saldana E (1993a) The cochlear root neurons in the rat, mouse and gerbil. In: The mammalian cochlear nuclei: organization and function (Merchán MA, ed), pp 291-301. New York: Plenum.
57. López DE, Warr WB, Sinex DG (1993b) The cochlear root neurons: first sentinels of the auditory pathway. Sixteenth ARO meeting Abstract 471.
58. Mansbach RS, Geyer MA (1991) Parametric determinants in prestimulus modification of acoustic startle: interaction with ketamine. Psychopharmacology 105:162-168.
59. Meloni EG, Davis M (1992) Anatomical connections mediating the pinna component of the acoustic startle reflex in the rat. Soc Neurosci Abstr 18:1547.
60. Merchán MA, Collía F, López DE, Saldana E (1988) Morphology of cochlear root neurons in the rat. J Neurocytol 17:711-725.
61. Miserendino MJD, Davis M (1993) NMDA and non-NMDA antagonists infused into the nucleus reticularis pontis caudalis depress the acoustic startle reflex. Brain Res 623:215-222.
62. Mller AR (1983) On the origin of the compound action potentials (N1, N2) of the cochlear of the rat. Exp Neurol 80:633-644.
63. Ornitz EM, Guthrie D, Kaplan AR, Lane SJ, Norman RJ (1986) Maturation of startle modulation. Psychophysiology 23:624-634.
64. Osen KK, López DE, Slyngstad TA, Ottersen OP, Storm-Mathisen J (1991) GABA-like and glycine-like immunoreactivities of the cochlear root nucleus in rat. J Neurocytol 20:17-25.
65. Parham K, Willott JF (1990) Effects of inferior colliculus lesions on the acoustic startle response. Behav Neurosci 104:831-840.
66. Paxinos G, Watson C (1986) The rat brain in stereotaxic coordinates. New York: Academic.
67. Pellet J (1990) Neural organization in the brainstem circuit mediating the primary acoustic head startle: an electrophysiological study in the rat. Physiol Behav 48:1-10.
68. Peterson BW (1979) Reticulospinal projection to spinal motor nuclei. Annu Rev Physiol 41:127-140.
69. Peterson BW, Pitts NO, Fukushima K (1979) Reticulospinal connections with limb and axial motoneurons. Exp Brain Res 36:1-20.
70. Prosser CL, Hunter WS (1936) The extinction of startle responses and spinal reflexes in the white rat. Am J Physiol 117:609-618.
71. Rossignol S (1973) Auditory influence on motor systems. Unpublished dissertation, McGill University.
72. Russo JM, Ison JR (1979) Sensitization of the rat's acoustic startle response by repetition of a photic stimulus. Physiol Psychol 7:102-106.
73. Spiera RF, Davis M (1988) Excitatory amino acid antagonists depress acoustic startle after infusion into the ventral nucleus of the lateral lemniscus or paralemniscal zone. Brain Res 445:130-136.
74. Swanson LW (1992) Brain maps: structure of the rat brain. New York: Elsevier.
75. Swerdlow NR, Geyer MA, Vale WW, Koob GF (1986) Corticotropin-releasing factor potentiates acoustic startle in rats: blockade by chlordiazepoxide. Psychopharmacology 88:147-152.
76. Swerdlow NR, Caine SB, Braff DL, Geyer MA (1992) The neural substrates of sensorimotor gating of the startle reflex: a review of recent findings and their implications. J Psychopharmacol 6:176-190.
77. Szabo I (1965) Analysis of the muscular action potentials accompanying the acoustic startle reaction. Acta Physiol Acad Sci Hung 27:167-178.
78. Szabo I, Hazafi K (1965) Elicitability of the acoustic startle reaction after brain stem lesions. Acta Physiol Acad Sci Hung 27:155-165.
79. Tohyama M, Sakai K, Salvert D, Touret M, Jouvet M (1979) Spinal projections from the lower brainstem in the cat as demonstrated by the horseradish technique. I. Origins of the reticulospinal tracts and their funicular trajectories. Brain Res 173:383-403.
80. Wu MF, Suzuki SS, Siegel JM (1988) Anatomical distribution and response patterns of reticular neurons in relation to acoustic startle. Brain Res 457:399-406.
81. Yeomans JS, Cochrane KA (1993) Collision-like interactions between acoustic and electrical signals that produce startle reflexes in reticular formation sites. Brain Res 320-328.
82. Yeomans JS, Rosen JB, Barbeau J, Davis M (1989) Double-pulse stimulation of startle-like responses in rats: refractory periods and temporal summation. Brain Res 486:147-158.
83. Yeomans JS, Hempek CME, Chapman CA (1993) Axons and synapses mediating startle-like responses evoked by electrical stimulation of the reticular formation in rats: symmetric and asymmetric collision effects. Brain Res 617:309-319.