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. 2020 May 12:14:126.
doi: 10.3389/fncel.2020.00126. eCollection 2020.

Dopamine Modulates Excitatory Synaptic Transmission by Activating Presynaptic D1-like Dopamine Receptors in the RA Projection Neurons of Zebra Finches

Songhua Wang  1 , Shaoyi Liu  2 , Qingqin Wang  1 , Yalun Sun  1 , Lihua Yao  3 , Dongfeng Li  2 , Wei Meng  1
Affiliations

Dopamine Modulates Excitatory Synaptic Transmission by Activating Presynaptic D1-like Dopamine Receptors in the RA Projection Neurons of Zebra Finches

Songhua Wang et al. Front Cell Neurosci. .

Abstract

Songbirds are useful vertebrate study models for vocal learning and memory. The robust nucleus of the arcopallium (RA) receives synaptic inputs from both the posterior and anterior pathways of the song control system in songbirds. Hence, RA plays an important role in the control of singing. RA receives dopaminergic (DArgic) inputs that increase the excitability of RA projection neurons (PNs). However, the effects of DA on excitatory synaptic transmission are yet to be deciphered. In this study, the effects of DA on the excitatory synaptic transmission of the PNs in the RA of adult male zebra finches were investigated using a whole-cell patch-clamp recording. We observed that DA decreased the frequency of spontaneous excitatory postsynaptic currents (sEPSCs) and miniature excitatory postsynaptic currents (mEPSCs). The effects of DA were mimicked by the D1-like DA receptor (D1R) agonist, SKF-38393, but not the D2-like DA receptor (D2R) agonist, Quinpirole. Also, the effects of DA were blocked by D1R antagonist, SCH-23390, but not the D2R antagonist, Sulpiride. These results demonstrate that DA modulates excitatory synaptic transmission by acting on D1R in the RA of adult male zebra finches.

Keywords: D1-like dopamine receptors; dopamine; excitatory synaptic transmission; the robust nucleus of the arcopallium; zebra finch.

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Figures

Figure 1
Figure 1
A simplified diagram of the song control system (Nottebohm et al., 1976). The song system consists of two major pathways. The vocal motor pathway (VMP) starts with nucleus HVC (letter-based name). HVC projects to the robust nucleus of archistriatum (RA), which innervates the tracheosyringeal part of the hypoglossal nucleus (nXIIts). The anterior forebrain pathway (AFP) starts with the projection from HVC to Area X, AreaX projects to the medial portion of the dorsolateral nucleus of the anterior thalamus (DLM), which sends its output to the lateral magnocellular nucleus of the anterior nidopallium (LMAN), then projects to RA (Ding et al., 2003). RA receives glutamatergic inputs from HVC and LMAN (Mooney and Konishi, 1991). HVC, RA, Area X, and LMAN also receive dopaminergic inputs from the ventral tegmental area (VTA) and express dopamine receptors (Kubikova and Kostál, 2010).
Figure 2
Figure 2
Effects of dopamine (DA) on spontaneous excitatory postsynaptic currents (sEPSCs) in arcopallium (RA) projection neurons (PNs). (A) Representative sample traces of sEPSCs recordings for control and DA treatment. (B) Cumulative inter-event interval (IEI) distributions for sEPSCs demonstrating that DA could increase intervals (p < 0.01). (C) Cumulative amplitude distributions for sEPSCs demonstrating that DA did not affect the amplitude of sEPSCs (p > 0.05). (D,E) DA significantly reduced the frequency but not the amplitude in RA PNs. Horizontal lines indicate median values.
Figure 3
Figure 3
Effects of DA on miniature excitatory postsynaptic currents (mEPSCs) in RA PNs. (A) Representative sample traces of mEPSCs recording from RA PNs before and after DA addition to tissue slices. (B) Cumulative IEI distribution for mEPSCs for control and DA treated samples. (C) Cumulative amplitude distributions of mEPSCs in the control and DA treated samples. DA notably increased the interval between mEPSCs events (p < 0.01) but did not affect their amplitudes (p > 0.05). (D,E) DA significantly reduced the frequency but not the amplitude in RA PNs. Horizontal lines indicate median values.
Figure 4
Figure 4
Effects of D1-like DA receptor (D1R) agonist SKF-38393 on mEPSCs in RA PNs. (A) Recordings of mEPSCs in the absence and presence of SKF38393. (B) Cumulative IEI distributions for mEPSCs in the control and after application of SKF (p < 0.01). (C) Cumulative amplitude distributions of mEPSCs in the control and after application of SKF. (D,E) SKF significantly decreased the frequency, but not the amplitude of mEPSCs in RA PNs. Horizontal lines indicate median values.
Figure 5
Figure 5
Effects of DA and D1R antagonist SCH-23390 (20 μM) on mEPSCs in RA PNs. (A) Recordings of mEPSCs in the absence and presence of SCH and DA. (B) Cumulative IEI distributions for mEPSCs in the control and after DA and SCH (p > 0.05). (C) Cumulative amplitude distributions of mEPSCs in control and after DA and SCH (p > 0.05). (D,E) DA and SCH did not affect the frequency and amplitude of mEPSCs in RA PNs. Horizontal lines indicate median values.
Figure 6
Figure 6
Effects of D2-like DA receptor (D2R) agonist quinpirole on mEPSCs in RA PNs. (A) Recordings of mEPSCs in the absence and presence of quinpirole. (B) Cumulative IEI distributions for mEPSC in the control and after addition of quinpirole (p > 0.05). (C) Cumulative amplitude distributions of mEPSCs in the control and after addition of quinpirole (p > 0.05). (D,E) Quinpirole did not affect the frequency and amplitude of mEPSCs in RA PNs. Horizontal lines indicate median values.
Figure 7
Figure 7
Effects of DA and D2R blocker, sulpiride, on mEPSCs in RA PNs. (A) Recordings of mEPSCs in the absence and presence of sulpiride and DA. (B) Cumulative distributions of IEIs for mEPSCs in the control and after addition of DA and sulpiride (p < 0.01). (C) Cumulative distributions of the amplitudes for mEPSCs in the control and after addition of DA and sulpiride (p > 0.05). (D,E) DA and sulpiride significantly decreased the frequency but not the amplitude of mEPSCs in RA PNs. Horizontal lines indicate median values.
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