Review
Neural pathways underlying vocal control

https://doi.org/10.1016/S0149-7634(01)00068-9Get rights and content

Abstract

Vocalization is a complex behaviour pattern, consisting of essentially three components: laryngeal activity, respiratory movements and supralaryngeal (articulatory) activity. The motoneurones controlling this behaviour are located in various nuclei in the pons (trigeminal motor nucleus), medulla (facial nucleus, nucl. ambiguus, hypoglossal nucleus) and ventral horn of the spinal cord (cervical, thoracic and lumbar region). Coordination of the different motoneurone pools is carried out by an extensive network comprising the ventrolateral parabrachial area, lateral pontine reticular formation, anterolateral and caudal medullary reticular formation, and the nucl. retroambiguus. This network has a direct access to the phonatory motoneurone pools and receives proprioceptive input from laryngeal, pulmonary and oral mechanoreceptors via the solitary tract nucleus and principal as well as spinal trigeminal nuclei. The motor-coordinating network needs a facilitatory input from the periaqueductal grey of the midbrain and laterally bordering tegmentum in order to be able to produce vocalizations. Voluntary control of vocalization, in contrast to completely innate vocal reactions, such as pain shrieking, needs the intactness of the forebrain. Voluntary control over the initiation and suppression of vocal utterances is carried out by the mediofrontal cortex (including anterior cingulate gyrus and supplementary as well as pre-supplementary motor area). Voluntary control over the acoustic structure of vocalizations is carried out by the motor cortex via pyramidal/corticobulbar as well as extrapyramidal pathways. The most important extrapyramidal pathway seems to be the connection motor cortex–putamen–substantia nigra–parvocellular reticular formation–phonatory motoneurones. The motor cortex depends upon a number of inputs for fulfilling its task. It needs a cerebellar input via the ventrolateral thalamus for allowing a smooth transition between consecutive vocal elements. It needs a proprioceptive input from the phonatory organs via nucl. ventralis posterior medialis thalami, somatosensory cortex and inferior parietal cortex. It needs an input from the ventral premotor and prefrontal cortex, including Broca's area, for motor planning of longer purposeful utterances. And it needs an input from the supplementary and pre-supplementary motor area which give rise to the motor commands executed by the motor cortex.

Introduction

Vocal behaviour can take place on different levels of complexity. The lowest level is represented by a completely genetically determined vocal reaction. An example is the infant's pain shrieking. A heavy blow against the body, for instance, elicits shrieking from birth on. An infant does not need prior experience with this stimulus in the form of a pairing with another, unconditioned stimulus. It also does not need to hear shrieking from other humans in order to be able to produce it. The infant's shrieking reaction to a painful stimulus thus may be considered as a reflex behaviour, comparable to coughing induced by an irritating stimulus in the glottis or swallowing elicited by a food bolus entering the pharynx.

When the child has grown up, pain does not automatically elicit shrieking. In adolescents and adults, shrieking can be suppressed, even if pain is severe; and, on the other hand, shrieking can be produced in the complete absence of pain—for instance, on the stage by an actor mimicking pain. As we will see in the following, this higher level of vocal behaviour depends on brain structures dispensable for the production of reflex-like vocal reactions.

Another type of higher-level vocal behaviour is vocal imitation. An example are the songs of humpback whales [1]. In this case, there is not only voluntary control over the initiation process of an (innate) vocal pattern, but also a voluntary control over the acoustic structure of the pattern, that is, vocal plasticity. This level of vocal behaviour, although common in birds, is only rarely found in mammals. The behaviour is dependent on a number of brain areas in addition to those involved in voluntary control of innate vocal patterns.

Finally, the most complex level of vocal behaviour is represented by human speech. In this case, there is not only voluntary control on initiation and acoustic structure of the vocal utterances, but also attribution of specific meanings to these utterances. The utterances, furthermore, are organised in the form of long sequences structured according to syntactical and grammatical rules.

The present review is an attempt to identify brain areas involved in the control of vocal behaviour at each of the aforementioned complexity levels.

