Precise auditory–vocal mirroring in neurons for learned vocal communication

“Thus, for example, when a songbird or whale sings, it strings together species-specific notes into phrases that, together, provide information on individual, population and species identity (e.g., Prather et al. 2008; Suzuki et al. 2006).”

“In particular, HVC(X) neurons (HVC neurons that project to Area X, see Figure 1) are selectively responsive to the bird’s own or a conspecific’s song [65,66].”

“HVCAFP) are active during singing and in response to song playback [30,31], their singing-related activity is unaffected by DAF [31,32].”

“, 2000; Long and Fee, 2008), and HVC neurons are active during both singing and hearing song (Prather et al., 2008; Yu and Margoliash, 1996).”

“Mirror neurons also exist in HVC of songbirds; these neurons fire at a precise time in the song, both when the bird sings the song and when it hears a similar song produced by another bird (Prather et al., 2008).”

“HVCX Neurons HVCX neurons typically burst only at specific times during song [23–26] and are thought to provide an efference copy of motor commands to song basal ganglia (area X).”

“Error bars indicate standard error of the mean. are phylogenetically most ancient species where mirror neurons are discovered in forebrain (Prather et al., 2008; Keller and Hahnloser, 2009; Giret et al., 2014).”

“…that exhibit BOS auditory preferences also display song-related pre-motor activity (Mooney, 2000; Rosen and Mooney, 2003) an attribute that has received new interest due to its similarities to the properties of “mirror neurons” in primates (Prather et al., 2008; Striedter and Charvet, 2008).”

“Mirror neurons responsive to both the production and perception of song have also been found in the forebrain of the swamp sparrow [54].”

“For example, HVC neurons in juvenile zebra finches show auditory related responses to both tutor song and the bird’s own song during waking states early in development (Nick and Konishi, 2005) and recordings from HVC in Bengalese finches, starlings and several species of sparrows reveal auditory responses that are sel…”

“5) (Prather et al., 2008).”

“In certain conditions (sleep and anesthesia), projection neurons within HVC can produce patterned activity elicited by the playback of the bird’s own song (BOS) (Lewicki, 1996; Mooney, 2000; Prather et al., 2008; Amador et al., 2013; Hamaguchi et al., 2014), indicating that sensory input can affect the motor system by…”

“For instance, in the case of syllable-length identification by songbirds, the goal of the underlying neural circuit is the determination of how the length of a syllable compares to a fixed value ( Prather et al., 2008 ).”

“chain (or parallel chains) than by a single long chain encoding multiple syllables (36).”

“The HVC neurons projecting to Area X burst very sparsely, many generating a single highly reliable burst of spikes at one or a few specific moments in the song (Kozhevnikov and Fee, 2007; Prather et al., 2008; Fujimoto et al., 2011; Figure 2D).”

“…Brainard (2008) observed significant and consistent responses to feedback perturbation in the vocal premotor nucleus HVC, but several other studies did not observe responses to feedback perturbation in HVC or other song system nuclei (Kozhevnikov and Fee 2007; Leonardo 2004; Prather et al. 2008).”

“georgiana), it has been reported that HVC projection neurons repeat their spiking pattern when a syllable is being repeated [19].”

“Recordings in freely behaving songbirds showed that a subset of a specific class of HVC neurons (those projecting to song nucleus Area X) are similarly active both during singing and BOS playback (Fujimoto et al., 2011; Prather et al., 2008).”

“If so, this functionality is not uniquely human as mirror neurons have also been described in swamp sparrows as identical neural responses while singing or listening to their own or similar songs [24 ].”

“In songbirds, MNs for vocalization have been localized through single-cell recording in the high vocal center (HVC) song nucleus, a premotor area necessary for learning and voluntary control of songs (Prather et al., 2008).”

“This system can be regarded as the core neural mechanism of associative and mimetic forms of culture – at least in primates; mirror neurons have been identified in the swamp sparrow (Prather et al., 2008), but an action recognition system remains to be characterized in birds.”

“been identified in the HVC that are activated in both auditory and motor contexts, with exquisite syllable-level precision [76].”

“’’ Since their discovery in macaques, similar (audio-motor) mirroring mechanisms have been reported in songbirds, possibly reflecting socially driven sensorimotor learning.(9) An extensive amount of work has suggested that the mirror neuron network could play a role in the development of key cognitive functions.”

“Specifically, HVCX activity associated with a focal syllable varies depending on the identity of the syllable preceding and following the focal syllable (Fujimoto et al. 2011; Prather et al. 2008).”

“Perhaps some of these cells—particularly those with reliable firing—will later express motor patterns of activity mirroring juvenile auditory patterns of response to tutor song (Prather et al. 2008).”

“…can occur in single brain areas and even in single neurons, as exemplified by neurons that show traces of either sensory responses or motor signals depending on the behavioral state or neuron type (Cardin and Schmidt 2004; Dave and Margoliash 2000; Keller and Hahnloser 2009; Prather et al. 2008).”

“, 1996), a range of evidence has demonstrated that similar phenomena of action mirroring occur also in other animal species (e.g., Keller and Hahnloser, 2009; Prather et al., 2008), including humans (e.”

“Both types of projection neurons are active at specific time points during singing renditions (8, 20, 33).”

“Mirror neurons in HVC project to a portion of the striatum involved in song learning (Area X) and are hypothesized to be important for young birds to improve their song as they practice (23, 28, 38).”

“Vocal learning and maintenance in songbirds is dramatically disrupted by deafening or other hearing impairments [11,12,13,14], leading to the view that vocal learning requires the integration of auditory feedback with vocal/motor commands [15].”

