REVIEW ARTICLE

published: 03 June 2013

HUMAN NEUROSCIENCE doi: 10.3389/fnhum.2013.00237

The neural control of singing

Jean Mary Zarate*
Department of Psychology, New York University, New York, NY, USA

Edited by: Singing provides a unique opportunity to examine music performance—the musical
Eckart Altenmüller, University of instrument is contained wholly within the body, thus eliminating the need for creating
Music and Drama Hannover,
Germany
artificial instruments or tasks in neuroimaging experiments. Here, more than two decades
of voice and singing research will be reviewed to give an overview of the sensory-motor
Reviewed by:
Boris Kleber, McGill University, control of the singing voice, starting from the vocal tract and leading up to the brain regions
Canada involved in singing. Additionally, to demonstrate how sensory feedback is integrated with
Hermann Ackermann, University of vocal motor control, recent functional magnetic resonance imaging (fMRI) research on
Tuebingen, Germany
somatosensory and auditory feedback processing during singing will be presented. The
*Correspondence:
relationship between the brain and singing behavior will be explored also by examining:
Jean Mary Zarate, Department of
Psychology, New York University, (1) neuroplasticity as a function of various lengths and types of training, (2) vocal amusia
6 Washington Place, Room 275-276, due to a compromised singing network, and (3) singing performance in individuals
New York, NY 10003, USA with congenital amusia. Finally, the auditory-motor control network for singing will be
e-mail: [Link]@[Link]
considered alongside dual-stream models of auditory processing in music and speech
to refine both these theoretical models and the singing network itself.
Keywords: auditory processing, audio-vocal integration, dual-stream model, non-musicians, singers,
somatosensory, vocal pitch

Most of the literature on sensory-motor control in music SENSORY-MOTOR CONTROL OF VOCALIZATION

production and training-induced plasticity focuses on trained SENSORY-MOTOR CONTROL OBSERVED FROM THE VOCAL TRACT
instrumental musicians or learning paradigms with musical When air passes through the glottis (opening of the larynx) and
instruments (e.g., learning to play short piano melodies, etc.). causes the vocal folds surrounding the glottis to vibrate at a
Singing, however, provides a unique opportunity to examine particular rate, the resulting vibration rate determines the fun-
sensory-motor processes during musical production, since the damental frequency (i.e., perceived pitch) of the voice (Sundberg,
instrument is already contained within the body; there is no need 1987). Different intrinsic and extrinsic laryngeal muscles inter-
to create artificial instruments to assess motor control mecha- act to regulate fundamental frequency by altering the length
nisms with neuroimaging or any other experimental approach. of the vocal folds, thus changing the rate of vocal-fold vibra-
Moreover, the adult vocal apparatus is highly trained to pro- tion (Hirano et al., 1969; Sundberg, 1987). The precise control
duce nuanced utterances in both song and speech. Across their of laryngeal muscles is maintained in part by laryngeal reflexo-
lifetime, healthy non-musicians have sung (or have attempted genic control systems, in which receptors within the larynx adjust
to sing) a full repertoire of songs in socially and culturally spe- muscular contractions during perturbations. For instance, during
cific settings, (“Happy Birthday,” their national anthem, etc.). vocalization, the uneven airflow passing through the glottis stim-
Additionally, healthy individuals can control their vocal pitch ulates the myotatic mechanoreceptors in the intrinsic laryngeal
and/or output intensity to indicate the intent of a sentence (e.g., muscles; these stretch-sensitive receptors initiate reflexive mus-
declarative statements vs. questions vs. commands), set the emo- cular adjustments to ensure that the vocal folds remain at the
tional context for a conversation (e.g., happiness, anger, sadness), intended length and tension and therefore maintain a steady vocal
or in tonal languages, distinguish between words and their mean- pitch (Wyke, 1974). Additional reflexogenic systems work in con-
ings. Singers, on the other hand, undergo many years of extensive cert with the intrinsic laryngeal reflexogenic system to ensure a
sensory-motor training and practice to exert much finer vocal stable vocalization (Wyke, 1974). Vocalization also involves the
control during more difficult tasks, such as singing fast vocal runs coordination of many other muscles, including the diaphragm
(e.g., melismata, melodic embellishments, etc.) or maintaining a and abdominal/thoracic muscles to provide airflow and regulate
melodic passage as someone else simultaneously sings a harmonic vocal output intensity, and articulatory muscles (e.g., lip, jaw, and
line. Therefore, using singing tasks to test groups with different tongue muscles, Hardcastle, 1976; Sundberg, 1987). The articula-
levels of singing experience is a rare opportunity to determine tory muscles contain somatosensory receptors that play a role in
how musical experience specifically enhances sensory-motor con- generating different vocal-tract configurations, which shape the
trol of this particular instrument, beyond the remarkable feats formant frequencies that contribute toward vowel formation and
it already can perform. However, the mechanisms by which the vocal timbre (Sundberg, 1987; Jürgens, 2002; Perkell, 2012).
vocal instrument is precisely controlled for singing are highly Similar to the somatosensory contribution to reflexogenic
complex and thus require multiple networks for vocal motor vocal control systems, auditory feedback also plays a role in
control and sensory feedback processing. reflex-like adjustments of ongoing vocal motor control. For

