Dopaminergic-induced changes in Mauthner cell excitability disrupt prepulse inhibition in the startle circuit of goldfish

Journal of Neurophysiology

Volumn 106, Issue 6, 2011, Pages 3195-3204

  Medan, Violeta ^a   Preuss, Thomas ^a  

^a CITY UNIVERSITY OF NEW YORK   (United States)

Author keywords

Cellular mechanisms; Dopamine; Input resistance; Sensorimotor gating; Time specific neuromodulation

Indexed keywords

APOMORPHINE; DOPAMINE; HALOPERIDOL;

ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; ATTENUATION; AUDITORY STIMULATION; CELL DISRUPTION; CELL POPULATION; CONTROLLED STUDY; DENDRITE; DOPAMINERGIC SYSTEM; GOLDFISH; IN VIVO STUDY; LATENT PERIOD; MAUTHNER CELL; NERVE CELL; NERVE CELL EXCITABILITY; NERVE CELL MEMBRANE CONDUCTANCE; NERVE CELL MEMBRANE POTENTIAL; NERVE CELL MEMBRANE STEADY POTENTIAL; NEUROMODULATION; NONHUMAN; NONLINEAR SYSTEM; POSITIVE FEEDBACK; POSTSYNAPTIC POTENTIAL; PREPULSE INHIBITION; PRIORITY JOURNAL; SENSORY STIMULATION; STARTLE REFLEX; TIME;

ACOUSTIC STIMULATION; ANALYSIS OF VARIANCE; ANIMALS; APOMORPHINE; BIOPHYSICS; DOPAMINE; DOPAMINE AGENTS; ELECTRIC STIMULATION; GOLDFISH; HALOPERIDOL; MEDULLA OBLONGATA; MEMBRANE POTENTIALS; NEURAL INHIBITION; STARTLE REACTION;

EID: 83055165916     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00644.2011     Document Type: Article

References (63)

