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Dopamine Modulates Auditory Responses in the Inferior Colliculus in a Heterogeneous Manner

  • Joshua X. Gittelman
  • David J. Perkel
  • Christine V. PortforsEmail author
Research Article

Abstract

Perception of complex sounds such as speech is affected by a variety of factors, including attention, expectation of reward, physiological state, and/or disorders, yet the mechanisms underlying this modulation are not well understood. Although dopamine is commonly studied for its role in reward-based learning and in disorders, multiple lines of evidence suggest that dopamine is also involved in modulating auditory processing. In this study, we examined the effects of dopamine application on neuronal response properties in the inferior colliculus (IC) of awake mice. Because the IC contains dopamine receptors and nerve terminals immunoreactive for tyrosine hydroxylase, we predicted that dopamine would modulate auditory responses in the IC. We recorded single-unit responses before, during, and after the iontophoretic application of dopamine using piggyback electrodes. We examined the effects of dopamine on firing rate, timing, and probability of bursting. We found that application of dopamine affected neural responses in a heterogeneous manner. In more than 80 % of the neurons, dopamine either increased (32 %) or decreased (50 %) firing rate, and the effects were similar on spontaneous and sound-evoked activity. Dopamine also either increased or decreased first spike latency and jitter in almost half of the neurons. In 3/28 neurons (11 %), dopamine significantly altered the probability of bursting. The heterogeneous effects of dopamine observed in the IC of awake mice were similar to effects observed in other brain areas. Our findings indicate that dopamine differentially modulates neural activity in the IC and thus may play an important role in auditory processing.

Keywords

mouse iontophoresis midbrain D2 receptors 

Notes

Acknowledgments

We thank Zachary Mayko for help with data collection. This work was supported by National Science Foundation grant no. IOS-0920060 to CVP.