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Zarate Neural control of singing

instance, a slight decrease in auditory feedback amplitude elic-

its a quick increase in vocal output amplitude, which is known
as the Lombard reflex (Lombard, 1911). During speech pro-
duction, when the first formant frequency is shifted so that a
produced vowel (e.g., /ε/) sounds like a different one (e.g., /æ/),
the vocal motor system immediately compensates for the for-
mant shift (Houde and Jordan, 1998, 2002; Purcell and Munhall,
2006a,b). Arguably, the most relevant auditory-vocal motor cor-
rection for singers deals with vocal pitch. When the pitch of
auditory feedback is shifted up or down as participants vocal-
ize for a few seconds (either at a comfortable pitch or to match
a target pitch), investigators have observed pitch-shift responses,
during which vocal pitch is adjusted quickly in the opposite direc-
tion of the feedback shift (Anstis and Cavanagh, 1979; Burnett
et al., 1998; Larson, 1998; Hain et al., 2000; Jones and Munhall,
2000, 2005; Larson et al., 2000; Burnett and Larson, 2002; Liu
and Larson, 2007; Jones and Keough, 2008). These pitch-shift
responses often have two components: (1) an early pitch-shift
response of 25–50 cents (irrespective of the pitch-shift magni-
tude) that occurs 100–150 ms after the pitch shift; and (2) a
late pitch-shift response with a latency of 250–600 ms, whose
magnitude and direction can be under voluntary control, if lis-
teners are instructed to make a specific response (e.g., change
pitch to either oppose or follow the pitch shift, etc., Burnett
et al., 1998; Larson, 1998; Hain et al., 2000). Interestingly, pro- FIGURE 1 | Neural networks of vocal motor control (central column),
longed exposure to feedback that is incrementally pitch-shifted somatosensory (left) and auditory feedback processing (right), and
over numerous trials can produce aftereffects in which intended hypothesized regions of sensory-motor control of voice [modified from
a model proposed by Jürgens (2009)]. The vocal motor control hierarchy
vocal pitch and vocal output are mismatched, such that vocal
starts with the generation of complete vocal patterns from the reticular
pitch is automatically adjusted even when auditory feedback is formation and phonatory motoneurons (white boxes), and then the next
returned to normal (Jones and Munhall, 2000, 2005; Jones and highest level of control (green boxes) stems from the anterior cingulate
Keough, 2008). cortex (ACC) and periaqueductal gray (PAG), which can initiate and
emotionally motivate vocal responses. The highest level of vocal control
comes from the primary motor cortex (M1, blue box; its modulatory brain
NEURAL NETWORKS GOVERNING SENSORY-MOTOR CONTROL OF regions are not depicted), which is responsible for producing learned
VOCALIZATION vocalizations (i.e., speech and song). Somatosensory feedback (dotted
Brain regions involved in vocal motor control arrow) from various receptors distributed throughout the vocal tract is
Multiple neural networks are required for precise control of the processed in the ascending somatosensory pathway (yellow boxes, left;
black slanted lines indicate that only selected regions of this pathway are
“phonatory” muscles mentioned above. The reticular formation shown) and transmitted to the primary and secondary somatosensory
of the pons and medulla has direct connections to the motoneu- cortex (S1, S2). Auditory feedback (dashed arrow) from the vocalization is
rons for all phonatory muscles (Figure 1, white boxes, Thoms processed by the ascending auditory pathway and auditory cortical regions
and Jürgens, 1987), and thus may coordinate phonatory mus- (orange boxes, right). Potential neural regions that integrate sensory
feedback processing with vocal motor control are indicated with
cle groups to generate complete vocal patterns (Jürgens and
red-outlined boxes, and their shared connections are represented by red
Hage, 2007). This region receives excitatory input from two dis- arrows: (A) the PAG, (B) ACC, and (C) the insula (in purple, classified as a
tinct neural pathways of vocal control (Figure 1; Jürgens, 2009; higher-order associative area).
Owren et al., 2011). The first vocal control pathway (Figure 1,
green boxes) contains the anterior cingulate cortex (ACC) and
the midbrain periaqueductal gray (PAG), both of which produce In humans, these networks form a tripartite hierarchy of vocal
vocalizations when stimulated electrically or pharmacologically motor control (Figure 1, center column, Simonyan and Horwitz,
(Müller-Preuss and Jürgens, 1976; Müller-Preuss et al., 1980; Suga 2011): (1) the reticular formation constitutes the lowest level at
and Yajima, 1988; Dujardin and Jürgens, 2005). The second neu- which complete vocal patterns are generated; (2) the next level is
ral pathway includes the primary motor cortex (M1, Figure 1, comprised of the ACC and the PAG, which are attributed with the
blue box) and two subcortical loops—comprised of putamen, voluntary initiation and emotional/motivational control of vocal-
globus pallidus, pontine gray, and cerebellum—that modulate izations (Jürgens, 2002, 2009); and (3) the highest level of vocal
vocal motor commands from M1 and subsequently send modi- control occurs in M1 (and its modulatory brain regions), which
fied motor programs via the ventrolateral thalamus back to M1; is associated with the generation of learned vocalizations, such
electrical stimulation of the ventral part of M1 elicits vocaliza- as speech and song (Jürgens, 2002, 2009). Importantly, this func-
tions, as well as individual movements of the jaw, tongue, and lips tional distinction of M1 is based on humans’ unique possession of
(Penfield and Rasmussen, 1950). direct connections between the phonatory region of M1 (i.e., the

