Dopamine Depletion Affects Vocal Acoustics and Disrupts Sensorimotor Adaptation in Songbirds

Abstract

Dopamine is hypothesized to convey error information in reinforcement learning tasks with explicit appetitive or aversive cues. However, during motor skill learning feedback signals arise from an animal’s evaluation of sensory feedback resulting from its own behavior, rather than any external reward or punishment. It has previously been shown that intact dopaminergic signaling from the ventral tegmental area/substantia nigra pars compacta (VTA/SNc) complex is necessary for vocal learning when songbirds modify their vocalizations to avoid hearing distorted auditory feedback (playbacks of white noise). However, it remains unclear whether dopaminergic signaling underlies vocal learning in response to more naturalistic errors (pitch-shifted feedback delivered via headphones). We used male Bengalese finches ( Lonchura striata var. domestica ) to test the hypothesis that the necessity of dopamine signaling is shared between the two types of learning. We combined 6-hydroxydopamine (6-OHDA) lesions of dopaminergic terminals within Area X, a basal ganglia nucleus critical for song learning, with a headphones learning paradigm that shifted the pitch of auditory feedback and compared their learning to that of unlesioned controls. We found that 6-OHDA lesions affected song behavior in two ways. First, over a period of days lesioned birds systematically lowered their pitch regardless of the presence or absence of auditory errors. Second, 6-OHDA lesioned birds also displayed severe deficits in sensorimotor learning in response to pitch-shifted feedback. Our results suggest roles for dopamine in both motor production and auditory error processing, and a shared mechanism underlying vocal learning in response to both distorted and pitch-shifted auditory feedback.

Mapping the vocal circuitry of Alston’s singing mouse with pseudorabies virus

“…Like the noradrenergic populations, these neurons are known to have roles in auditory processing (Nevue, Felix 2nd, & Portfors, 2016) as well as motor functions (Koblinger et al, 2014). Interestingly, our dopaminergic results contrast with work that emphasizes the role of dopamine in other taxa (Saravanan, Hoffmann, Jacob, Berman, & Sober, 2019;Simonyan, Horwitz, & Jarvis, 2012), in that our TH/PRV triple-labeling revealed no PRV infection in either the ventral tegmental area or the substantia nigra pars compacta (Figure 14b).…”

Unilateral vocal nerve resection alters neurogenesis in the avian song system in a region-specific manner

“…This is important for many reasons, but relevant to our findings it shows that DA modulation is a read out of the bird’s perceived vocal success based on an internally encoded, or expected, goal. Similarly, decreasing VTA activity in Area X via 6-OHDA-induced retrograde lesions of dopaminergic cells in the VTA resulted in loss of the vocal learning that is normally driven by disruptive auditory feedback in a negative reinforcement task [ 106 , 107 ]. The association between DA and encoding of altered auditory feedback was further tested via optogenetic inhibition and excitation of VTA axon terminals during singing, modulating DA in Area X. DA modulation predictably guided changes in targeted song syllable production consistent with positive and negative reinforcement of performance [ 101 ].…”

Application of the Hierarchical Bootstrap to Multi-Level Data in Neuroscience

“…However, this statement is not to say that there are no assumptions in its use. As mentioned previously, the bootstrap cannot be used on a metric that does not obey the law of large numbers (i.e., the central limit theorem) or is not linear in the probability space (e.g., depends on the product or logarithm of probabilities like entropy for example given equal weight to each syllable independent of its frequency of occurrence in the actual dataset [29] while in the experimental results analyzed here, each syllable is weighted by its frequency of occurrence due to the differences in the nature of experiments and questions being analyzed.…”