Abstract
Rationale: Adult rats emit ultrasonic vocalizations (USVs) at around 50-kHz; these commonly occur in contexts that putatively engender positive affect. While several reports indicate that dopaminergic (DAergic) transmission plays a role in the emission of 50-kHz calls, the pharmacological evidence is mixed. Different modes of dopamine (DA) release (i.e., tonic and phasic) could potentially explain this discrepancy.Objective: To investigate the potential role of phasic DA release in 50-kHz call emission.Methods: In Experiment 1, USVs were recorded in adult male rats following unexpected electrical stimulation of the medial forebrain bundle (MFB). In parallel, phasic DA release in the nucleus accumbens (NAcc) was recorded using fast-scan cyclic voltammetry. In Experiment 2, USVs were recorded following response-contingent or non-contingent optogenetic stimulation of midbrain DAergic neurons. Four 20-s schedules of optogenetic stimulation were used: fixed-interval, fixed-time, variable-interval, and variable-time.Results: Brief electrical stimulation of the MFB increased both 50-kHz call rate and phasic DA release in the NAcc. During optogenetic stimulation sessions, rats initially called at a high rate comparable to that observed following reinforcers such as psychostimulants. Although optogenetic stimulation maintained reinforced responding throughout the 2-h session, the call rate declined to near zero within the first 30 min. The trill call subtype predominated following both electrical and optical stimulation.Conclusion: The occurrence of electrically-evoked 50-kHz calls, time-locked to phasic DA (Experiment 1), provides correlational evidence supporting a role for phasic DA in USV production. However, in Experiment 2, the temporal dissociation between calling and optogenetic stimulation of midbrain DAergic neurons suggests that phasic mesolimbic DA release is not sufficient to produce 50-kHz calls. The emission of the trill subtype of 50-kHz calls potentially provides a marker distinguishing positive affect from positive reinforcement.
Highlights
Adult rats produce two categories of ultrasonic vocalizations (USVs; Portfors, 2007; Clarke and Wright, 2015): 22-kHz and 50-kHz (30–90 kHz)
A variety of dopaminergic (DAergic) manipulations alter the rate at which adult rats emit 50-kHz calls (Burgdorf et al, 2000, 2001, 2007; Williams and Undieh, 2010; Brudzynski et al, 2012; Simola et al, 2014); in particular, DAergic transmission in the nucleus accumbens (NAcc) appears both necessary and sufficient for call emission, as evidenced by studies using DA-targeted lesions and intracerebral microinjection of DAergic drugs (Burgdorf et al, 2001, 2007)
We and others have found that both amphetamine (AMPH)induced and spontaneous 50-kHz vocalizations are profoundly inhibited by systemically-administered D1 and D2 antagonists (Scardochio and Clarke, 2013; Wright et al, 2013; Wöhr et al, 2015)
Summary
Adult rats produce two categories of ultrasonic vocalizations (USVs; Portfors, 2007; Clarke and Wright, 2015): 22-kHz (range: 20–30 kHz) and 50-kHz (30–90 kHz). Calls in both categories are thought to play a role in communication (for review see: Seffer et al, 2014). Some DAergic drugs have produced unexpected effects after systemic administration: (1) direct DAergic agonists inhibited 50-kHz calling across a wide dose range (Scardochio and Clarke, 2013), and (2) the DA transporter blocker GBR 12909 failed to mimic AMPH’s stimulatory effect on 50-kHz call emission, even when combined with a noradrenaline transporter blocker (Wright et al, 2013)
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