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Zarate Neural control of singing

ventral portion) and the motoneurons of phonatory muscles (see fashion, since patients with lesions in this region displayed
Figure 1); bilateral lesions to this M1 region destroys the ability much higher discrimination thresholds than controls when asked
to speak and sing (Jürgens, 2009), while innate vocalizations (e.g., to indicate the direction of pitch change between two notes
shrieking, crying, etc.) that may be controlled by the ACC and (Johnsrude et al., 2000). Processing pitch changes or melodic
PAG are left intact. In contrast, damage to the modulatory brain phrases within a sung passage recruits additional auditory cor-
regions associated with M1 (e.g., putamen, globus pallidus, pon- tical regions outside of Heschl’s gyrus, including regions in the
tine gray, and cerebellum) can result in speech disorders such as right superior temporal gyrus (STG), planum polare, and planum
stuttering and dysarthria (Ackermann et al., 1992; Jürgens, 2002; temporale (Zatorre et al., 1994; Patterson et al., 2002; Hyde
Alm, 2004). Lesions in the second level of vocal control may lead et al., 2008). When pitch comparisons are performed within a
to mutism (attributed to PAG damage, Esposito et al., 1999) or sequence of tones or short melodies, increased activity is observed
loss of emotional/motivational intonation in speech (following within right auditory and frontal cortical regions presumably
damage to the ACC, Simonyan and Horwitz, 2011). Importantly, during tonal working memory processes, compared to passive
the functional organization of vocal motor control in humans melody perception (Zatorre et al., 1994). Melodic phrase com-
is concurrently hierarchical and parallel, since damage to brain parisons in the same key, which may be done to ensure correct
regions within the second or third levels does not abolish all melodic reproduction, engages extensive activity within several
vocalizations. auditory cortical regions along bilateral STG, whereas melodic
phrase comparisons across a pitch transposition (i.e., a key
Neural processing of somatosensory feedback change) engages additional activity from the intraparietal sulcus
Various somatosensory receptors transmit feedback about the (IPS, Foster and Zatorre, 2010).
current state of the vocal motor system (e.g., placement of articu- Aside from providing details about vocal pitch, auditory feed-
lators, respiration, etc.) via the glossopharyngeal and vagus nerves back can also provide information about vocal timbre, which is
and the ascending somatosensory pathway, which includes the argued to be processed specifically along the superior temporal
nuclei gracilis, solitarius, and spinalis nervi trigemini and the sulcus (STS, Belin et al., 2000). Kriegstein and Giraud (2004) dis-
medial lemniscus in the medulla, and the ventral posterome- covered three functionally distinct regions along the STS. The
dial nucleus in the thalamus (Jürgens and Kirzinger, 1985; Willis, anterior STS is associated with familiar voice recognition, while
1986). The thalamus sends somatosensory information to pri- the mid/anterior STS preferentially responds to the spectral char-
mary and secondary somatosensory cortex (S1 and S2), as well acteristics of voices. The posterior STS (pSTS), which is recruited
as the insula (Jones and Powell, 1970; Augustine, 1996; Jürgens, during recognition of unfamiliar voices, may be involved in ana-
2002; Ackermann and Riecker, 2004, 2010). More specifically, lyzing spectral details (or the changes therein) of voices over
the ventral portion of the primary somatosensory cortex (S1)— time (Kriegstein and Giraud, 2004; Warren et al., 2006). Given
posteriorly adjacent to the M1 phonatory area that governs vocal- that the pSTS is also recruited in response to presentation of
izations and individual movements of the articulators (Penfield frequency-modulated sweeps of pure tones (Poeppel et al., 2004)
and Rasmussen, 1950)—processes somatosensory information and phonological processing (Hickok and Poeppel, 2007), this
about articulatory movements (Grabski et al., 2012), while the region may be involved generally in processing spectrotempo-
anterior portion of the insula is recruited particularly during ral fluctuations in sound, including notable changes in auditory
overt vocalizations (compared to covert speech and song, Riecker feedback.
et al., 2000) and may contribute to voluntarily controlled respi-
ration during vocalizations in general (Ackermann and Riecker, Potential substrates for integrating sensory feedback with vocal
2010). motor control
The constituents of the vocal motor network associated with
Neural processing of auditory feedback during singing voluntary initiation and emotional/motivational control of
As each sung note reaches a singer’s ear as auditory feedback, vocalizations—the PAG and ACC—receive both somatosensory
each of the different frequencies within that particular vocal and auditory input, and thus form two potential substrates for
pitch are transduced by the organ of Corti on the basilar mem- sensory-motor control of vocalization (Figure 1, red-outlined
brane of the cochlea (Hudspeth, 2000). The frequency charac- boxes and arrows). The PAG (Figure 1A) receives somatosensory
teristics that are required to perceive the pitch are transmitted input via afferent projections from the nucleus gracilis (impli-
and/or processed along different parts of the ascending auditory cated in respiratory control, Hannig and Jürgens, 2006) and
pathway—comprised of the cochlear nucleus, lateral lemniscus, nuclei solitarius and spinalis nervi trigemini (kinesthetic and pro-
inferior colliculus, and the medial geniculate nucleus of the tha- prioceptive information, Jürgens and Kirzinger, 1985; Yoshida
lamus (Griffiths et al., 2001)—before the extracted frequencies et al., 2000), as well as auditory information from the inferior
(and many other attributes of sounds) are further processed in colliculus and lateral lemniscus (Dujardin and Jürgens, 2005),
primary and secondary auditory cortex within Heschl’s gyrus. all of which may facilitate initiating vocalizations in response
In particular, pitch information may be processed specifically to external stimuli or adjusting vocalizations based on sensory
by a (rightward lateralized) pitch-sensitive area located in lateral feedback. For example, when connections to the cerebrum are
Heschl’s gyrus, reported to be involved in conscious pitch per- severed, the Lombard reflex is preserved during PAG-induced
ception (Griffiths, 2003; Bendor and Wang, 2006). This region vocalizations coupled with auditory masking, suggesting that
may also be involved in organizing pitches in a hierarchical the PAG may govern auditory-motor control during involuntary

