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Tonic effects of the dopaminergic ventral midbrain on the auditory cortex of awake macaque monkeys

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Abstract

This study shows that ongoing electrical stimulation of the dopaminergic ventral midbrain can modify neuronal activity in the auditory cortex of awake primates for several seconds. This was reflected in a decrease of the spontaneous firing and in a bidirectional modification of the power of auditory evoked potentials. We consider that both effects are due to an increase in the dopamine tone in auditory cortex induced by the electrical stimulation. Thus, the dopaminergic ventral midbrain may contribute to the tonic activity in auditory cortex that has been proposed to be involved in associating events of auditory tasks (Brosch et al. Hear Res 271:66–73, 2011) and may modulate the signal-to-noise ratio of the responses to auditory stimuli.

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References

  • Adachi YU, Yamada S, Satomoto M, Higuchi H, Watanabe K, Kazama T (2005) Isoflurane anesthesia induces biphasic effect on dopamine release in the rat striatum. Brain Res Bull 67:176–181

    Article  CAS  PubMed  Google Scholar 

  • Amunts KPM, Hilbig H, Zilles K (2012) Auditory system: cyto-, myelo-, and receptorarchitecture of the auditory cortex. In: Mai JK, Paxinos G (eds) The human nervous system, 3rd edn. Elsevier Academic Press, San Diego, pp 1257–1287

    Google Scholar 

  • Arsenault JT, Nelissen K, Jarraya B, Vanduffel W (2013) Dopaminergic reward signals selectively decrease fMRI activity in primate visual cortex. Neuron 77:1174–1186

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Arsenault JT, Rima S, Stemmann H, Vanduffel W (2014) Role of the primate ventral tegmental area in reinforcement and motivation. Curr Biol CB 24:1347–1353

    Article  CAS  PubMed  Google Scholar 

  • Atzori M, Kanold PO, Pineda JC, Flores-Hernandez J, Paz RD (2005) Dopamine prevents muscarinic-induced decrease of glutamate release in the auditory cortex. Neuroscience 134:1153–1165

    Article  CAS  PubMed  Google Scholar 

  • Bao S, Chan VT, Merzenich MM (2001) Cortical remodelling induced by activity of ventral tegmental dopamine neurons. Nature 412:79–83

    Article  CAS  PubMed  Google Scholar 

  • Bao S, Chan VT, Zhang LI, Merzenich MM (2003) Suppression of cortical representation through backward conditioning. Proc Natl Acad Sci USA 100:1405–1408

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Berger B, Gaspar P, Verney C (1991) Dopaminergic innervation of the cerebral cortex: unexpected differences between rodents and primates. Trends Neurosci 14:21–27

    Article  CAS  PubMed  Google Scholar 

  • Brosch M, Schulz A, Scheich H (1999) Processing of sound sequences in macaque auditory cortex: response enhancement. J Neurophysiol 82:1542–1559

    CAS  PubMed  Google Scholar 

  • Brosch M, Selezneva E, Scheich H (2011) Formation of associations in auditory cortex by slow changes of tonic firing. Hear Res 271:66–73

    Article  PubMed  Google Scholar 

  • Carr DB, Sesack SR (2000) GABA-containing neurons in the rat ventral tegmental area project to the prefrontal cortex. Synapse 38:114–123

    Article  CAS  PubMed  Google Scholar 

  • Durstewitz D, Seamans JK (2008) The dual-state theory of prefrontal cortex dopamine function with relevance to catechol-o-methyltransferase genotypes and schizophrenia. Biol Psychiatry 64:739–749

    Article  CAS  PubMed  Google Scholar 

  • Garcia-Cabezas MA, Rico B, Sanchez-Gonzalez MA, Cavada C (2007) Distribution of the dopamine innervation in the macaque and human thalamus. NeuroImage 34:965–984

    Article  PubMed  Google Scholar 

  • Gaucher Q, Edeline JM, Gourevitch B (2012) How different are the local field potentials and spiking activities? Insights from multi-electrodes arrays. J Physiol Paris 106:93–103

    Article  PubMed  Google Scholar 

  • Gaucher Q, Huetz C, Gourevitch B, Edeline JM (2013) Cortical inhibition reduces information redundancy at presentation of communication sounds in the primary auditory cortex. J Neurosci Off J Soc Neurosci 33:10713–10728