“Experiments by Mooney and Prather (2005) on the HVC network structure revealed projections from HVCRA to HVCX via HVCI and divergent connections from HVCI to HVCRA and HVCX.”

“…activity of the AFP output neurons, and of neurons in the sensorimotor nucleus HVC that provide input to the AFP (i.e., HVCAFP neurons), is insensitive to peripheral disruption of auditory feedback (Hessler and Doupe, 1999a; Kozhevnikov and Fee, 2007; Leonardo, 2004; Prather et al., 2008).”

“A spike raster for a standard single run of the network is shown in Fig 3a.”

“argued that HVC may provide a motor-based prediction of auditory feedback [68], based on the observation that HVC sequences in adult birds are reactivated during exposure to the bird’s own song, and building on previous ideas that HVC may be involved in computing an internal prediction or ‘efference copy’ of auditory…”

“HVC of zebra finches also contains mirror neurons involved in vocal production/perception [70], but whether a similar mechanism is also used for manipulating (food) objects with the beak remains to be elucidated.”

“Certain HVC PNs display complex properties, including sensorimotor mirroring and auditory selectivity for songs, syllables, or syllable combinations, consistent with the idea that, as a population, HVC neurons encode song and syllable representations (McCasland and Konishi, 1981; Margoliash, 1983; Lewicki and Konishi,…”

“In the anterior pathway, some neurons respond to both singing and hearing, which is indicative of the mirror neuron functionality (Prather et al. 2008) fundamental to imitation-mediated learning (Rizzolatti & Craighero 2004).”

“Mirror neurons, first characterized in pre-motor cortex (2, 3) then PPC (4) in monkeys, and later reported in humans (5) and birds (6), respond reliably both when an individual performs a specific action and when they observe the same action performed by a conspecific.”

“…finches show that HVC neurons projecting to the AFP (i.e., HVC AFP cells) display motor-related activity, the pattern of which is highly similar to auditory activity evoked in these same cells when the bird is quietly listening to the same song played through an audio speaker (Prather et al. 2008).”

“Recently, Prather et al. (2008) observed a group of motor neurons in the swamp sparrow forebrain that fired along with the auditory note sequences in the sparrow’s repertoire, and on a similar note, the song sequences of other birds.”

“…speech system, the same neurons that are responsible for the control of behavior are also responsive to the sensory stimuli associated with the behavior (i.e., the sound of one’s own voice) (Rizzolatti and Craighero, 2004; Prather et al., 2008; Sakata and Brainard, 2008; Edwards et al., 2010).”

“As Pazzaglia notes, songbirds do have mirror-like neurons (Prather et al. 2008) but here we tap the general discussion (H241–244) of whether vocal learning in humans arose much as it did for songbirds, with semantics being the uniquely human sequel, or whether human evolution was “semantics first,” with vocal learning…”

“Today, neurons with mirroring properties have been reported also in marmosets (Suzuki et al., 2015) and song birds (Prather et al., 2008; Keller and Hahnloser, 2009), demonstrating the pervasive nature of such sensory-evoked neural activity in motor pathways across the phylogenetic line.”

“However, several studies in awake swamp sparrows (Melospiza georgiana) have demonstrated significant electrophysiological responsiveness in song system nuclei, including the HVC [37,38,39].”

“DOI: 10.7554/eLife.18205 2 of 18 selective, sparse-firing neurons recently described in the high-level auditory area, NCM (Schneider and Woolley, 2013), as well as in the auditory-motor association area, HVC (high vocal center) (Prather et al., 2008).”

“The linearity of the Hamming distance makes it easier to separate patterns in instantaneously trained neural networks [6–8 , 13 The role of unary coding in biology has become clear in the study of avian birdsong production [1–3, 5 , 9– 11].”

“Prather et al. (2008) identified auditory–motor mirror neurons in the songbird with properties similar to the visual-motor mirror neurons first observed in the monkey frontal cortex (Rizzolatti and Craighero 2004).”

“between singing-related and auditory-evoked activity [12,25].”

“In addition, the HVC neurons that project to Area X do not distinguish between hearing and production of the BOS in the mature adult (Prather et al. 2008), which suggests that the HVC neural signal driven by BOS auditory playback may be sensorimotor, as opposed to purely sensory, in nature.”

“However, responses to conspecific song in HVC and downstream in a basal ganglia circuit suggested that HVC may also serve an important perceptual role, possibly by comparing conspecific vocalizations with vocal motor corollary discharge (Prather et al., 2008).”

“…and timing (Andalman et al. 2011; Ashmore et al. 2005; Basista et al. 2014; Fujimoto et al. 2011; Hahnloser et al. 2002; Kosche et al. 2015; Long and Fee 2008; Long et al. 2010; Prather et al. 2008; Sakata and Brainard 2008; Schmidt 2003; Vu et al. 1994; Wang et al. 2008; Yu and Margoliash 1996).”

“…crayfish (Krasne and Bryan, 1973), the auditory sensory system in crickets (Poulet and Hedwig, 2003, 2006), the vocal-auditory system of songbirds (Prather et al., 2008), the vestibular system in monkeys (Roy and Cullen, 2001; Cullen and Minor, 2002; Brooks and Cullen, 2013), and the human…”

“In the highthreshold regime, model neurons were BOS selective, and during BOS presentation they fired sparsely and were hyperpolarized on average, all very much like HVC mirror neurons that project to Area X (HVCX neurons): HVCX neurons are hyperpolarized by playback of the BOS and produce a high frequency burst in re…”

“An efference copy of HVC activation is thought to be involved in auditory feedback controlled song learning (e.g., Troyer & Doupe, 2000; Prather et al., 2008; Mooney, 2009; Bolhuis, Okanoya & Scharff, 2010; Brainard & Doupe, 2013; Fee, 2014).”