ReviewNeural pathways underlying vocal control
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.
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