    Article  CAS  Google Scholar 

  • Gittelman JX, Perkel DJ, Portfors CV (2013) Dopamine modulates auditory responses in the inferior colliculus in a heterogeneous manner. J Assoc Res Otolaryngol JARO 14:719–729

    Article  PubMed  Google Scholar 

  • Goldman-Rakic PS, Lidow MS, Smiley JF, Williams MS (1992) The anatomy of dopamine in monkey and human prefrontal cortex. J Neural Transm Suppl 36:163–177

    CAS  PubMed  Google Scholar 

  • Gottlieb Y, Vaadia E, Abeles M (1989) Single unit activity in the auditory cortex of a monkey performing a short term memory task. Exp Brain Res 74:139–148

    Article  CAS  PubMed  Google Scholar 

  • Grace AA (1991) Phasic versus tonic dopamine release and the modulation of dopamine system responsivity: a hypothesis for the etiology of schizophrenia. Neuroscience 41:1–24

    Article  CAS  PubMed  Google Scholar 

  • Happel MF, Deliano M, Handschuh J, Ohl FW (2014) Dopamine-modulated recurrent corticoefferent feedback in primary sensory cortex promotes detection of behaviorally relevant stimuli. J Neurosci Off J Soc Neurosci 34:1234–1247

    Article  CAS  Google Scholar 

  • Huang Y, Zacharias N, König R, Brosch M, Heil P (2012) Physiological mechanisms of working memory in the auditory cortex of humans an nonhuman primates. In: Santi PA (ed) 34th ARO Meeting San Diego, California, USA, p 164

  • Jacob SN, Ott T, Nieder A (2013) Dopamine regulates two classes of primate prefrontal neurons that represent sensory signals. J Neurosci Off J Soc Neurosci 33:13724–13734

    Article  CAS  Google Scholar 

  • Kroner S, Krimer LS, Lewis DA, Barrionuevo G (2007) Dopamine increases inhibition in the monkey dorsolateral prefrontal cortex through cell type-specific modulation of interneurons. Cereb Cortex 17:1020–1032

    Article  PubMed  Google Scholar 

  • Kudoh M, Shibuki K (2006) Sound sequence discrimination learning motivated by reward requires dopaminergic D2 receptor activation in the rat auditory cortex. Learn Mem 13:690–698

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lavin A, Nogueira L, Lapish CC, Wightman RM, Phillips PE, Seamans JK (2005) Mesocortical dopamine neurons operate in distinct temporal domains using multimodal signaling. J Neurosci Off J Soc Neurosci 25:5013–5023

    Article  CAS  Google Scholar 

  • Lewis DA, Melchitzky DS, Sesack SR, Whitehead RE, Auh S, Sampson A (2001) Dopamine transporter immunoreactivity in monkey cerebral cortex: regional, laminar, and ultrastructural localization. J Comp Neurol 432:119–136

    Article  CAS  PubMed  Google Scholar 

  • Lou Y, Luo W, Zhang G, Tao C, Chen P, Zhou Y, Xiong Y (2014) Ventral tegmental area activation promotes firing precision and strength through circuit inhibition in the primary auditory cortex. Front Neural Circuits 8:25

    Article  PubMed  PubMed Central  Google Scholar 

  • Mylius J, Happel MFK, Gorkin AG, Huang Y, Scheich H, Brosch M (2014) Fast transmission from the dopaminergic ventral midbrain to the sensory cortex of awake primates. Brain Struct Funct (in press)

  • Pirot S, Godbout R, Mantz J, Tassin JP, Glowinski J, Thierry AM (1992) Inhibitory effects of ventral tegmental area stimulation on the activity of prefrontal cortical neurons: evidence for the involvement of both dopaminergic and GABAergic components. Neuroscience 49:857–865

    Article  CAS  PubMed  Google Scholar 

  • Ramayya AG, Misra A, Baltuch GH, Kahana MJ (2014) Microstimulation of the human substantia nigra alters reinforcement learning. J Neurosci Off J Soc Neurosci 34:6887–6895

    Article  CAS  Google Scholar 

  • Schicknick H, Schott BH, Budinger E, Smalla KH, Riedel A, Seidenbecher CI, Scheich H, Gundelfinger ED, Tischmeyer W (2008) Dopaminergic modulation of auditory cortex-dependent memory consolidation through mTOR. Cereb Cortex 18:2646–2658

