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A Possible Mechanism of Learning-Evoked Reorganization of Receptive Fields in the Primary Auditory Cortex: A Role of the Basal Ganglia, Prefrontal Cortex, Hippocampus, Acetylcholine and Dopamine

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Advances in Cognitive Neurodynamics (VII) (ICCN2019 2019)

Part of the book series: Advances in Cognitive Neurodynamics ((ICCN))

Abstract

A hypothetical mechanism is advanced that determines a role of acetylcholine and dopamine in the reorganization of receptive fields (RFs) in the primary auditory cortical area A1 evoked by learning with a pure tone with a frequency F. This mechanism is based on dopamine- and acetylcholine-dependent long-term changes in the efficacy of neural connections in the auditory and limbic cortico-basal ganglia-thalamocortical loops. Dopamine, released in response to the tone F and reinforcing signal acting at D1 receptors on striatonigral cells of the dorsal striatum promotes the induction of LTP in the efficacy of inputs from A1 neurons with preferred tuning frequency (PTF) equal or close to F. As a result, basal ganglia (BG) output more strongly disinhibits neurons in the MGB with the PTF close to F, thus promoting a rise in the activity of tonotopically connected MGB and A1 neurons. Simultaneously, LTD is induced at other corticostriatal inputs, leading to inhibition of MGB and A1 neurons with PTF different from F. Voluntary attention promotes RFs narrowing due to a rise in the prefrontal cortex activity and its excitatory input to A1, as well as by dopamine-dependent disinhibition of MGB neurons by the limbic part of the BG that includes the nucleus accumbens. Hippocampus is involved in auditory processing due to its connections with the cortex and projections to the nucleus accumbens. Acetylcholine released by the basal forebrain and pedunculopontine nucleus (that is also under inhibitory control from the BG) modulates RFs due to activity reorganization in the whole network. The complex effect of acetylcholine is determined by location of muscarinic and nicotinic receptors at both pyramidal cell and GABAergic interneurons. Therefore, it depends on ACh concentration and strength of inhibition.

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Acknowledgements

This work is supported by the Russian Scientific Foundation, grant number 16-15-10403p.

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Silkis, I.G. (2021). A Possible Mechanism of Learning-Evoked Reorganization of Receptive Fields in the Primary Auditory Cortex: A Role of the Basal Ganglia, Prefrontal Cortex, Hippocampus, Acetylcholine and Dopamine. In: Lintas, A., Enrico, P., Pan, X., Wang, R., Villa, A. (eds) Advances in Cognitive Neurodynamics (VII). ICCN2019 2019. Advances in Cognitive Neurodynamics. Springer, Singapore. https://doi.org/10.1007/978-981-16-0317-4_15

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