References

  1. Adams J (1979) Ascending projections to the inferior colliculus. J Comp Neurol 183:519–538PubMedCrossRefGoogle Scholar
  2. Adams J, Mugnaini E (1984) Dorsal nucleus of the lateral lemniscus: a nucleus of GABAergic projection neurons. Brain Res Bull 13:585–590PubMedCrossRefGoogle Scholar
  3. Allen PD, Ison JR (2010) Sensitivity of the mouse to changes in azimuthal sound location: angular separation, spectral composition, and sound level. Behav Neurosci 124:265–277PubMedCrossRefGoogle Scholar
  4. Allen PD, Ison JR (2012) Kcna1 gene deletion lowers the behavioral sensitivity of mice to small changes in sound location and increases asynchronous brainstem auditory evoked potentials but does not affect hearing thresholds. J Neurosci 32:2538–2543PubMedCrossRefGoogle Scholar
  5. Aragona BJ, Liu Y, Curtis JT, Stephan FK, Wang Z (2003) A critical role for nucleus accumbens dopamine in partner-preference formation in male prairie voles. J Neurosci 23:3483–3490PubMedGoogle Scholar
  6. Bamford NS, Robinson S, Palmiter RD, Joyce JA, Moore C, Meshul CK (2004) Dopamine modulates release from corticostriatal terminals. J Neurosci 24:9541–9552PubMedCrossRefGoogle Scholar
  7. Bender KJ, Uebele VN, Renger JJ, Trussell LO (2012) Control of firing patterns through modulation of axon initial segment T-type calcium channels. J Physiol 590:109–118PubMedGoogle Scholar
  8. Braff D, Stone C, Callaway E, Geyer M, Glick I, Bali L (1978) Prestimulus effects on human startle reflex in normals and schizophrenics. Psychophysiology 15:339–343PubMedCrossRefGoogle Scholar
  9. Brunso-Bechtold JK, Thompson GC, Masterton RB (1981) HRP study of the organization of auditory afferents ascending to central nucleus of inferior colliculus in cat. J Comp Neurol 197:705–722PubMedCrossRefGoogle Scholar
  10. Calabresi P, Mercuri NB, Sancesario G, Bernardi G (1993) Electrophysiology of dopamine-denervated striatal neurons. Brain 116:433–452PubMedCrossRefGoogle Scholar
  11. Charlier TD, Ball GF, Balthazart J (2005) Sexual behavior activates the expression of the immediate early genes c-fos and Zenk (egr-1) in catecholaminergic neurons of male Japanese quail. Neuroscience 131:13–30PubMedCrossRefGoogle Scholar
  12. Drescher MJ, Drescher DG, Khan KM, Hatfield JS, Ramakrishnan NA, Abu-Hamdan MD, Lemonnier LA (2006) Pituitary adenylyl cyclase-activating polypeptide (PACAP) and its receptor (PAC1-R) are positioned to modulate afferent signaling in the cochlea. Neuroscience 142:139–164PubMedCrossRefGoogle Scholar
  13. Flagel SB, Clark JJ, Robinson TE, Mayo L, Czuj A, Willuhn I, Akers CA, Clinton SM, Phillips PE, Akil H (2011) A selective role for dopamine in stimulus-reward learning. Nature 469:53–57PubMedCrossRefGoogle Scholar
  14. Frisina D, Walton J, Lynch-Armour M, Klotz D (1998) Inputs to a physiologically characterized region of the inferior colliculus of the young adult CBA mouse. Hear Res 115:61–81PubMedCrossRefGoogle Scholar
  15. Gáborján A, Lendvai B, Vizi ES (1999) Neurochemical evidence of dopamine release by lateral olivo- cochlear efferents and its presynaptic modulation in guinea-pig cochlea. Neuroscience 90:131–138PubMedCrossRefGoogle Scholar
  16. Gale SD, Perkel DJ (2010) A basal ganglia pathway drives selective auditory responses in songbird dopaminergic neurons via disinhibition. J Neurosci 30:1027–1037PubMedCrossRefGoogle Scholar
  17. Gittelman JX, Wang L, Colburn HS, Pollak GD (2012) Inhibition shapes response selectivity in the inferior colliculus by gain modulation. Front Neural Circ 6:67Google Scholar
  18. Gonzalez-Hernandez T, Mantolan-Sarmiento B, Gonzalez-Gonzalez B, Perez-Gonzalez H (1996) Sources of GABAergic input to the inferior colliculus of the rat. J Comp Neurol 372:309–326PubMedCrossRefGoogle Scholar
