Neural processing of auditory feedback during vocal practice in a songbird

Abstract

Songbirds are capable of vocal learning and communication and are ideally suited to the study of neural mechanisms of complex sensory and motor processing. Vocal communication in a noisy bird colony and vocal learning of a specific song template both require the ability to monitor auditory feedback to distinguish self-generated vocalizations from external sounds and to identify mismatches between the developing song and a memorized template acquired from a tutor. However, neurons that respond to auditory feedback from vocal output have not been found in song-control areas despite intensive searching. Here we investigate feedback processing outside the traditional song system, in single auditory forebrain neurons of juvenile zebra finches that were in a late developmental stage of song learning. Overall, we found similarity of spike responses during singing and during playback of the bird's own song, with song responses commonly leading by a few milliseconds. However, brief time-locked acoustic perturbations of auditory feedback revealed complex sensitivity that could not be predicted from passive playback responses. Some neurons that responded to playback perturbations did not respond to song perturbations, which is reminiscent of sensory-motor mirror neurons. By contrast, some neurons were highly feedback sensitive in that they responded vigorously to song perturbations, but not to unperturbed songs or perturbed playback. These findings suggest that a computational function of forebrain auditory areas may be to detect errors between actual feedback and mirrored feedback deriving from an internal model of the bird's own song or that of its tutor. Such feedback-sensitive spikes could constitute the key signals that trigger adaptive motor responses to song disruptions or reinforce exploratory motor gestures for vocal learning.

The functional role of the parieto-frontal mirror circuit: interpretations and misinterpretations

“…This interpretation is supported by a recent study showing that to understand the intentions of other people, children with ASD do not rely on the observed motor behaviour but on the semantics of the object that is being manipulated or on the context in which the motor act takes place 125 . Figure is Such motor-based understanding seems to be a primary way in which individuals relate to one another, as shown by its presence not only in humans and monkeys, but also in evolutionarily distant species, such as swamp sparrows 4 and zebra finches 5 . Furthermore, this mechanism indicates the existence of a profound natural link between individuals that is crucial for establishing inter-individual interactions.…”

“…The basic functions of these areas and centres vary considerably, from song production to the organization of goal-directed motor acts, to emotional processes. Thus, like other basic mechanisms (for example, excitatory postsynaptic potentials), the functional role of the mirror mechanism depends on its anatomical location, with its function ranging from recognition of the song of conspecifics in birds 4,5 to empathy in humans 6 .…”

Neural Correlates of the Lombard Effect in Primate Auditory Cortex

“…On the other hand, Sakata and Brainard (2008) showed that some neurons in HVC, a premotor song structure, in adult Bengalese finches responded to feedback manipulations. Another recent study, using altered feedback, demonstrated feedback sensitivity in the auditory nuclei of juvenile zebra finches including field-L, the analog of the mammalian auditory cortex (Keller and Hahnloser, 2009). Interestingly, although these auditory nuclei are feedback sensitive like the mammalian auditory cortex, their neural activity during normal song production closely parallels that during song playback and does not exhibit the same degree of prominent vocalization-induced suppression common to both humans (Crone et al, 2001;Houde et al, 2002;Flinker et al, 2010;Greenlee et al, 2011) and nonhuman primates (Eliades and Wang, 2003).…”

Evidence for a causal inverse model in an avian cortico-basal ganglia circuit

“…For example, to accurately sense the external world while simultaneously moving within it, the nervous system must be able to detect changes in its sensory inputs that are not a predictable consequence of self-motion. Indeed, many sensory neurons respond with high sensitivity to unpredictable stimuli during motor behavior despite self-caused sensory feedback (1)(2)(3)(4)(5). Such remarkable sensitivity can be achieved by circuit mechanisms that counteract sensory feedback associated with self-generated motor output (6).…”