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Zarate Neural control of singing

auditory-vocal reflexes (e.g., Lombard reflex, formant- and pitch- TRAINING EFFECTS ON THE SENSORY-MOTOR CONTROL OF
shift responses) without additional control from cortical regions SINGING
(Nonaka et al., 1997). The ACC (Figure 1B) directly receives VOCAL TRAINING EFFECTS ON THE NEURAL CORRELATES OF
somatosensory input from S2 and auditory input from auditory SENSORY-MOTOR CONTROL OF SINGING
cortical regions along the STG and STS (Jürgens, 1983; Barbas In general, due to their extensive auditory-motor training and
et al., 1999). This region also receives these types of sensory input experience, musicians excel in various auditory and motor tasks.
indirectly from S1 and auditory association areas via the insula For instance, previous studies report that musicians perform
(Mesulam and Mufson, 1982; Augustine, 1996). Since the insula better at pitch, timbre, and voice discrimination tasks than non-
is a gateway of both somatosensory and auditory information musicians (Kishon-Rabin et al., 2001; Tervaniemi et al., 2005;
for the ACC, this region itself may provide another substrate for Chartrand and Belin, 2006; Micheyl et al., 2006). In addition
sensory-motor control of vocalization (Figure 1C, purple box). to possessing better auditory discrimination skills than non-
In particular, the anterior insula, whose cytoarchitecture and musicians, musicians also display more precise control over the
projections classify it as an association area that integrates dif- vocal apparatus in the absence of proper auditory feedback. For
ferent modalities (e.g., auditory, visual, somatosensory, motor, example, trained singers sang more accurately with masked audi-
etc., Rivier and Clarke, 1997; Lewis et al., 2000; Bamiou et al., tory feedback than non-musicians (Schultz-Coulton, 1978), yet
2003; Ackermann and Riecker, 2004), is engaged specifically dur- one study reported the reverse (Watts et al., 2003). However,
ing voiced speech and song, relative to covert or internal versions Watts’ group of singers may have had less vocal training than
(Riecker et al., 2000; but see Hillis et al., 2004; Ackermann and the singers in Schultz-Coulton’s study; Watts suggested that dur-
Riecker, 2010 for conflicting clinical evidence of the insula’s role ing the earlier stages of vocal training, more emphasis is placed
in speech production). on monitoring auditory feedback for vocal accuracy (Watts et al.,
2003), which may account for their recruited singers’ greater vocal
Neuroimaging evidence: a general functional network for human inaccuracy with masked feedback compared to non-musicians.
vocalization In fact, in a longitudinal study with trained singers performing
Neuroimaging studies from the past two decades have confirmed various slow and fast singing tasks, vocal accuracy was not dif-
that many regions within vocal motor and sensory networks are ferentially affected by masked auditory feedback neither before
recruited during various overt speech and song tasks, including: nor after 3 years of vocal training (Mürbe et al., 2004), which
word or letter generation (Paus et al., 1993); syllable repetition suggests that auditory feedback may not play a crucial role in
(Riecker et al., 2005); singing a note repeatedly (Perry et al., vocal accuracy after extensive vocal training. Nevertheless, vocal
1999), in a sustained fashion (Zarate and Zatorre, 2008), or while accuracy did improve during slow singing tasks with masked feed-
changing vowels in particular rhythms (Jungblut et al., 2012); back after vocal training, which Mürbe et al. (2004) attributed
repeating syllables, spoken words, and sung or hummed melodies to training-enhanced “neuromuscular memory of pitch” (p. 240).
(Özdemir et al., 2006); humming, speaking, or singing lyrics of This implies that trained singers may rely more on somatosensory
a well-known song (Formby et al., 1989; Jeffries et al., 2003); feedback to make sure that notes are produced properly, since they
reciting the months of the year or singing a familiar melody can still sing accurately for some time after losing their hearing
(Riecker et al., 2000); telling a story (Schulz et al., 2005); impro- (Wyke, 1974). Indeed, a functional magnetic resonance imag-
vising word phrases, melodies, or harmonies (Brown et al., 2004, ing (fMRI) singing study demonstrated that both vocal students
2006); spontaneous and synchronized speaking and singing (Saito (enrolled in a performance program) and professional opera
et al., 2006); and singing an Italian aria (Kleber et al., 2007). singers recruited more activity within S1 and somatosensory asso-
Summarized from the neuroimaging evidence above, a general ciation cortex than amateur singers, and moreover, the amount
functional network for human vocalization (including speech and of singing practice positively correlated with the activity in these
song) is comprised of the brain regions reviewed in the preced- regions (Kleber et al., 2010). In a more recent fMRI study, Kleber
ing sections: M1, ACC, basal ganglia, thalamus, and cerebellum et al. (2013) effectively reduced the amount of somatosensory
for vocal motor control; S1 and S2 for somatosensory feedback feedback available by applying a topical anesthetic to the vocal
processing; bilateral auditory cortical regions (primary auditory folds just prior to singing in the MR scanner. The investigators
cortex and a pitch-sensitive region within Heschl’s gyrus, various determined that under vocal-fold anesthesia, singers displayed
portions of STG and STS) for auditory feedback processing; and reduced activity in the right anterior insula than non-musicians,
the insula presumably during multimodal processing of sensory who had enhanced insular activity with anesthesia. Additionally,
feedback. In addition, premotor and parietal areas are recruited this region exhibited decreased functional connectivity to M1,
during human vocalization, and their functional roles will be S1, and auditory cortex in singers under topical anesthesia, while
further discussed below. functional connectivity increased between these regions in non-
Until this point, both speech and song studies have been musicians with anesthetized vocal folds. Notably, singers still sang
included to outline the brain regions associated with general more accurately under anesthesia than non-musicians, despite the
vocal control in humans, since speaking and singing employ com- observed reduction of insular activity and functional connectivity.
mon mechanisms involved in vocal production. Moving forward, Both of Kleber’s experiments provide evidence that: (1) singers
we will focus more on singing studies to examine how musical may rely more heavily on somatosensory feedback as a function
training modulates the general functional network for human of vocal training and practice, and (2) singers, perhaps by virtue
vocalization as it is used for singing. of their training, can regulate activity within the right anterior

