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

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.

Stimulus-specific adaptation in the inferior colliculus: The role of excitatory, inhibitory and modulatory inputs

“…Neuromodulatory influences to the IC include those mediated by noradrenergic (Hormigo, Horta Junior Jde, Gomez-Nieto, & Lopez, 2012;Klepper & Herbert, 1991), serotoninergic (Hurley & Sullivan, 2012;Obara, Kamiya, & Fukuda, 2014;Ramsey, Sinha, & Hurley, 2010;Thompson & Thompson, 2009), dopaminergic (Gittelman, Perkel, & Portfors, 2013;Olazabal & Moore, 1989) and cholinergic projections (Schofield, 2010). The cholinergic inputs originate in the pontomesencephalic tegmentum, that includes the pedunculopontine and laterodorsal tegmental nucleus.…”

Dopaminergic projections of the subparafascicular thalamic nucleus to the auditory brainstem

“…A variety of studies have provided intriguing data suggesting that the neuromodulator dopamine plays an important role in modulating auditory responses. For example, Bender et al (2010) showed that dopamine can modulate action potential initiation in the dorsal cochlear nucleus and Gittelman et al (2013) showed that dopamine heterogeneously modulates response properties of neurons in the inferior colliculus (IC). Moreover, people with Parkinson’s disease and schizophrenia, both disorders characterized by a dysfunction in dopamine signaling, have speech processing problems (Gräber et al, 2002; Schröder et al, 2010; Kantrowitz et al, 2015) and people with schizophrenia may experience auditory hallucinations (Lennox et al, 2000).…”

Catecholaminergic connectivity to the inner ear, central auditory, and vocal motor circuitry in the plainfin midshipman fish porichthys notatus

“…Thus, DAergic and/or NAergic input may function to alter temporal encoding and frequency discrimination in a complex naturalistic sound field (see Hurley et al, 2004). Recently, Gittelman et al (2013) demonstrated both excitatory and inhibitory DA modulation of auditory responses in IC of mice and there is evidence for NE-induced suppression of IC neuronal response in the bat (Hurley et al, 2004). Less is known about behavioral implications of CA action in the auditory midbrain although manipulating DA receptor activation in IC of rats disrupts acoustic startle-mediated prepulse inhibition (Satake et al, 2012).…”