Precise auditory–vocal mirroring in neurons for learned vocal communication

“, [21]) and birds [22].”

“Evidence for this CD function was recently found in neurons in the high vocal centre (HVC) that fired with the same latency irrespective of whether the bird was actively singing or passively listenin”

“This concept has recently been proven for single neurons in the songbird brain [ 89 ].”

“Mirror neurons also exist in songbirds, in which neurons of the telecephalic nucleus HVC respond both when the bird itself sings and when it hears other birds sing [15 ] (Figure 1a) and similar neurons also exist in the bird’s auditory association region, Field L [16].”

“, 1993); and (2) The gestural mirror neuron hypothesis of language evolution (Arbib, 2005; Prather et al., 2008; Arbib, 2010).”

“more recently in birds (Prather et al. 2008); another set, much larger, concerns experiments in humans.”

“Second, neurophysiological studies in songbirds revealed another set of neurons (anatomofunctionally homologous to primates’ corticostriatal cells) that do not directly influence the motor output but exhibit audiovocal mirror properties by receiving auditory information and a corollary discharge of the motor-related a…”

“The argument that mirror neurons imply a gestural protolanguage has been further weakened by the discovery of audiovocal mirror neurons in songbirds (Prather et al., 2008).”

“The authors used zebra finches because they learn their songs by “imitating” adult tutors and because they change songs seasonally.”

“These include auditory responses in the motor pathway and AFP (Doupe, 1997; Prather et al., 2008; Sakata and Brainard, 2008), neurogenesis in HVC and Area X (Alvarez-Buylla et al., 1988; Scott and Lois, 2007), the effect of sleep on song learning and physiology (Dave and Margoliash, 2000;…”

“Obviously, manipulations that can selectively inhibit USVs without altering other postshock fear responses (currently unavailable) will be required to further test this notion of auto-conditioning, perhaps analogous to auditory mirroring hypothesized in birds [40].”

“At the neural level, the song system possesses song mirror neurons well suited to subserve learning, mimicry, and social coordination (Dave & Margoliash 2000, Fortune et al. 2011, Prather et al. 2008).”

“These songbird nuclei also feature both auditory andmotor representations, and this is thought to have significant implications for mimicking behavior and vocal learning (Prather et al., 2008).”

“In songbirds, audio-vocal MNs are located in neural circuits important for birdsong learning, and these MNs have functional properties that suggest their role in imitative learning (Keller & Hahnloser, 2009; Prather et al., 2009; Prather et al., 2008).”

“Altogether, these findings indicate that in monkeys the acoustic input reaching frontal areas might not be coupled with the motor representation of vocalizations, at difference with what occurs in other species, such as humans and songbirds [66,67,68], in which several aspects of the species-specific vocalization are…”

“It has been proposed (ChristovMoore et al., 2014, 2020; De Waal, 2008) that affective empathy is sustained by a phylogenetically ancient neural mechanism, the mirror neuron mechanism, that is shared among species (di Pellegrino et al., 1992; Prather et al., 2008; Viario et al., 2021).”

“However, experiments combining chronic recordings and DAF in both juvenile and adult songbirds indicate that the singing-related activity of HVCX neurons is insensitive to acute feedback perturbation [43 ,44].”

“Spiny neurons in Area X are inner-vated by glutamatergic HVC neurons (Farries et al. 2005a), which fi re sparsely during singing (Kozhevnikov and Fee 2007) and in response to auditory stimuli in swamp sparrows ( Melospiza georgiana ; Prather et al. 2008).”

“Mirror neurons have been discovered in monkeys (Rizzolatti et al. 1996; Rizzolatti and Sinigaglia 2010), humans (Keysers et al. 2010), and most recently in birds (Prather et al. 2008; Keller and Hahnloser 2009).”

“DOI:10.1523/JNEUROSCI.1606-11.2011 Copyright © 2011 the authors 0270-6474/11/3110023-11$15.00/0 sponse to the individual bird’s own song (BOS) playback and similar songs of other birds (Prather et al., 2008).”

“Interestingly, the HVC timing network is activated both when the bird sings and when it listens to a song (Prather et al., 2008).”

“In fact, there is evidence that a system for matching vocalization sounds and the corresponding vocal motor patterns has evolved several times among vertebrates, as neurons that activate for song perception/ production are also present in birds (Mooney, 2009; Prather et al., 2008).”

“During singing, the song premotor nucleus HVC transmits a precise timing signal to the song motor nucleus RA and to Area X (Hahnloser et al., 2002; Kozhevnikov and Fee, 2007; Prather et al., 2008; Long and Fee, 2008; Fujimoto et al., 2011).”

“Some hypotheses have emphasized the possible role of HVC (used as a proper name), a premotor cortical circuit that receives auditory inputs and also projects to Area X (Troyer and Doupe, 2000; Mooney, 2006; Prather et al., 2008; Roberts et al., 2012).”

“…and RA show patterned activity during song production (reviewed in Fee et al., 2004; Hahnloser et al., 2002; McCasland, 1987; Ölveczky et al., 2011; Prather et al., 2008; Sakata and Brainard, 2008; Sober et al., 2008; Yu and Margoliash, 1996), and perturbations of activity in HVC and RA lead to…”

“…singing finches, from regions analogous to the mammalian secondary auditory cortex, detect neurons that are similarly activated during singing and in response to song playback, consistent with their role in processing singing-related auditory feedback (Keller & Hahnloser 2009, Prather et al. 2008).”

“Various findings indicate that HVC RA neurons are a source of premotor signals that contribute to song timing and that HVC X neurons convey song motor-related information to the basal ganglia 24,35–38 , 40 .”

