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.
The zebra finch (ZF) and the Bengalese finch (BF) are animal models that have been commonly used for neurobiological studies on vocal learning. Although they largely share the brain structure for vocal learning and production, BFs produce more complex and variable songs than ZFs, providing a great opportunity for comparative studies to understand how animals learn and control complex motor behaviors. Here, we performed a comparative study between the two species by focusing on intrinsic motivation for non-courtship singing (“undirected singing”), which is critical for the development and maintenance of song structure. A previous study has demonstrated that ZFs dramatically increase intrinsic motivation for undirected singing when singing is temporarily suppressed by a dark environment. We found that the same procedure in BFs induced the enhancement of intrinsic singing motivation to much smaller degrees than that in ZFs. Moreover, unlike ZFs that rarely sing in dark conditions, substantial portion of BFs exhibited frequent singing in darkness, implying that such “dark singing” may attenuate the enhancement of intrinsic singing motivation during dark periods. In addition, measurements of blood corticosterone levels in dark and light conditions provided evidence that although BFs have lower stress levels than ZFs in dark conditions, such lower stress levels in BFs are not the major factor responsible for their frequent dark singing. Our findings highlight behavioral and physiological differences in spontaneous singing behaviors of BFs and ZFs and provide new insights into the interactions between singing motivation, ambient light, and environmental stress.
Songbirds, such as zebra finches, spontaneously produce many song renditions for vocal practice even in the absence of apparent recipients throughout their lives. Such “undirected singing” is driven by intrinsic motivation, which arises within individuals for internal satisfaction without immediate external rewards. Intrinsic motivation for undirected singing in adult zebra finches was previously demonstrated to be critically regulated by dopamine through D2 receptors. Here, we further investigate the mechanisms of intrinsic motivation for undirected singing by focusing on endocannabinoids, which modulate dopamine signaling and contribute to motivation and reward in mammals. In songbirds, endocannabinoids have been shown to be involved in the production of undirected songs, but whether they are involved in the intrinsic motivation for undirected singing remains unknown. Using latencies of the first song production following temporary singing suppression as a measure of intrinsic motivation for undirected singing, we demonstrate that systemic administration of the direct cannabinoid agonist WIN55212-2 decreases intrinsic motivation for singing and that those effects are largely reversed by the cannabinoid antagonist SR141716A co-administered with WIN55212-2. Administration of SR141716A alone or that of two indirect cannabinoid agonists did not significantly affect intrinsic singing motivation. These results suggest that endocannabinoids are critically involved in regulating intrinsic motivation for undirected singing and provide new insights into the neural mechanisms of intrinsically motivated motor behaviors.
Many songbirds learn to produce songs through vocal practice in early life and continue to produce many renditions of learned songs daily throughout their lifetime. While it is well-known that adult songbirds sing as part of a mating ritual, additional functions of their singing behavior are not fully understood. Here, we demonstrate that adult singing outside the reproductive contexts functions to prevent passive changes in song performance. Using a reversible behavioral manipulation, we suppressed the daily singing behavior of adult zebra finches produced in the solo context for two weeks and examined its effect on song performance. We found that singing suppression significantly decreases the pitch of song elements and both amplitude and duration of song motifs. This suggests that adult song is not acoustically stable without singing and that adult birds maintain their song performance by daily singing. Moreover, suppression-induced changes in song structure were substantially recovered within two weeks of free singing even in deafened birds. Thus, the recovery of song performance does not necessarily require auditory feedback but rather is caused predominantly by singing behavior per se (i.e., the physical act of singing). Finally, unlike the auditory feedback-dependent song plasticity previously reported, passive song changes caused by singing suppression were not significantly dependent on age. Our findings demonstrate that adult songbirds maintain song performance by preventing passive song changes through the physical act of daily singing outside the reproductive contexts throughout life. Such daily singing presumably functions as vocal training to maintain the neural and/or muscular system for song production in optimal conditions to make the best song performance in reproductive contexts.
Many songbirds learned to produce songs through vocal practice in early life and continue to sing these songs daily throughout their lifetime. While it is well-known that adult songbirds sing as part of their mating rituals, the functions of singing behavior outside of reproductive contexts remain unclear. Here, we tested the hypothesis that adult singing outside of reproductive contexts may serve to prevent passive changes in song performance. We found that suppressing daily singing for two weeks altered the acoustic and temporal structure of song, and that the song structure substantially recovered within two weeks of free singing. These reversible song changes were not dependent on auditory feedback or the age of the birds, contrasting with the adult song plasticity that has been reported previously. These results demonstrate that adult song structure is not stable without daily singing in non-reproductive contexts, and suggest that adult songbirds maintain song performance by preventing passive song changes through the physical act of daily singing throughout their life. Such daily singing likely functions as vocal training to maintain the song production system in optimal conditions for song performance in reproductive contexts, similar to how human singers and athletes practice daily to maintain their performance.
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