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Zarate Neural control of singing

insula to “disengage” or ignore somatosensory feedback when it 1982), and is attributed to conditional sensory-motor associa-
is perturbed or deemed unreliable and thus may significantly alter tions (Petrides, 1986; Chouinard and Paus, 2006)—to prepare
their singing performance. a vocal response (e.g., maintain steady vocal output or correct
Similar to the somatosensory feedback perturbation induced for the pitch shift). Second, despite the observed lack of per-
in Kleber’s recent study, Zarate and colleagues (2008, 2010b) formance differences in the compensate task—i.e., both groups
utilized pitch-shifted auditory feedback with fMRI techniques voluntarily adjusted for the pitch-shifted feedback to a similar
to target explicitly the brain regions involved in auditory-vocal extent—different neural substrates for auditory-motor control
motor control in singing. As discussed earlier, pitch-altered feed- were recruited in each group. Compared to singers, the non-
back elicits pitch-shift responses that often contain early and musicians exhibited more activity within the dPMC while volun-
late components. Larson and colleagues suggested that the early tarily correcting for the pitch shift (Figure 2A; Zarate and Zatorre,
pitch-shift response, which may be governed by the midbrain 2008); the authors proposed that the dPMC was recruited selec-
PAG, is a more automatic reaction used to stabilize vocal out- tively in non-musicians as they learned to associate a pitch-shift
put by correcting small, unexpected fluctuations in vocal pitch; “cue” in auditory feedback with a corrective adjustment in vocal
the late pitch-shift response, on the other hand, may be under pitch. Therefore, this region may constitute a basic substrate
more voluntary control—perhaps controlled by the auditory cor- for voluntary auditory-motor control of vocal pitch (Zarate and
tex, ACC, etc.,—and thus may contribute to vocal pitch control Zatorre, 2008) and perhaps music production in general—after
during speaking and singing (Burnett et al., 1998; Larson, 1998; more training and practice, the dPMC is recruited less in non-
Hain et al., 2000; Liu and Larson, 2007). Indeed, although trained musicians during the same musical production task that was
singers exhibit early pitch-shift responses to briefly pitch-shifted learned (and assessed with fMRI) at earlier stages of an exper-
feedback, they were still able to maintain their intended goal iment (Chen et al., 2012). Indeed, rather than recruiting the
for vocalization (either sustaining a steady pitch or glissandos, dPMC, singers engaged auditory cortex within the pSTS, ante-
Burnett and Larson, 2002; Hafke, 2008), perhaps due to enhanced rior insula, and ACC for this task (Figure 2B; Zarate and Zatorre,
top–down control of the late pitch-shift response that resulted 2008; Zarate et al., 2010b). Moreover, voluntary vocal-control
from years of vocal training. In contrast, non-musicians may singing tasks (i.e., compensating for and ignoring large pitch
not exhibit such precise vocal control over the late pitch-shift shifts in feedback) specifically enhanced the functional connec-
response. To assess the effects of extensive vocal training on pitch tivity between the pSTS and IPS (Figure 2C; Zarate et al., 2010b).
control in singing, Zarate and colleagues (2008, 2010b) tested Given the IPS’ role in sensory-motor transformations, Zarate
singers and non-musicians with two singing tasks that required and colleagues suggested that within singers, the auditory cor-
different types of top–down voluntary control: (1) an “ignore” tex and IPS jointly process and extract pitch-shift information
task where subjects were required to hold their pitch steady, that can be used to control vocal pitch (e.g., magnitude and
despite hearing pitch-shifted auditory feedback; and (2) a “com- direction of the pitch shift). Since the auditory cortex is func-
pensate” task in which subjects had to voluntarily adjust their tionally connected to the insula and ACC (Zarate and Zatorre,
vocal pitch precisely to correct for the pitch shift. The authors 2008; Zarate et al., 2010b), the pitch-shift information may be
hypothesized that ignoring a small pitch shift would not only sent via the anterior insula to the ACC for initiation of the task-
elicit an early pitch-shift response, but also target the PAG rel- appropriate vocal motor program (i.e., maintain the originally
ative to the compensate task, which was specifically designed to produced note or correct for the shift). The authors proposed that
engage their proposed cortical substrates for auditory-motor con- these four cortical regions constitute an experience-dependent
trol of vocal pitch—auditory cortex, insula, and ACC (Zarate and network for auditory-motor control of the singing voice, which
Zatorre, 2008; Zarate et al., 2010b). may be recruited increasingly as a function of more vocal training
Due to the temporal limitations of fMRI methodology, Zarate and practice.
et al. (2010b) were not able to determine whether the PAG is
involved particularly with eliciting early pitch-shift responses, SHORT-TERM TRAINING EFFECTS ON AUDITORY AND VOCAL SKILLS
since these responses have a latency that is shorter than the AND THEIR NEURAL CORRELATES
best temporal resolution for fMRI. Nevertheless, two interest- Based on the studies above, trained singers may have more pre-
ing cortical findings from their singing tasks were observed. cise vocal control compared to non-musicians, due to extensive
First, both groups recruited the IPS and dorsal premotor cortex vocal training that recruits an experience-dependent cortical net-
(dPMC) in each pitch-shifted singing task, compared to singing work and/or selectively gates access to sensory feedback within
with normal feedback (Zarate and Zatorre, 2008). The authors this network. However, Amir et al. (2003) determined that instru-
suggested that since the IPS is associated with transformations mental musicians (without formal vocal training) also sang more
of sensory input for motor preparation (Astafiev et al., 2003; accurately than non-musicians in a simple pitch-matching task,
Grefkes et al., 2004; Tanabe et al., 2005), it was recruited specif- in which subjects were required to sing a note that was just
ically during transformations of auditory input (see Foster and presented. Additionally, two studies report a significant corre-
Zatorre, 2010; Zatorre et al., 2010; Foster et al., 2013) into spa- lation between pitch discrimination and vocal accuracy in both
tial information within the frequency domain (i.e., up or down). instrumental musicians and non-musicians—individuals who
This “frequency spatial information” can then be used by the sang more accurately also had better discrimination skills (Amir
dPMC—an area that receives indirect connections from audi- et al., 2003; Watts et al., 2005). If this observed correlational rela-
tory and parietal areas via the insula (Mufson and Mesulam, tionship is a causal one, as these studies suggest, then refining

