A Lightweight, Headphones-based System for Manipulating Auditory Feedback in Songbirds

Abstract

Experimental manipulations of sensory feedback during complex behavior have provided valuable insights into the computations underlying motor control and sensorimotor plasticity 1 . Consistent sensory perturbations result in compensatory changes in motor output, reflecting changes in feedforward motor control that reduce the experienced feedback error. By quantifying how different sensory feedback errors affect human behavior, prior studies have explored how visual signals are used to recalibrate arm movements 2,3 and auditory feedback is used to modify speech production [4][5][6][7] . The strength of this approach rests on the ability to mimic naturalistic errors in behavior, allowing the experimenter to observe how experienced errors in production are used to recalibrate motor output.Songbirds provide an excellent animal model for investigating the neural basis of sensorimotor control and plasticity 8,9 . The songbird brain provides a well-defined circuit in which the areas necessary for song learning are spatially separated from those required for song production, and neural recording and lesion studies have made significant advances in understanding how different brain areas contribute to vocal behavior [9][10][11][12] . However, the lack of a naturalistic error-correction paradigm -in which a known acoustic parameter is perturbed by the experimenter and then corrected by the songbird -has made it difficult to understand the computations underlying vocal learning or how different elements of the neural circuit contribute to the correction of vocal errors 13 .The technique described here gives the experimenter precise control over auditory feedback errors in singing birds, allowing the introduction of arbitrary sensory errors that can be used to drive vocal learning. Online sound-processing equipment is used to introduce a known perturbation to the acoustics of song, and a miniaturized headphones apparatus is used to replace a songbird's natural auditory feedback with the perturbed signal in real time. We have used this paradigm to perturb the fundamental frequency (pitch) of auditory feedback in adult songbirds, providing the first demonstration that adult birds maintain vocal performance using error correction 14 . The present protocol can be used to implement a wide range of sensory feedback perturbations (including but not limited to pitch shifts) to investigate the computational and neurophysiological basis of vocal learning. Video LinkThe video component of this article can be found at http://www.jove.com/video/50027/ ProtocolImplementing the headphones system consists of four major steps. Section 1 below details the assembly of the headphones frame, which houses the electronics (speakers and a miniaturized microphone). Section 2 describes how the frame is attached to the bird. Section 3 describes the assembly of the electronics. Section 4 explains how the electronics are connected to sound-processing and data-collection hardware and details a procedure for testing that the system is functioning...

The Effects of Pitch Shifts on Delay-Induced Changes in Vocal Sequencing in a Songbird

“…Miniature, lightweight headphones were custom-built out of lightweight carbon fiber and custom-fitted to each bird’s head (Hoffmann et al, 2012). A condenser microphone in the bird’s cage (Fig.…”

“…As described in detail below, auditory feedback conditions included a null condition in which no manipulation was introduced, a DAF condition in which auditory feedback was delayed by 175 ms, or a DAF+PS condition in which both a 175-ms delay and an upward or downward pitch shift were applied simultaneously. As detailed previously, the sound-processing hardware relayed the online acoustic signal to the headphones with a minimal delay (i.e., when auditory feedback was not being intentionally delayed) of ∼10 ms, a delay which does not in itself evoke any measurable changes in vocal behavior (Sober and Brainard, 2009; Hoffmann et al, 2012; Kelly and Sober, 2014). Note that subjects might receive some unmanipulated auditory feedback via bone conduction, although such a scenario is very unlikely to account for our results (see Discussion).…”

“…Although the effects of auditory feedback delays on song have been tested previously using song-triggered playbacks of previously recorded songs, technical challenges have prevented the use of continuous delayed feedback. We overcame this obstacle using miniaturized headphones (see Methods), which provided continuous, delayed feedback in real time (Hoffmann et al, 2012). Experimental conditions included a null condition (no delay or pitch manipulation), delayed auditory feedback (DAF) without any pitch shift, and a condition in which auditory feedback was both delayed and pitch shifted (DAF+PS).…”

Variations on a theme: Songbirds, variability, and sensorimotor error correction

“…To perform this study, we took advantage of a new technique that uses lightweight headphones to introduce arbitrary errors to a songbird’s auditory feedback in real time (Hoffmann et al, 2012). As shown in Figure 1a, as the bird sang, sound-processing hardware was used to manipulate the acoustic signal, which was then played through speakers inside the headphones with a total processing delay of <10 msec.…”

Dopamine depletion affects vocal acoustics and disrupts sensorimotor adaptation in songbirds

“…Since the cell bodies of dopaminergic 69 neurons in VTA/SNc that innervate Area X are intermingled with those projecting to the rest of 70 the songbird basal ganglia (Person et al, 2008), we injected 6-OHDA directly into Area X to 71 avoid introducing general motor or song production deficits. We fitted the birds with custom-72 built headphones through which we introduced a shift in pitch (either upwards or downwards) of 73 the bird's auditory feedback (Sober and Brainard, 2009;Hoffmann et al, 2012) to measure how 74 birds changed their pitch over time in response to this induced sensory error and how self-guided 75 error correction was affected by dopamine manipulations.…”