1. Aubert L, Reiss D, Ouagazzal AM. Auditory and visual prepulse inhibition in mice: parametric analysis and strain comparisons. Genes Brain Behav 5: 423-431, 2006.
2. Bosch D, Schmid S. Cholinergic mechanism underlying prepulse inhibition of the startle response in rats. Neuroscience 155: 326-335, 2008.
3. Braff D, Stone C, Callaway E, Geyer M, Glick I, Bali L. Prestimulus effects on human startle reflex in normals and schizophrenics. Psychophysiology 15: 339-343, 1978.
4. Braff DL, Geyer MA, Light GA, Sprock J, Perry W, Cadenhead KS, Swerdlow NR. Impact of prepulse characteristics on the detection of sensorimotor gating deficits in schizophrenia. Schizophr Res 49: 171-178, 2001.
5. Braff DL, Geyer MA, Swerdlow NR. Human studies of prepulse inhibition of startle: normal subjects, patient groups, and pharmacological studies. Psychopharmacology (Berl) 156: 234-258, 2001.
6. Burgess HA, Granato M. Sensorimotor gating in larval zebrafish. J Neurosci 27: 4984-4994, 2007.
7. Cachope R, Mackie K, Triller A, O'Brien J, Pereda AE. Potentiation of electrical and chemical synaptic transmission mediated by endocannabinoids. Neuron 56: 1034-1047, 2007.
8. Campeau S, Davis M. Prepulse inhibition of the acoustic startle reflex using visual and auditory prepulses: disruption by apomorphine. Psychopharmacology (Berl) 117: 267-274, 1995.
9. Canfield JG. Temporal constraints on visually directed C-start responses: behavioral and physiological correlates. Brain Behav Evol 61: 148-158, 2003.
10. Cordova MS, Braun CB. The use of anesthesia during evoked potential audiometry in goldfish (Carassius auratus). Brain Res 1153: 78-83, 2007.
11. Davis M, Gendelman DS, Tischler MD, Gendelman PM. A primary acoustic startle circuit: lesion and stimulation studies. J Neurosci 2: 791-805, 1982.
12. Diamond J, Huxley AF. The activation and distribution of GABA and L-glutamate receptors on goldfish Mauthner neurones: an analysis of dendritic remote inhibition. J Physiol 194: 669-723, 1968.
13. Eaton RC, Lee RK, Foreman MB. The Mauthner cell and other identified neurons of the brainstem escape network of fish. Prog Neurobiol 63: 467-485, 2001.
14. Faber DS, Fetcho JR, Korn H. Neuronal networks underlying the escape response in goldfish. General implications for motor control. Ann NY Acad Sci 563: 11-33, 1989.
15. Faber DS, Korn H. Electrical field effects: their relevance in central neural networks. Physiol Rev 69: 821-863, 1989.
16. Faber DS, Korn H. Instantaneous inward rectification in the Mauthner cell: a postsynaptic booster for excitatory inputs. Neuroscience 19: 1037-1043, 1986.
17. Faber DS, Korn H. Transmission at a central inhibitory synapse. I. Magnitude of unitary postsynaptic conductance change and kinetics of channel activation. J Neurophysiol 48: 654-678, 1982.
18. Faber DS, Korn H. Unitary conductance changes at teleost Mauthner cell glycinergic synapses: a voltage-clamp and pharmacologic analysis. J Neurophysiol 60: 1982-1999, 1988.
19. Fetcho JR, Faber DS. Identification of motoneurons and interneurons in the spinal network for escapes initiated by the Mauthner cell in goldfish. J Neurosci 8: 4192-4213, 1988.
20. Frost NW, Tian L, Hoppe TA, Mongeluzi DL, Wang J. A cellular mechanism for prepulse inhibition. Neuron 40: 991-1001, 2003.
21. Fukami Y, Furukawa T, Asada Y. Excitability changes of the Mauthner cell during collateral inhibition. J Gen Physiol 48: 581-600, 1965.
22. Furshpan EJ, Furukawa T. Intracellular and extracellular responses of the several regions of the Mauthner cell of the goldfish. J Neurophysiol 25: 732-771, 1962.
23. Furukawa T. Synaptic interaction at the mauthner cell of goldfish. Prog Brain Res 21: 44-70, 1966.
24. Geyer MA, Krebs-Thomson K, Braff DL, Swerdlow NR. Pharmacological studies of prepulse inhibition models of sensorimotor gating deficits in schizophrenia: a decade in review. Psychopharmacology (Berl) 156: 117-154, 2001.
25. Gorelova N, Seamans JK, Yang CR. Mechanisms of dopamine activation of fast-spiking interneurons that exert inhibition in rat prefrontal cortex. J Neurophysiol 88: 3150-3166, 2002.
26. Graham FK. Presidential Address, 1974. The more or less startling effects of weak prestimulation. Psychophysiology 12: 238-248, 1975.
27. Hatta K, Ankri N, Faber DS, Korn H. Slow inhibitory potentials in the teleost Mauthner cell. Neuroscience 103: 561-579, 2001.
28. Hoffman HS, Ison JR. Reflex modification 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, 1980.
29. Koch C, Segev I. The role of single neurons in information processing. Nat Neurosci 3: 1171-1177, 2000.
30. Koch M. The neurobiology of startle. Prog Neurobiol 59: 107-128, 1999.
31. Korn H, Faber DS. Escape behavior-brainstem and spinal cord circuitry and function. Curr Opin Neurobiol 6: 826-832, 1996.
32. Korn H, Faber DS. The Mauthner cell half a century later: a neurobiological model for decision-making? Neuron 47: 13-28, 2005.
33. Lee RK, Finger TE, Eaton RC. GABAergic innervation of the Mauthner cell and other reticulospinal neurons in the goldfish. J Comp Neurol 338: 601-611, 1993.
34. Lin JW, Faber DS. Synaptic transmission mediated by single club endings on the goldfish Mauthner cell. II. Plasticity of excitatory postsynaptic potentials. J Neurosci 8: 1313-1325, 1988.
35. Lingenhohl K, Friauf E. Giant neurons in the rat reticular formation: a sensorimotor interface in the elementary acoustic startle circuit? J Neurosci 14: 1176-1194, 1994.