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Zarate Neural control of singing

FIGURE 2 | Brain regions involved in auditory-motor control of (C) Analyses of task-modulated functional connectivity revealed that
singing, as observed in non-musicians and singers. (A) When relative to singing with normal auditory feedback, the 200-cent pitch shift
voluntarily correcting for a 200-cent pitch shift in auditory feedback specifically enhanced functional connectivity between right pSTS and
(“compensate 200c” task), non-musicians recruited more activity within intraparietal sulcus (IPS) during both the “ignore 200c” and “compensate
the dorsal premotor cortex (dPMC) than singers. (B) Singers engaged the 200c” tasks, as well as the postcentral gyrus (containing somatosensory
posterior superior temporal sulcus (pSTS), anterior cingulate cortex (ACC), cortex) during the “ignore 200c” task. Data from Zarate and colleagues
and anterior insula (aINS) when performing the “compensate 200c” task. (2008, 2010b).

pitch-discrimination skills may lead to better vocal accuracy. and a control group that received no training—with auditory
For instance, many studies have reported that auditory training discrimination and singing tasks. In this study, the investiga-
improves pitch discrimination both at the training frequency and tors employed more naturalistic melodic singing tasks to target
at other non-trained frequencies (Demany, 1985; Delhommeau the experience-dependent network, since accurate production
et al., 2002, 2005; Ari-Even Roth et al., 2003). Furthermore, of novel melodies requires auditory-motor control in a simi-
the effects of auditory training with pure tones also general- lar fashion as voluntarily correcting for pitch-shifted feedback;
ize to more complex tones (Grimault et al., 2003). In light of the auditory feedback of the currently produced note may be
these observations and the proposed causal relationship between monitored in order to produce the correct pitch interval to the
pitch discrimination and vocal accuracy, the newly enhanced next note. Although the experimental group displayed enhanced
ability to discriminate between pitches (following training) may auditory discrimination skills and training-induced changes in
increase the likelihood of detecting slight errors in vocal out- auditory task-associated neural activity (Zatorre et al., 2012), they
put, which may result in increased vocal accuracy. In turn, these did not show significant improvements in singing performance
training-induced behavioral changes are often accompanied by or recruit the experience-dependent network for auditory-motor
neural plasticity. For example, after non-musicians had received control in singing (Zarate et al., 2010a). Consequently, Zarate
pitch-discrimination training, improved pitch discrimination was et al. (2010a) concluded that auditory training alone (at least
accompanied by enhanced auditory cortical responses (Bosnyak in an experimental setting) is not sufficient to improve vocal
et al., 2004). Additionally, when non-musicians were trained to performance or recruit the experience-dependent network for
associate specific piano keys with their corresponding pitches and auditory-motor control of singing (auditory cortex, IPS, ante-
play short piano melodies, significant training-induced increases rior insula, and ACC); perhaps only simultaneous enhancements
in cortical activity were observed within auditory, sensorimo- in both auditory and vocal motor skills via extensive training
tor, frontal, and parietal regions (Bangert and Altenmüller, 2003; (e.g., voice lessons) would bring forth improvements in vocal
Lahav et al., 2007). performance and engage this particular network.
Therefore, to examine whether: (1) singing accuracy improves
subsequent to auditory training, and (2) auditory-training SENSORY-MOTOR CONTROL OF SINGING IN OTHER
enhanced singing specifically engaged the experience-dependent POPULATIONS
network for auditory-motor control in singing (i.e., auditory ACQUIRED VOCAL AMUSIA
cortex, IPS, anterior insula, and ACC), Zarate et al. (2010a) Clinical evidence that complements the proposed roles of the
tested two groups of non-musicians—an experimental group that auditory cortex, IPS, S1, insula, and premotor regions during
received training to improve their auditory discrimination skills, singing comes from case reports of brain lesions that result

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Zarate Neural control of singing

