Real-Time Contributions of Auditory Feedback to Avian Vocal Motor Control

Abstract

Songbirds and humans both rely critically on hearing for learning and maintaining accurate vocalizations. Evidence strongly indicates that auditory feedback contributes in real time to human speech, but similar contributions of feedback to birdsong remain unclear. Here, we assessed real-time influences of auditory feedback on Bengalese finch song using a computerized system to detect targeted syllables as they were being sung and to disrupt feedback transiently at short and precisely controlled latencies. Altered feedback elicited changes within tens of milliseconds to both syllable sequencing and timing in ongoing song. These vocal disruptions were larger when feedback was altered at segments of song with variable sequence transitions than at stereotyped sequences. As in humans, these effects depended on the feedback delay relative to ongoing song, with the most disruptive delays approximating the average syllable duration. These results extend the parallels between speech and birdsong with respect to a moment-by-moment reliance on auditory feedback. Moreover, they demonstrate that song premotor circuitry is sensitive to auditory feedback during singing and suggest that feedback may contribute in real time to the control and calibration of song.

Social Modulation of Sequence and Syllable Variability in Adult Birdsong

“…Our results extend the finding of variability regulation from syllable structure to syllable sequencing and suggest that plasticity of syllable sequencing could also be heightened during UD song. Furthermore, our results are consistent with the possibility that species differences in the intrinsic variability of syllable sequencing are correlated with differences in the plasticity of syllable sequencing in adult song; syllable sequencing in adult Bengalese finch song is more variable than in zebra finch song, and adult Bengalese finches demonstrate more rapid plasticity of sequencing following manipulations of auditory feedback than adult zebra finches (Brainard and Doupe 2001;Nordeen and Nordeen 1992;Okanoya and Yamaguchi 1997;Sakata and Brainard 2006;Scott et al 2000;Woolley and Rubel 1997).…”

“…Typically, there are 2-5 first-order transitions at branch points. For each branch point, this variability was quantified as the transition entropy transition entropy ϭ⌺Ϫp i * log 2 (p i ) where the sum is over all possible transitions, and p i is the probability of the ith transition across all songs (Gil and Slater 2000;Sakata and Brainard 2006). Branch points with transitions that are more variable (i.e., closer to uniform probability) have higher transition entropy scores.…”

“…Transitions from 'ab' to the sequences 'ab', 'ccc', and 'i', respectively, were produced 36.1, 49.6, and 14.3% of the time during UD song (n ϭ 252 transitions in 40 songs) and 66.4, 31.4, and 2.2% of the time during FD song (n ϭ 223 transitions in 33 songs). For each branch point, we characterized the variability in sequence transitions by quantifying transition entropy (Gil and Slater 2000;Sakata and Brainard 2006); stereotyped sequences have entropy scores of zero, and increased variability translates into increased entropy (see METH-ODS). This example illustrates a case in which transition entropy was reduced by 27.4% during FD song relative to UD song.…”

Neural Coding of Syntactic Structure in Learned Vocalizations in the Songbird

“…Variable song sequences of the individual birds, composed according to finite-state type syntax (Okanoya, 2004), can be described using transition diagrams (Okanoya and Yamaguchi, 1997;Sakata and Brainard, 2006;Wohlgemuth et al, 2010). As illustrated in Figure 1 A, a transition diagram consists of a finite number of nodes (circles A-J) and node-connecting arrows that indicate the identities of syllables and the possible transition directions between syllables, respectively.…”

Integrating perspectives on vocal performance and consistency

“…However, more recent studies in estrildid finches and other songbird species demonstrate that auditory feedback is crucial for the maintenance of consistent adult song and suggest that vocal practice continues to be important in adult songbirds (reviewed in Brainard and Doupe, 2000;Konishi, 2004;Leonardo and Konishi, 1999;Mooney, 2009). For example, syllable structure and sequencing rapidly degrade and become less consistent following deafening in adult zebra and Bengalese finches (Brainard and Doupe, 2001;Horita et al, 2008;Nordeen and Nordeen, 1992;Okanoya and Yamaguchi, 1997;Sakata and Brainard, 2006;Woolley and Rubel, 1997). Manipulation of auditory feedback and reinforcement signals can drive adaptive changes to song structure (Andalman and Fee, 2009;Charlesworth et al, 2011;Tumer and Brainard, 2007;Sober and Brainard, 2009;Warren et al, 2011), and urban noise alters vocal performance in numerous populations of adult songbirds (reviewed in Slabbekoom and Ripmeester, 2008).…”