Intrinsic motivation for singing in songbirds is enhanced by temporary singing suppression and regulated by dopamine

Abstract

Behaviors driven by intrinsic motivation are critical for development and optimization of physical and brain functions, but their underlying mechanisms are not well studied due to the complexity and autonomy of the behavior. Songbirds, such as zebra finches, offer a unique opportunity to study neural substrates of intrinsic motivation because they spontaneously produce many renditions of songs with highly-quantifiable structure for vocal practice, even in the absence of apparent recipients (“undirected singing”). Neural substrates underlying intrinsic motivation for undirected singing are still poorly understood partly because singing motivation cannot be easily manipulated due to its autonomy. Also, undirected singing itself acts as an internal reward, which could increase singing motivation, leading to difficulty in measuring singing motivation independent of singing-associated reward. Here, we report a simple procedure to easily manipulate and quantify intrinsic motivation for undirected singing independent of singing-associated reward. We demonstrate that intrinsic motivation for undirected singing is dramatically enhanced by temporary suppression of singing behavior and the degree of enhancement depends on the duration of suppression. Moreover, by examining latencies to the first song following singing suppression as a measure of singing motivation independent of singing-associated reward, we demonstrate that intrinsic singing motivation is critically regulated by dopamine through D2 receptors. These results provide a simple experimental tool to manipulate and measure the intrinsic motivation for undirected singing and illustrate the importance of zebra finches as a model system to study the neural basis of intrinsically-motivated behaviors.

Contribution of Endocannabinoids to Intrinsic Motivation for Undirected Singing in Adult Zebra Finches

“…Birds were housed individually in sound-attenuating chambers (MC-050, Muromachi Kikai) under a 14:10 h light:dark cycle throughout the experiments. Undirected songs, which the birds spontaneously produced in a solo context, were recorded as previously reported ( Kim et al, 2021 ). Briefly, the output from a microphone (PRO35, Audio-Technica) positioned above the cage was amplified using a mixer (402-VLZ4, Mackie) and digitized via an audio interface (Octa-Capture UA-1010, Roland) at 44.1 kHz (16-bit).…”

“…Intrinsic motivation for undirected singing was quantified by measuring the latency of the first song produced following the temporal suppression of singing (“first song latency”) ( Kim et al, 2021 ). Singing was suppressed by turning off the light in the sound-attenuating chambers for 1 or 2 h depending on the drugs administered (see below), and the time interval from the offset of the lights-out (LO) period to the onset of the first song was measured.…”

“…We have previously demonstrated that the intrinsic motivation for undirected singing in adult zebra finches is critically regulated by dopamine through D2 receptors ( Kim et al, 2021 ). In mammals, dopamine signaling is modulated by endocannabinoids ( El Khoury et al, 2012 ; Wenzel and Cheer, 2018 ) and they play a critical role in motivation for voluntary behaviors, such as social play and physical exercise ( Muguruza et al, 2019 ; Parsons and Hurd, 2015 ; Vanderschuren et al, 2016 ).…”

“…To better understand the role of endocannabinoids in undirected singing, we examined whether they are critically involved in intrinsic singing motivation. To quantify the motivation for undirected singing, we used the latency to the first song following the temporary suppression of singing (referred to as “first song latency”), a measure recently developed and described in our previous work ( Kim et al, 2021 ). Unlike the singing rate and song amount, the first song latency is not directly influenced by any process following the act of singing, allowing for examination of intrinsic singing motivation independent of singing-associated reward.…”

“…We systemically administered WIN and SR as in a previous study that examined their effects on undirected song production ( Soderstrom and Johnson, 2001 ), and examined their effects on the first song latency to determine the role of the endocannabinoid system in intrinsic singing motivation. We additionally examined the effects of these drugs on the mean singing rates measured over a 30-min period starting at the first song after singing suppression (“initial singing rate”), which can reflect both intrinsic singing motivation and singing-associated reward ( Kim et al, 2021 ). Moreover, we assessed the effects of two indirect cannabinoid agonists, URB597 and VDM11, on undirected singing, both of which have been shown to enhance intrinsically motivated social play in adolescent rats ( Manduca et al, 2014 ; Trezza and Vanderschuren, 2009 , 2008a , 2008b ).…”