    Article  PubMed  PubMed Central  Google Scholar 

  • Schicknick H, Reichenbach N, Smalla KH, Scheich H, Gundelfinger ED, Tischmeyer W (2012) Dopamine modulates memory consolidation of discrimination learning in the auditory cortex. Eur J Neurosci 35:763–774

    Article  PubMed  Google Scholar 

  • Seamans JK, Yang CR (2004) The principal features and mechanisms of dopamine modulation in the prefrontal cortex. Prog Neurobiol 74:1–58

    Article  CAS  PubMed  Google Scholar 

  • Silver RA (2010) Neuronal arithmetic. Nature reviews. Neuroscience 11:474–489

    CAS  PubMed  PubMed Central  Google Scholar 

  • Smith Y, Wichmann T, DeLong MR (2014) Corticostriatal and mesocortical dopamine systems: do species differences matter? Nat Rev Neurosci 15:63

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stark H, Scheich H (1997) Dopaminergic and serotonergic neurotransmission systems are differentially involved in auditory cortex learning: a long-term microdialysis study of metabolites. J Neurochem 68:691–697

    Article  CAS  PubMed  Google Scholar 

  • Tseng KY, Mallet N, Toreson KL, Le Moine C, Gonon F, O’Donnell P (2006) Excitatory response of prefrontal cortical fast-spiking interneurons to ventral tegmental area stimulation in vivo. Synapse 59:412–417

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Weis T, Puschmann S, Brechmann A, Thiel CM (2012) Effects of L-dopa during auditory instrumental learning in humans. PLoS One 7:e52504

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wilson NR, Runyan CA, Wang FL, Sur M (2012) Division and subtraction by distinct cortical inhibitory networks in vivo. Nature 488:343–348

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yamaguchi T, Wang HL, Li X, Ng TH, Morales M (2011) Mesocorticolimbic glutamatergic pathway. J Neurosci Off J Soc Neurosci 31:8476–8490

    Article  CAS  Google Scholar 

  • Yang CR, Mogenson GJ (1990) Dopaminergic modulation of cholinergic responses in rat medial prefrontal cortex: an electrophysiological study. Brain Res 524:271–281

    Article  CAS  PubMed  Google Scholar 

  • Zilles K, Palomero-Gallagher N, Grefkes C, Scheperjans F, Boy C, Amunts K, Schleicher A (2002) Architectonics of the human cerebral cortex and transmitter receptor fingerprints: reconciling functional neuroanatomy and neurochemistry. Eur Neuropsychopharmacol J Eur Coll Neuropsychopharmacol 12:587–599

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The authors thank Dr. Jonathan Lovell for excellent technical help. The work was supported by grants from the federal state of Saxony-Anhalt and the European Regional Development Fund (ERDF 2007-2013), Vorhaben: Center for Behavioral Brain Sciences (CBBS) and the Deutsche Forschungsgemeinschaft (DFG SFB779; DFG He1721/10-1).

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There are no conflicts of interest.

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Authors and Affiliations

  1. Special Laboratory Primate Neurobiology, Leibniz Institute for Neurobiology, Brenneckestraße 6, 39118, Magdeburg, Germany

    Ying Huang, Judith Mylius & Michael Brosch

  2. Emeritus Group Lifelong Learning, Leibniz Institute for Neurobiology, Brenneckestraße 6, 39118, Magdeburg, Germany

    Henning Scheich

  3. Center for Behavioral Brain Sciences, Otto-von-Guericke-University, Universitätsplatz 2, 39106, Magdeburg, Germany

    Henning Scheich & Michael Brosch

Authors
  1. Ying Huang
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  2. Judith Mylius
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  3. Henning Scheich
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  4. Michael Brosch
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Corresponding authors

Correspondence to Ying Huang or Judith Mylius.

Additional information

Y. Huang and J. Mylius contributed equally to this work.

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Huang, Y., Mylius, J., Scheich, H. et al. Tonic effects of the dopaminergic ventral midbrain on the auditory cortex of awake macaque monkeys. Brain Struct Funct 221, 969–977 (2016). https://doi.org/10.1007/s00429-014-0950-2

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  • DOI: https://doi.org/10.1007/s00429-014-0950-2

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