in vocal amusia or oral-expressive amusia (for a review, see somewhat accurately, despite observed problems with pitch per-
Berkowska and Dalla Bella, 2009; Stewart et al., 2009). For ception (Ayotte et al., 2002; Loui et al., 2008; Dalla Bella et al.,
instance, a woman with cortical atrophy in the right temporal 2009; Hutchins et al., 2010).
lobe and insula, as well as diminished blood flow to right frontal Based on this behavioral evidence, as well as observations of
and temporal regions, exhibited signs of progressive amusia and singing in the general population, Berkowska and Dalla Bella
aprosodia—she gradually was incapable of perceiving and pro- proffered a “vocal sensorimotor loop” model to outline two func-
ducing well-known melodies and affective intonation or prosody tional pathways within the song system that may explain observa-
in speech (Confavreux et al., 1992). Additionally, a female tango tions of accurate-pitch and poor-pitch singing (Berkowska and
singer who suffered a right-lateralized cerebral infarction pre- Dalla Bella, 2009; Dalla Bella et al., 2011). In this model, the
sented with damage to right Heschl’s gyrus and STG, inferior authors list potential brain regions—based on previous neu-
parietal regions including supramarginal gyrus and S1, and pos- roimaging studies, many of which are included in the section
terior insula; her music perception was greatly diminished post- Neuroimaging Evidence: A General Functional Network For
stroke (relative to speech discrimination), and her singing was Human Vocalization—that contribute to mechanims underlying
considered less stable within single notes, less accurate in pitch, singing, such as: regions within the STG for processing auditory
and monotonous in affect (Terao et al., 2006). input, which includes the auditory target to be reproduced and
While the two previous cases with damage to auditory cortex, auditory feedback; dorsal prefrontal cortex, inferior sensorimo-
insula, and other regions within the singing network presented tor cortex, area “Spt” within the planum temporale, and insula
with deficits in both music perception and production, two addi- for auditory-motor mapping and memory access; supplementary
tional cases present perhaps the strongest evidence for these motor area, ACC, and insula for motor preparation; and ven-
regions’ involvement specifically for singing in the absence of tral M1 for vocal motor execution. Berkowska and colleagues
impaired auditory perception. In a female patient who suffered also make distinctions between two pathways—a covert path-
a stroke in the right hemisphere affecting the lateral frontal lobe way involved in pitch discrimination (that can be compromised
and M1, STG, insula, S1, and inferior parietal lobe, investiga- in congenital amusia), and an overt pathway involved in pitch
tors observed impaired affective intonation in speech and the production—but they do not clarify which of the aforementioned
inability to sing pitch intervals accurately, while familiar-song brain regions belong to each pathway. Congenital amusia may
perception and singing rhythms or melodic contour were rela- be due to a structural and functional “disconnection” between
tively preserved (Murayama et al., 2004). Finally, a male amateur right auditory and inferior frontal cortical regions that contribute
singer with right-lateralized damage to his posterior temporal to pitch processing—although the right auditory cortex exhibits
lobe, inferior parietal lobe, insula, and inferior frontal gyrus pre- differential responses to pitch changes, the right inferior frontal
sented with relatively spared speech comprehension and produc- cortex does not show a correlated increase in activity, as it does
tion, prosodic perception and production, music perception, and in normal listeners (Hyde et al., 2011). Even though this partic-
rhythm production; however, he exhibited specifically impaired ular covert pathway is affected, auditory input (e.g., presented
pitch-interval production (Schön et al., 2004). This rather pure auditory targets, auditory feedback, etc.) can still be processed by
case of vocal amusia—in the absence of aphasia, aprosodia, auditory cortex (Moreau et al., 2009; Peretz et al., 2009; Moreau
and “perceptual” amusia—demonstrates that the damaged brain et al., 2013). Hypothetically speaking, auditory input may then
regions, which overlap with the areas outlined by Zarate and col- be processed further by IPS (depending on the amount of vocal
leagues (2008, 2010b), contribute to the finely-grained sensory- training), anterior insula, and premotor regions (dPMC or ACC)
motor control of singing. for auditory-motor control of singing based on Zarate’s find-
ings (Zarate and Zatorre, 2008; Zarate et al., 2010b), rendering
CONGENITAL AMUSIA vocal production relatively spared in some instances of congenital
Recall that the same neural network is recruited for singing in amusia.
healthy individuals, irrespective of the amount of vocal train-
ing or experience (see section Neuroimaging Evidence: A General COMPARISONS WITH MODELS OF AUDITORY PROCESSING
Functional Network For Human Vocalization). However, when Berkowska and Dalla Bella’s (2009), Dalla Bella et al.’s (2011)
pitch processing is compromised as observed in congenital amu- vocal sensorimotor loop model for singing, when enriched with
sia (Ayotte et al., 2002; Peretz and Hyde, 2003; Foxton et al., neuroimaging evidence from Zarate and Zatorre (2008), Hyde
2004)—due to cortical malformations in the STG and inferior et al. (2011), and Loui et al. (2009), potentially consists of audi-
frontal gyrus (Hyde et al., 2007) and disrupted structural and tory and inferior frontal cortex in the covert perception pathway
functional connectivity (Loui et al., 2009; Hyde et al., 2011)—it (Figure 3, blue arrow), and auditory cortex, IPS, anterior insula,
may be assumed that pitch production in singing would similarly and premotor areas in the overt production pathway (Figure 3,
be affected as well. Yet, as observed in Murayama’s et al. (2004) red arrows). These updated pathways resemble the more rec-
and Schön’s et al. (2004) case reports, a dissociation between pitch ognized (and widely debated) dual-stream model for auditory
perception and production skills can exist—following a stroke, processing, which was first proposed by Rauschecker and Tian
spared pitch perception does not necessarily preclude inaccurate (2000). The dorsal stream was originally suggested to be spe-
pitch production. Conversely, some individuals with congenital cialized for processing auditory spatial information (the “where”
amusia still can sing pitch changes in the correct direction (e.g., pathway), while the ventral stream was attributed with pro-
up vs. down), match target notes, and sing familiar song excerpts cessing auditory object/sound identity information (the “what”