  19. Goodson JL, Kabelik D, Kelly AM, Rinaldi J, Klatt JD (2009) Dopamine-beta-hydroxylase and tyrosine hydroxylase immunoreactive neurons in the human brainstem. Proc Natl Acad Sci 106:8737–8742PubMedCrossRefGoogle Scholar
  20. Govindaiah G, Wang Y, Cox CL (2010) Dopamine enhances the excitability of somatosensory thalamocortical neurons. Neuroscience 170:981–991PubMedCrossRefGoogle Scholar
  21. Havey D, Caspary DM (1980) A simple technique for constructing piggy-back multibarrel micro-electrodes. Electroencephalogr Clin Neurophysiol 45:249–251Google Scholar
  22. Higley MJ, Sabatini BL (2010) Competitive regulation of synaptic Ca2+ influx by D2 dopamine and A2A adenosine receptors. Nat Neurosci 13:958–966PubMedCrossRefGoogle Scholar
  23. Holmstrom L, Eeuwes LB, Roberts PD, Portfors CV (2010) Efficient encoding of vocalizations in the auditory midbrain. J Neurosci 30:802–819PubMedCrossRefGoogle Scholar
  24. Hormigo S, Horta Júnior Jde A, Gómez-Nieto R, López DE (2012) The selective neurotoxin DSP-4 impairs the noradrenergic projections from the locus coeruleus to the inferior colliculus in rats. FrontNeural Circ 6:41Google Scholar
  25. Ison JR, Allen PD (2012) Deficits in responding to brief noise offsets in Kcna1 −/− mice reveal a contribution of this gene to precise temporal processing seen previously only for stimulus onsets. J Assoc Res Otolaryngol 13:351–358PubMedCrossRefGoogle Scholar
  26. Khurana S, Remme MW, Rinzel J, Golding NL (2011) Dynamic interaction of Ih and IK-LVA during trains of synaptic potentials in principal neurons of the medial superior olive. J Neurosci 31:8936–8947PubMedCrossRefGoogle Scholar
  27. Kitahama K, Sakamoto N, Jouvet A, Nagatsu I, Pearson J (1996) Dopamine-beta-hydroxylase and tyrosine hydroxylase immunoreactive neurons in the human brainstem. J Chem Neuroanat 10:137–146PubMedCrossRefGoogle Scholar
  28. Koch U, Grothe B (2003) Hyperpolarization-activated current (Ih) in the inferior colliculus: distribution and contribution to temporal processing. J Neurophysiol 90:3679–3687PubMedCrossRefGoogle Scholar
  29. Kubikova L, Kostál L (2010) Dopaminergic system in birdsong learning and maintenance. J Chem Anatomy 39:112–123Google Scholar
  30. Kubikova L, Wada K, Jarvis ED (2010) Dopamine receptors in a songbird brain. J Comp Neurol 518:741–769PubMedCrossRefGoogle Scholar
  31. Kulesza RJ, Spirou GA, Berrebi AS (2003) Physiological response properties of neurons in the superior paraolivary nucleus of the rat. J Neurophysiol 89:2299–2312PubMedCrossRefGoogle Scholar
  32. Leblois A, Wendel BJ, Perkel DJ (2010) Striatal dopamine modulates basal ganglia output and regulates social context-dependent behavioral variability through D1 receptors. J Neurosci 30:5730–5743PubMedCrossRefGoogle Scholar
  33. Li L, Korngut LM, Frost BJ, Beninger RJ (1998) Prepulse inhibition following lesions of the inferior colliculus: prepulse intensity functions. Physiol Behav 65:133–139PubMedCrossRefGoogle Scholar
  34. Lobarinas E, Hayes SH, Allman BL (2013) The gap-startle paradigm for tinnitus screening in animal models: limitations and optimization. Hear Res 295:150–160PubMedCrossRefGoogle Scholar
  35. Maia T, Frank MJ (2011) From reinforcement learning models to psychiatric and neurological disorders. Nat Neurosci 14:154–162PubMedCrossRefGoogle Scholar
  36. Maison SF, Liu XP, Eatock RA, Sibley DR, Grandy DK, Liberman MC (2012) Dopaminergic signaling in the cochlea: receptor expression patterns and deletion phenotypes. J Neurosci 32:344–355PubMedCrossRefGoogle Scholar
