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Fast transmission from the dopaminergic ventral midbrain to the sensory cortex of awake primates

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Abstract

Motivated by the increasing evidence that auditory cortex is under control of dopaminergic cell structures of the ventral midbrain, we studied how the ventral tegmental area and substantia nigra affect neuronal activity in auditory cortex. We electrically stimulated 567 deep brain sites in total within and in the vicinity of the two dopaminergic ventral midbrain structures and at the same time, recorded local field potentials and neuronal discharges in cortex. In experiments conducted on three awake macaque monkeys, we found that electrical stimulation of the dopaminergic ventral midbrain resulted in short-latency (~35 ms) phasic activations in all cortical layers of auditory cortex. We were also able to demonstrate similar activations in secondary somatosensory cortex and superior temporal polysensory cortex. The electrically evoked responses in these parts of sensory cortex were similar to those previously described for prefrontal cortex. Moreover, these phasic responses could be reversibly altered by the dopamine D1-receptor antagonist SCH23390 for several tens of minutes. Thus, we speculate that the dopaminergic ventral midbrain exerts a temporally precise, phasic influence on sensory cortex using fast-acting non-dopaminergic transmitters and that their effects are modulated by dopamine on a longer timescale. Our findings suggest that some of the information carried by the neuronal discharges in the dopaminergic ventral midbrain, such as the motivational value or the motivational salience, is transmitted to auditory cortex and other parts of sensory cortex. The mesocortical pathway may thus contribute to the representation of non-auditory events in the auditory cortex and to its associative functions.

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Acknowledgments

The authors thank Dr. Jörg Stadler for MRI measurements and Drs. Eike Budinger, Nikolaos Aggelopoulos, and Daniel Zaldivar for valuable suggestions on the manuscript. The work was supported by the Deutsche Forschungsgemeinschaft (DFG, SFB 779), the federal state of Saxony-Anhalt and the European Regional Development Fund (ERDF 2007–2013) and the Russian Science Foundation (RSCF 14-28-00229).

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Authors and Affiliations

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

    Judith Mylius, Ying Huang & Michael Brosch

  2. Department Systems Physiology of Learning, Leibniz Institute for Neurobiology, Brenneckestraße 6, 39118, Magdeburg, Germany

    Max F. K. Happel

  3. Institute of Psychology, Russian Academy of Sciences, Yaroslavskaya Street 13, 129366, Moscow, Russia

    Alexander G. Gorkin

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

    Henning Scheich

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

    Henning Scheich & Michael Brosch

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  1. Judith Mylius
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  2. Max F. K. Happel
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  3. Alexander G. Gorkin
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Correspondence to Judith Mylius.

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Mylius, J., Happel, M.F.K., Gorkin, A.G. et al. Fast transmission from the dopaminergic ventral midbrain to the sensory cortex of awake primates. Brain Struct Funct 220, 3273–3294 (2015). https://doi.org/10.1007/s00429-014-0855-0

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