“Both types of PNs generate sparse and brief (5- to 10-ms) bursts of spikes reliably active at one or a few times in the song, with different neurons active at different times (Fujimoto et al., 2011; Kozhevnikov and Fee, 2007; Long et al., 2010; Prather et al., 2008).”

“example, some species such as the swamp sparrow engage in antiphonal song type-matching—selecting a song that best matches what the neighbor just sang [18].”

“Interestingly, however, HVCx neurons (those proposed as possibly connected to an MN system) but not HVCRA neurons respond robustly to bird’s own song (Prather et al., 2008), and HVCx neurons may trigger LMAN activity through disinhibitory mechanisms (see Mooney, 2004; note Doupe et al., 2004).”

“…has been identified in multimodal neurons called mirror neurons, that have now been recorded in humans (Mukamel et al., 2010), non-human primates (Gallese et al., 1996; Fogassi et al., 2005; Kraskov et al., 2009) and in non-mammalian vertebrates (Prather et al., 2008; Keller and Hahnloser, 2009).”

“…(the caudal part of the ventral hyperstriatum, HVc) in swamp sparrows revealed that neurons whose frequency discharge increased during song production were the same as those whose frequency discharge increased when the birds heard a similar song produced by a conspecific (Prather et al. 2008).”

“These neurons, described in primates and birds (Prather et al., 2008), not only fire for a particular movement performed by the animal (e.”

“It is not clear how thecommunicative variants are learned socially, although vocal learning in birds is known to involve dedicated neural circuits (Prather et al. 2008).”

“The work by Mooney and coworkers ([33], see also [34]) clearly demonstrates that, in songbirds, areas involved in song production and learning (i.”

“This is the more plausible, as mirror neurons have recently been found in birds (Prather et al. 2008).”

“…singing-related activity of HVC neurons providing input to area X is not acutely affected by auditory-feedback perturbations, these same neurons are active during identical portions of BOS regardless of whether the bird is singing or hearing them (Kozhevnikov and Fee, 2007; Prather et al., 2008).”

“However, the singing-related action potential activity of HVCX cells does not change when auditory feedback is masked by noise bursts (Kozhevnikov and Fee, 2007; Prather et al., 2008).”

“As such, mirror neurons likely play a role in acquiring motor skill (Cooper, Cook, Dickinson, & Heyes, 2013; Prather et al., 2008; Tchernichovski & Wallman, 2008).”

“It is the same neurons in the song system that can switch, within seconds, from premotor to auditory responses of very similar patterns (Prather et al., 2008).”

“for song production and perception (Brenowitz, 1991; Gentner et al., 2000; Long and Fee, 2008; Prather et al., 2008).”

“The idea that vocal perception and production at least in part share the same neural system has been supported by work on both humans (Fadiga et al., 2002; Watkins, Strafella & Paus, 2003; D’Ausilio et al., 2014) and songbirds (Prather et al., 2008).”

“Aspects of such a system are seen in the song learning systems of some birds in which neurons fire during listening and producing songs (Prather et al. 2008).”

“However, the singing-related activity of these cells is unperturbed by acoustic manipulations that disrupt auditory feedback, suggesting that HVCX cells switch from auditory to purely motor-related activity as the bird transitions from listening to singing [38,57].”

“We examined the auditory responses of HVC neurons in our laboratory-raised birds to determine whether those cells expressed stronger responses to songs in the bird’s adult repertoire than to other swamp sparrow songs, as reported for wild sparrows (Margoliash and Konishi, 1985; Margoliash, 1986; Mooney et al., 2001; P…”

“In birds, Prather, Peters, Nowicki, and Mooney (2008) demonstrated that mirror-like neurons in the higher vocal center of swamp sparrows display nearly identical patterns of activity when the bird either hears a birdsong or sings it in the absence of auditory feedback.”

“Although beyond the scope of this review, such mirror neurons have also been observed in songbirds (Prather et al., 2008).”

“The premotor area HVC is involved in generating the stereotyped song motifs of adult birds (13), whereas the lateral magnocellular nucleus of the anterior nidopallium (LMAN) forms the output of a basal-ganglia pathway involved in generating subtle song variability (14–17).”

“…electrophysiological recordings failed to detect feedback-driven changes in the singing-related activity of HVC X neurons (Kozhevnikov and Fee, 2007; Prather et al., 2008), in vivo imaging permitted detection of subtle changes in HVC X dendritic spines within the first few days of deafening.”

“Much more is known experimentally about the exact neuronal mechanisms in songbirds than in humans, due to detailed electrophysiological studies which have shown that songbirds use a sequence of auditory dynamics to generate and recognize song in a highly effective manner [6,13].”

“A noteworthy model of audio–vocal interaction derives from birdsong literature (Margoliash 2002; Prather et al. 2008).”

“76 This mechanism has been shown to be optimized for shaping so-cialresponses and mayalsocontributetothe previouslyobserved overall suppression of discharge of pyramidal (especially cortico-spinal) neurons during action observation.”

“This communicative phenomenon is widespread in the animal world (Bargh et al., 1996; Dyer, 2002; Hauser, 1996; Mather, 2004), and it could be supported by “mirror” neurons that couple perceived and executed behaviors (Prather et al., 2008).”

“Because these neurons continue to fire during singing even when auditory feedback is distorted (Kozhevnikov and Fee, 2007; Prather, 2013; Prather et al., 2008), the activity of these neurons is thought to be related to the motor performance of song.”

“In the last two decades, neuroscientific research has demonstrated that humans (Mukamel et al., 2010), non-human primates (Rizzolatti and Craighero, 2004) and birds (Prather et al., 2008) are equipped with a particular class of multimodal neurons active during action execution and action perception.”