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Zarate Neural control of singing

pathway). The scientific debate focuses mostly on competing regions via the insula to premotor areas for vocal motor adjust-
accounts and hypotheses of the dorsal stream’s contributions, ments. Therefore, according to these neuroimaging findings,
which include: (1) processing spectral changes over time (the transformations of task-relevant auditory features into subse-
“where in frequency” or “how” pathway, Belin and Zatorre, quent motor responses may not take place in only one brain
2000); (2) extracting relevant sound features and matching them region, as purported by the Warren et al. and Hickok/Poeppel
with stored templates of motor responses (the “do” pathway, models, but rather may be parceled among a network of dif-
Warren et al., 2005); (3) transforming auditory representations ferent areas within the dorsal auditory stream. Thus, it could
of speech into motor programs for speech gestures (Hickok be argued that many brain regions along the dorsal auditory
and Poeppel, 2000, 2004, 2007); and (4) comparing between stream are involved in processing “how” auditory features change
feedforward and feedback mechanisms (Rauschecker and Scott, over time before executing or “doing” a specific motor act in
2009). response to these auditory events, regardless of the particular
For our purposes here, the most relevant dorsal-stream mod- modality—be it information related to auditory space, speech, or
els are the spectrotemporal processing account from Belin and music.
Zatorre (2000) and auditory-motor transformation hypothe-
ses for auditory spatial processing and speech from Warren CONCLUSION
et al. (2005) and Hickok and Poeppel (2000, 2004, 2007). It In this review, findings from over 20 years of research have
should be noted, however that the auditory-motor control net- been reviewed to outline a general neural network for song and
work for singing conflicts with the latter two models, in which speech production (section Neuroimaging Evidence: A General
area Spt in the planum temporale is the sole neural substrate Functional Network For Human Vocalization). Within this func-
for auditory-motor transformations (Hickok and Poeppel, 2000, tional network, cortical substrates that are specific for the
2004; Warren et al., 2005; Hickok and Poeppel, 2007). Zarate’s sensory-motor control of singing pitch and are sensitive to
singing research (2008, 2010b) provides empirical evidence both the amount of vocal training have been identified (Figure 4):
supporting, and perhaps, updating these dorsal-stream models— the pSTS and IPS for auditory processing and transformation
auditory cortex and IPS process and extract pitch changes for motor output (light orange boxes), S1 for somatosensory
from feedback, and the pitch information is sent from these

FIGURE 4 | Neural substrates for sensory-motor control of singing that

are sensitive to the amount of vocal training [based on findings from
Kleber et al. (2010, 2013), Zarate and Zatorre (2008), Zarate et al.
(2010b)]. Brain regions that are not visible normally from this lateral brain
FIGURE 3 | A revised version of Berkowska and Dalla Bella’s, Dalla view are indicated in boxes outlined with dashes, and box colors are
Bella, and colleagues’ (2009, 2011) vocal sensorimotor loop model for retained from Figures 1 and 3. Activity within primary somatosensory
singing, updated with findings from Zarate and colleagues (2008, cortex (S1) increases as a function of the amount of weekly vocal practice,
2010b) fMRI studies. The covert pathway for pitch production (blue arrow) suggesting a greater reliance on somatosensory feedback with more
includes auditory cortex and inferior frontal gyrus (IFG), while the overt training and experience. After extensive vocal training and practice, the
pathway for vocal pitch production (red arrows) is comprised of auditory anterior insula (aINS) can serve a gating function for somatosensory
cortex (STG/STS), intraparietal sulcus (IPS), anterior insula (aINS), anterior feedback. Features within auditory feedback are processed and extracted
cingulate cortex (ACC), and dorsal premotor cortex (dPMC). Brain regions by auditory cortex (STG/STS) and the intraparietal sulcus (IPS), and
that are not visible normally from this lateral brain view are indicated in task-relevant auditory information is sent via the aINS to the dorsal
boxes outlined with dashes. Box colors are retained from Figure 1: light premotor cortex (dPMC)—in people with little to no formal vocal
orange for auditory processing, green for vocal motor control, purple for training—or to the anterior cingulate cortex (ACC) in experienced singers to
multimodal processing. voluntarily adjust vocal output according to the singing task demands.

Frontiers in Human Neuroscience [Link] June 2013 | Volume 7 | Article 237 | 8

Zarate Neural control of singing

processing (yellow box), anterior insula (in purple, both for network’s similarity to prevalent dual-stream models of auditory
auditory-motor integration and somatosensory feedback gating), processing as a whole.
and premotor regions for vocal motor preparation and response
initiation (dPMC and ACC, in green). When the auditory- ACKNOWLEDGMENTS
related findings are placed within a larger framework—a dual- The author thanks Robert J. Zatorre, Ph.D. and David Poeppel,
pathway (i.e., perception vs. production), sensory-motor model Ph.D. for their invaluable mentorship and support. This work was
for singing (Berkowska and Dalla Bella, 2009)—these music- supported in part by grants from the GRAMMY Foundation®,
specific findings can then be linked to broader research interests the Eileen Peters McGill Majors Fellowship, and the Centre
in auditory cognition, such as auditory spatial localization and for Interdisciplinary Research in Music Media and Technology
speech perception/production, due to the auditory-motor control (CIRMMT).

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ynx. Am. J. Med. 108(Suppl. 4a), neural substrates involved in sal of imagined melodies: a role Copyright © 2013 Zarate. This is
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Zarate, J. M., Delhommeau, K., ing singing. Neuroimage 40, J. Cogn. Neurosci. 22, 775–789. doi: the terms of the Creative Commons
Wood, S., and Zatorre, R. J. 1871–1887. doi: 10.1016/[Link] 10.1162/jocn.2009.21239 Attribution License, which permits use,
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neural plasticity following Zatorre, R. J., Delhommeau, K., and forums, provided the original authors
micromelody-discrimination train- Zarate, J. M. (2012). Modulation Conflict of Interest Statement: The and source are credited and subject to any
ing. PLoS ONE 5:e11181. doi: of auditory cortex response to author declares that the research copyright notices concerning any third-
10.1371/[Link].0011181 pitch variation following training was conducted in the absence of any party graphics etc.

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