36. Ludewig K, Vollenweider FX. Impaired sensorimotor gating in schizophrenia with deficit and with nondeficit syndrome. Swiss Med Wkly 132: 159-165, 2002.
37. Mansbach RS, Geyer MA. Parametric determinants in pre-stimulus modification of acoustic startle: interaction with ketamine. Psychopharmacology (Berl) 105: 162-168, 1991.
38. Mansbach RS, Geyer MA, Braff DL. Dopaminergic stimulation disrupts sensorimotor gating in the rat. Psychopharmacology (Berl) 94: 507-514, 1988.
39. Miller EJ, Saint Marie LR, Breier MR, Swerdlow NR. Pathways from the ventral hippocampus and caudal amygdala to forebrain regions that regulate sensorimotor gating in the rat. Neuroscience 165: 601-611, 2010.
40. Neumeister H, Szabo TM, Preuss T. Behavioral and physiological characterization of sensorimotor gating in the goldfish startle response. J Neurophysiol 99: 1493-1502, 2008.
41. Pereda A, Triller A, Korn H, Faber DS. Dopamine enhances both electrotonic coupling and chemical excitatory postsynaptic potentials at mixed synapses. Proc Natl Acad Sci USA 89: 12088-12092, 1992.
42. Pereda AE, Nairn AC, Wolszon LR, Faber DS. Postsynaptic modulation of synaptic efficacy at mixed synapses on the Mauthner cell. J Neurosci 14: 3704-3712, 1994.
43. Perez MF, White FJ, Hu XT. Dopamine D2 receptor modulation of K channel activity regulates excitability of nucleus accumbens neurons at different membrane potentials. J Neurophysiol 96: 2217-2228, 2006.
44. Podda MV, Riccardi E, D'Ascenzo M, Azzena GB, Grassi C. Dopamine D1-like receptor activation depolarizes medium spiny neurons of the mouse nucleus accumbens by inhibiting inwardly rectifying K currents through a cAMP-dependent protein kinase A-independent mechanism. Neuroscience 167: 678-690, 2010.
45. Preuss T, Faber DS. Central cellular mechanisms underlying temperaturedependent changes in the goldfish startle-escape behavior. J Neurosci 23: 5617-5626, 2003.
46. Preuss T, Osei-Bonsu PE, Weiss SA, Wang C, Faber DS. Neural representation of object approach in a decision-making motor circuit. J Neurosci 26: 3454-3464, 2006.
47. Schall U, Keysers C, Kast B. Pharmacology of sensory gating in the ascending auditory system of the pigeon (Columba livia). Psychopharmacology (Berl) 145: 273-282, 1999.
48. Sickmann T, Alzheimer C. Short-term desensitization of G-protein-activated, inwardly rectifying K (GIRK) currents in pyramidal neurons of rat neocortex. J Neurophysiol 90: 2494-2503, 2003.
49. Simons-Weidenmaier NS, Weber M, Plappert CF, Pilz PK, Schmid S. Synaptic depression and short-term habituation are located in the sensory part of the mammalian startle pathway. BMC Neurosci 7: 38, 2006.
50. Swerdlow NR, Braff DL, Geyer MA, Koob GF. Central dopamine hyperactivity in rats mimics abnormal acoustic startle response in schizophrenics. Biol Psychiatry 21: 23-33, 1986.
51. Swerdlow NR, Light GA, Cadenhead KS, Sprock J, Hsieh MH, Braff DL. Startle gating deficits in a large cohort of patients with schizophrenia: relationship to medications, symptoms, neurocognition, and level of function. Arch Gen Psychiatry 63: 1325-1335, 2006.
52. Swerdlow NR, Weber M, Qu Y, Light GA, Braff DL. Realistic expectations of prepulse inhibition in translational models for schizophrenia research. Psychopharmacology (Berl) 199: 331-388, 2008.
53. Szabo TM, Weiss SA, Faber DS, Preuss T. Representation of auditory signals in the M-cell: role of electrical synapses. J Neurophysiol 95: 2617-2629, 2006.
54. Triller A, Sur C, Korn H. Heterogeneous distribution of glycinergic and GABAergic afferents on an identified central neuron. J Comp Neurol 338: 83-96, 1993.
55. Weiss SA, Preuss T, Faber DS. A role of electrical inhibition in sensorimotor integration. Proc Natl Acad Sci USA 105: 18047-18052, 2008.
56. Weiss SA, Zottoli SJ, Do SC, Faber DS, Preuss T. Correlation of C-start behaviors with neural activity recorded from the hindbrain in free-swimming goldfish (Carassius auratus). J Exp Biol 209: 4788-4801, 2006.
57. Whitaker KW, Neumeister H, Huffman LS, Kidd CE, Preuss T, Hofmann HA. Serotonergic modulation of startle-escape plasticity in an African cichlid fish: a single-cell molecular and physiological analysis of a vital neural circuit. J Neurophysiol 106: 127-137, 2011.
58. Witkowski G, Szulczyk B, Rola R, Szulczyk P. D(1) dopaminergic control of G protein-dependent inward rectifier K (GIRK)-like channel current in pyramidal neurons of the medial prefrontal cortex. Neuroscience 155: 53-63, 2008.
59. Yeomans JS, Bosch D, Alves N, Daros A, Ure RJ, Schmid S. GABA receptors and prepulse inhibition of acoustic startle in mice and rats. Eur J Neurosci 31: 2053-2061, 2010.
60. Yeomans JS, Frankland PW. The acoustic startle reflex: neurons and connections. Brain Res Brain Res Rev 21: 301-314, 1995.
61. Yeomans JS, Lee J, Yeomans MH, Steidl S, Li L. Midbrain pathways for prepulse inhibition and startle activation in rat. Neuroscience 142: 921-929, 2006.
62. Zottoli SJ. Correlation of the startle reflex and Mauthner cell auditory responses in unrestrained goldfish. J Exp Biol 66: 243-254, 1977.
63. Zottoli SJ, Newman BC, Rieff HI, Winters DC. Decrease in occurrence of fast startle responses after selective Mauthner cell ablation in goldfish (Carassius auratus). J Comp Physiol A 184: 207-218, 1999.