  37. Mayko ZM, Roberts PD, Portfors CV (2012) Inhibitory microcircuitry shapes selectivity to vocalizations in the inferior colliculus. Front Neurosci 6:73Google Scholar
  38. Metzger RR, Greene NT, Porter KK, Groh JM (2006) Effects of reward and behavioral context on neural activity in the primate inferior colliculus. J Neurosci 26:7468–7476PubMedCrossRefGoogle Scholar
  39. Michaeli A, Yaka R (2010) Dopamine inhibits GABA(A) currents in ventral tegmental area dopamine neurons via activation of presynaptic g-protein coupled inwardly-rectifying potassium channels. Neuroscience 165:1159–1169PubMedCrossRefGoogle Scholar
  40. Muniak MM, Mayko ZM, Ryugo DK, Portfors CV (2012) Preparation of an awake mouse for recording neural responses and injecting tracers. J Vis Exp 64(e3755):1–7Google Scholar
  41. Nicola SM, Surmeier DJ, Malenka RC (2000) Dopaminergic modulation of neuronal excitability in the striatum and nucleus accumbens. Annu Rev Neurosci 23:185–215PubMedCrossRefGoogle Scholar
  42. Orio P, Parra A, Madrid R, Gonzalez O, Belmonte C, Viana F (2012) Role of Ih in the firing pattern of mammalian cold thermoreceptor endings. J Neurophysiol 108:3009–3023PubMedCrossRefGoogle Scholar
  43. Paxinos G, Franklin K (2001) The mouse brain in stereotaxic coordinates, 2nd edn. Academic, San DiegoGoogle Scholar
  44. Perez MF, White FJ, Hu XT (2006) Dopamine D(2) receptor modulation of K(+) channel activity regulates excitability of nucleus accumbens neurons at different membrane potentials. J Neurophysiol 96:2217–2228PubMedCrossRefGoogle Scholar
  45. Phillips PE, Stuber GD, Heien ML, Wightman RM, Carelli RM (2003) Subsecond dopamine release promotes cocaine seeking. Nature 422:614–618PubMedCrossRefGoogle Scholar
  46. Portfors CV, Roberts PD, Jonson K (2009) Over-representation of species-specific vocalizations in the awake mouse inferior colliculus. Neuroscience 162:486–500PubMedCrossRefGoogle Scholar
  47. Ramanathan S, Tkatch T, Atherton JF, Wilson CJ, Bevan MD (2008) D2-like dopamine receptors modulate SKCa channel function in subthalamic nucleus neurons through inhibition of Cav2.2 channels. J Neurophysiol 999:442–459CrossRefGoogle Scholar
  48. Rinne T, Balk MH, Koistinen S, Autti T, Alho K, Sams M (2008) Auditory selective attention modulates activation of human inferior colliculus. J Neurophysiol 100:3323–3327PubMedCrossRefGoogle Scholar
  49. Rosenberger MH, Fremouw T, Casseday JH, Covey E (2003) Expression of the Kv1.1 ion channel subunit in the auditory brainstem of the big brown bat, Eptesicus fuscus. J Comp Neurol 462:101–120PubMedCrossRefGoogle Scholar
  50. Ruel J, Nouvian R, Gervais d’Aldin C, Pujol R, Eybalin M, Puel JL (2001) Dopamine inhibition of auditory nerve activity in the adult mammalian cochlea. Eur J Neurosci 14:977–986PubMedCrossRefGoogle Scholar
  51. Saint Marie R, Ostapoff RM, Morest D, Wenthold R (1989) Glycine-immunoreactive projection of the cat lateral superior olive: possible role in midbrain ear dominance. J Comp Neurol 279:382–396PubMedCrossRefGoogle Scholar
  52. Sasaki A, Sotnikova TD, Gainetdinov RR, Jarvis ED (2006) Social context-dependent singing-related dopamine. J Neurosci 35:9010–9014CrossRefGoogle Scholar
  53. Satake S, Yamada K, Melo LL, Barbosa Silva R (2012) Effects of microinjections of apomorphine and haloperidol into the inferior colliculus on prepulse inhibition of the acoustic startle reflex in rat. Neurosci Lett 509:60–63PubMedCrossRefGoogle Scholar
  54. Schultz W (2010) Dopamine signals for reward value and risk: basic and recent data. Behav Brain Funct 6:24PubMedCrossRefGoogle Scholar
  55. Schultz W (2013) Updating dopamine reward signals. Curr Opin Neurobiol 23:229–238PubMedCrossRefGoogle Scholar