Section snippets

Peripheral apparatus

Vocal behaviour, irrespective of its innate or learned character, represents a complex motor pattern made up of essentially three components: vocal fold adduction, respiratory activity (usually expiration) and supralaryngeal movements (articulation).

Premotor neurones

The production of a specific vocal pattern requires that the widely dispersed phonatory motoneurone groups are coordinated in their activity. Principally, this could be done in two ways: either by reciprocal interconnections between all the motoneurone groups involved in phonation, or by superordinate structures controlling the motoneurones differentially. Neuroanatomical studies show that direct interconnections between the different phonatory motoneurone pools are almost completely absent [54]

Mediofrontal cortex

The cortex within the interhemispheric fissure contains two areas that have been related to vocal behaviour: one is the anterior cingulate gyrus, the other the supplementary motor area (SMA). Both areas have been reported to produce vocalization when electrically stimulated. The SMA, however, has been found to produce vocalization only in humans, not in other mammals. The anterior cingulate gyrus, in contrast, produces vocalization in non-human mammals, such as the rhesus monkey, squirrel

Conclusion

The central control of vocal behaviour is hierarchically organized (Fig. 10). The lowest level is represented by a neural network consisting of essentially the parvocellular and dorsal medullary reticular formation, nucl. retroambiguus and solitary tract nucleus. This network serves to integrate laryngeal, respiratory and articulatory activity. In the case of innate vocal patterns, it also seems to be involved in pattern generation. The network has direct access to the phonatory motoneurones.

References (301)

  • K. Nakazawa et al.

    Role of pulmonary afferent inputs in vocal on-switch in the cat

    Neurosci Res

    (1997)
  • L.A.G. Segade et al.

    Contralateral projections of trigeminal mandibular primary afferents in the guinea pig as seen by transganglionic transport of horseradish peroxidase

    Brain Res

    (1990)
  • Y. Takeuchi et al.

    Afferent fibers in the hypoglossal nerve: a horseradish peroxidase study in the cat

    Brain Res Bull

    (1990)
  • G. Thoms et al.

    Common input of the cranial motor nuclei involved in phonation in squirrel monkey

    Exp Neurol

    (1987)
  • A.D. Miller et al.

    Brainstem projections to cats' upper lumbar spinal cord: implications for abdominal muscle control

    Brain Res

    (1989)
  • A. Kolta et al.

    Identification of brainstem interneurons projecting to the trigeminal motor nucleus and adjacent structures in the rabbit

    J Chem Neuroanat

    (2000)
  • Y. Sahara et al.

    Hypoglossal premotor neurons in the rostral medullary parvocellular reticular formation participate in cortically-induced rhythmical tongue movements

    Neurosci Res

    (1996)
  • M. Takada et al.

    Distribution of premotor neurons for the hypoglossal nucleus in the cat

    Neurosci Lett

    (1984)
  • Y.Q. Li et al.

    Identification of premotor interneurons which project bilaterally to the trigeminal motor, facial or hypoglossal nuclei. A fluorescent retrograde double-labeling study in the rat

    Brain Res

    (1993)
  • Y.Q. Li et al.

    Premotor neurons projecting simultaneously to orofacial motor nuclei by sending their branched axons. A study with a fluorescent retrograde double-labeling technique in the rat

    Neurosci Lett

    (1993)
  • K. Ezure et al.

    Location and axonal projection of one type of swallowing interneurons in cat medulla

    Brain Res

    (1993)
  • U. Jürgens et al.

    Glutamate-induced vocalization in the squirrel monkey

    Brain Res

    (1986)
  • A. Kirzinger et al.

    The effects of brain stem lesions on vocalization in the squirrel monkey

    Brain Res

    (1985)
  • L. Lüthe et al.

    Neuronal activity in the medulla oblongata during vocalization. A single-unit recording study in the squirrel monkey

    Behav Brain Res

    (2000)
  • H.H. Ellenberger et al.