  56. Schultz W, Dayan P, Montague PR (1997) A neural substrate of prediction and reward. Science 275:1593–1599PubMedCrossRefGoogle Scholar
  57. Sivaramakrishnan S, Oliver DL (2001) Distinct K currents result in physiologically distinct cell types in the inferior colliculus of the rat. J Neurosci 21:2861–2877PubMedGoogle Scholar
  58. Surmeier DJ, Carrillo-Reid L, Bargas J (2011) Dopaminergic modulation of striatal neurons, circuits and assemblies. Neuroscience 198:3–18PubMedCrossRefGoogle Scholar
  59. Swerdlow NR, Weber M, Qu Y, Light GA, Braff DL (2008) Realistic expectations of prepulse inhibition in translational models for schizophrenia research. Psychopharmacology (Berlin) 199:331–388CrossRefGoogle Scholar
  60. Tan ML, Theeuwes HP, Feenstra L, Borst JG (2007) Membrane properties and firing patterns of inferior colliculus neurons: an in vivo patch-clamp study in rodents. J Neurophysiol 98:443–453PubMedCrossRefGoogle Scholar
  61. Tierney PL, Thierry AM, Glowinski J, Deniau JM, Gioanni Y (2008) Dopamine modulates temporal dynamics of feedforward inhibition in rat prefrontal cortex in vivo. Cereb Cortex 18:2251–2262PubMedCrossRefGoogle Scholar
  62. Tobin AE, Calabrese RL (2005) Myomodulin increases Ih and inhibits the Na/K pump to modulate bursting in leech heart interneurons. J Neurophysiol 94:3938–3950PubMedCrossRefGoogle Scholar
  63. Tong L, Altschuler RA, Holt AG (2005) Tyrosine hydroxylase in rat auditory midbrain: distribution and changes following deafness. Hear Res 206:28–41PubMedCrossRefGoogle Scholar
  64. Trantham-Davidson H, Neely LC, Lavin A, Seamans JK (2004) Mechanisms underlying differential D1 versus D2 dopamine receptor regulation of inhibition in prefrontal cortex. J Neurosci 24:10652–10659PubMedCrossRefGoogle Scholar
  65. Turner JG, Brozoski TJ, Bauer CA, Parrish JL, Myers K, Hughes LF, Caspary DM (2006) Gap detection deficits in rats with tinnitus: a potential novel screening tool. Behav Neurosci 120:188–195PubMedCrossRefGoogle Scholar
  66. Vandecasteele M, Glowinski J, Deniau JM, Venance L (2008) Chemical transmission between dopaminergic neuron pairs. Proc Natl Acad Sci 105:4904–4909PubMedCrossRefGoogle Scholar
  67. Wamsley JK, Gehlert DR, Filloux FM, Dawson TM (1989) Comparison of the distribution of D-1 and D-2 dopamine receptors in the rat brain. J Chem Neuroanat 2:119–137PubMedGoogle Scholar
  68. Weiner DM, Levey AI, Sunahara RK, Niznik HB, O’Dowd BF, Seeman P, Brann MR (1991) D1 and D2 dopamine receptor mRNA in rat brain. Proc Natl Acad Sci 88:1859–1863PubMedCrossRefGoogle Scholar
  69. Willott JF (1986) Effects of aging, hearing loss, and anatomical location on thresholds of inferior colliculus neurons in C57Bl/6 and CBA mice. J Neurophysiol 56:391–408PubMedGoogle Scholar
  70. Winer J, Schreiner C (2005) The inferior colliculus. Springer, New YorkCrossRefGoogle Scholar
  71. Xie R, Gittelman JX, Li N, Pollak GD (2008) Whole cell recordings of intrinsic properties and sound-evoked responses from the inferior colliculus. Neuroscience 154:245–256PubMedCrossRefGoogle Scholar

Copyright information

© Association for Research in Otolaryngology 2013

Authors and Affiliations

  • Joshua X. Gittelman
    • 1
  • David J. Perkel
    • 2
    • 3
    • 4
  • Christine V. Portfors
    • 1
    Email author
  1. 1.School of Biological SciencesWashington State UniversityVancouverUSA
  2. 2.Department of BiologyUniversity of WashingtonSeattleUSA
  3. 3.Department of Otolaryngology—Head and Neck SurgeryUniversity of WashingtonSeattleUSA
  4. 4.The Virginia Merrill Bloedel Hearing Research CenterUniversity of WashingtonSeattleUSA

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