    Brainstem connections of the rostral ventral respiratory group of the rat

    Brain Res

    (1990)
  • I. Billig et al.

    Transneuronal tracing of neuronal pathways controlling an abdominal muscle, rectus abdominis, in the ferret

    Brain Res

    (1999)
  • A. Katada et al.

    Functional role of ventral respiratory group expiratory neurons during vocalization

    Neurosci Res

    (1996)
  • Y. Yajima et al.

    The midbrain central gray substance as a highly sensitive neural structure for the production of ultrasonic vocalization in the rat

    Brain Res

    (1980)
  • R. Bandler et al.

    Integrated defence reaction elicited by excitatory amino acid microinjection in the midbrain periaqueductal grey region of the unrestrained cat

    Brain Res

    (1988)
  • C.-L. Lu et al.

    Effects of chemical stimulation in the periaqueductal gray on vocalization in the squirrel monkey

    Brain Res Bull

    (1993)
  • K. Payne et al.

    Large scale changes over 19 years in songs of humpback whales in Bermuda

    Z Tierpsychol

    (1985)
  • S.P. Zhang et al.

    Brain stem integration of vocalization: role of the midbrain periaqueductal gray

    J Neurophysiol

    (1994)
  • I. Hiroto et al.

    Electromyographic investigation of the intrinsic laryngeal muscles related to speech sounds

    Ann Otol Rhinol Laryngol

    (1967)
  • R.E. Stone et al.

    Relative movements of the thyroid and cricoid cartilages assessed by neural stimulation in dogs

    Acta Otolaryng

    (1974)
  • Y. Yoshida et al.

    Peripheral nervous system in the larynx. An anatomical study on the motor, sensory and autonomic nerve fibers

    Folia Phoniatr

    (1992)
  • P. Gauthier et al.

    Mise en évidence électrophysiologique de bifurcations d'axone dans le nerf recurrent laryngé

    J Physiol

    (1980)
  • B. Roubeau et al.

    Electromyographic activity of strap and cricothyroid muscles in pitch change

    Acta Oto-Laryngol

    (1997)
  • M. Hirano et al.

    The sternohyoid muscle during phonation

    Acta Oto-Laryngol

    (1967)
  • J. Ohala et al.

    The function of the sternohyoid muscle in speech

    Res Inst Logoped Phoniatr, Ann Bull

    (1970)
  • T. Ueyama et al.

    The distribution of infrahyoid motoneurons in the cat: a retrograde horseradish peroxidase study

    Anat Embryol

    (1988)
  • A. Kirzinger et al.

    Motoneuronal location of external laryngeal and hyoid muscles involved in primate phonation

    J Brain Res

    (1994)
  • U. Jürgens et al.

    Respiratory muscle activity during vocalization in the squirrel monkey

    Folia Primatol

    (1991)
  • M.H. Draper et al.

    Respiratory muscles in speech

    J Speech Hear Res

    (1959)
  • J. Newsom Davis et al.

    The proprioceptive reflex control of the intercostal muscles during their voluntary activation

    J Physiol

    (1970)
  • M. Estenne et al.

    Chest wall motion and expiratory muscle use during phonation in normal humans

    J Appl Physiol

    (1990)
  • H. Sakamoto et al.

    An anatomical analysis of the relationships between the intercostal nerves and the thoracic and abdominal muscles in man

    Acta Anat

    (1996)
  • S. Schriever et al.

    Location of respiratory motoneurons involved in phonation. An HRP study in the squirrel monkey

    J Hirnforsch

    (1989)
  • A.D. Miller

    Localization of motoneurons innervating individual abdominal muscles of the cat

    J Comp Neurol

    (1987)
  • G. Holstege et al.

    Spinal cord location of the motoneurons innervating the abdominal, cutaneous maximus, latissimus dorsi and longissimus dorsi muscles in the cat

    Exp Brain Res

    (1987)
  • M. Hoshiko

    Electromyographic investigation of the intercostal muscles during speech

    Arch Phys Med Rehabil

    (1962)
  • Cited by (0)

    View full text