Uwe Jürgens

The neural control of vocalization in mammals: a review.

The review describes a model of vocal control, based mainly on research in the squirrel monkey, which consists of two hierarchically organized pathways. One runs from the anterior cingulate cortex via the periaqueductal gray (PAG) into the reticular formation of pons and medulla oblongata, and from there to the phonatory motoneurons. This pathway controls the readiness to vocalize. Although the anterior cingulate cortex in this pathway plays a role in voluntary initiation of vocal behavior, the PAG is involved in vocal gating at a more elementary level. The second pathway runs from the motor cortex via the reticular formation to the phonatory motoneurons and includes two feedback loops providing the motor cortex with preprocessed information needed by the latter to generate the final motor commands. One of these feedback loops involves the basal ganglia and the other the cerebellum. The motor cortex together with its feedback loops is involved in the production of learned vocal patterns. These structures seem to be dispensable, however, for the production of innate vocal patterns, such as the nonverbal emotional vocal utterances of humans and most nonhuman mammalian vocalizations. These innate vocal patterns seem to be generated in the pontine and medullary reticular formation.

ON THE VOCAL EXPRESSION OF EMOTION. A MULTI-PARAMETRIC ANALYSIS OF DIFFERENT STATES OF AVERSION IN THE SQUIRREL MONKEY

There is general agreement that in non-human primates, the emotional state of a caller is reflected in the vocal structure. But only few studies describe call features characterizing such correlates. This is mainly due to the fact that it is difficult to identify the emotional state of a caller. In the present study, we analysed calls from a study (Jurgens, 1979) in which squirrel monkeys had been given the opportunity to control vocalization-eliciting brain stimulation. In this way, the aversive or hedonistic quality of the emotional state underlying the production of specific calls could be determined. 758 of the recorded calls, representing 8 different call types, given by 25 subjects, were analysed in order to find out whether differences in the degree of aversion are reflected by specific acoustic parameters. It was found that an increase in aversion is parallelled, depending upon the call type, by an upward shift of maximal energy in the power spectrum, an increase in frequency range and/or an increase in the ratio of nonharmonic to harmonic energy.

Efferent subcortical projections of the laryngeal motorcortex in the rhesus monkey.

In order to better understand the descending voluntary vocal control pathway, the efferent subcortical projections of the laryngeal motorcortex were studied in the rhesus monkey (Macaca mulatta). For this purpose, the left motorcortex was exposed in three animals under narcosis. By electrical brain stimulation, sites were identified yielding vocal fold adduction. Effective sites were injected with the anterograde tracer biotin dextran amine. Subcortical projections could be traced within the forebrain to the putamen, caudate nucleus, claustrum, zona incerta, field H of Forel and a number of thalamic nuclei, with the heaviest projections to the nuclei ventralis lateralis, ventralis posteromedialis, including its parvocellular part, medialis dorsalis, centralis medialis, centrum medianum and reuniens. In the midbrain, labeling was found in the deep mesencephalic nucleus. In the lower brainstem, fibers terminated in the pontine and medullary reticular formation, locus coeruleus, nucleus subcoeruleus, medial parabrachial nucleus, nucleus of the spinal trigeminal tract, solitary tract nucleus and facial nucleus. No projections were found to the nucl. ambiguus. The fact that monkeys, in contrast to humans, lack a direct connection of the motorcortex with the laryngeal motoneurons suggests that this connection has evolved in the last few million years and might represent one of the factors that made speech evolution possible.

Acoustic Analyses of Developmental Changes and Emotional Expression in the Preverbal Vocalizations of Infants

The nonverbal vocal utterances of seven normally hearing infants were studied within their first year of life with respect to age- and emotion-related changes. Supported by a multiparametric acoustic analysis it was possible to distinguish one inspiratory and eleven expiratory call types. Most of the call types appeared within the first two months; some emerged in the majority of infants not until the 5th (laugh) or 7th month (babble). Age-related changes in acoustic structure were found in only 4 call types (discomfort cry, short discomfort cry, wail, moan). The acoustic changes were characterized mainly by an increase in harmonic-to-noise ratio and homogeneity of the call, a decrease in frequency range and a downward shift of acoustic energy from higher to lower frequencies. Emotion-related differences were found in the acoustic structure of single call types as well as in the frequency of occurrence of different call types. A change from positive to negative emotional state was accompanied by an increase in call duration, frequency range, and peak frequency (frequency with the highest amplitude within the power spectrum). Negative emotions, in addition, were characterized by a significantly higher rate of crying, hic and ingressive vocalizations than positive emotions, while positive emotions showed a significantly higher rate of babble, laugh, and raspberry.

VOCAL DEVELOPMENT IN SQUIRREL MONKEYS

Six squirrel monkeys (Saimiri sciureus) were studied for their vocal development over the first 20 months of life, using a multi-parametric acoustic analysis. Four of the animals were normally raised, one animal (Kaspar Hauser) was deprived of adult species-specific calls, one animal was congenitally deaf. The study showed that in all 12 call types under investigation, age-related changes in one or the other acoustic parameter occurred. The degree to which vocal structures changed, was call type-specific, with some calls showing dramatic changes and others showing only minor changes. Most changes occurred within the first four months; some lasted up to 10 months. All call types showed a high variability throughout the 20 months study period. Only five of the 12 call types showed a reduction in variability over time. Both acoustically deprived animals remained within the variability range of the normally raised animals, suggesting that the ontogenetic changes found were mainly maturational.

On the Role of the Pontine Brainstem in Vocal Pattern Generation: A Telemetric Single-Unit Recording Study in the Squirrel Monkey

In a recent study, we localized a discrete area in the ventrolateral pontine brainstem of squirrel monkeys, which seems to play a role in vocal pattern generation of frequency-modulated vocalizations. The present study compares the neuronal activity of this area with that of three motoneuron pools involved in phonation, namely the trigeminal motor nucleus, facial nucleus, and nucleus ambiguus. The experiments were performed in freely moving squirrel monkeys (Saimiri sciureus) during spontaneous vocal communication, using a telemetric single-unit recording technique. We found vocalization-related activity in all motoneuron pools recorded. Each of them, however, showed a specific profile of activity properties with respect to call types uttered, syllable structure, and pre-onset time. Different activity profiles were also found for neurons showing purely vocalization-correlated activity, vocalization- and mastication-correlated activity, and vocalization- and respiration-correlated activity. By comparing the activity properties of the proposed vocal pattern generator with the three motoneuron pools, we show that the pontine vocalization area is, in fact, able to control each of the three motoneuron pools during frequency-modulated vocalizations. The present study thus supports the existence of a vocal pattern generator for frequency-modulated call types in the ventrolateral pontine brainstem.

Afferents of vocalization-controlling periaqueductal regions in the squirrel monkey

In order to determine the input of vocalization-controlling regions of the midbrain periaqueductal gray (PAG), wheat germ agglutinin-horseradish peroxidase was injected in six squirrel monkeys (Saimiri sciureus) at PAG sites yielding vocalization when injected with the glutamate agonist homocysteic acid. Brains were scanned for retrogradely labeled areas common to all six animals. The results show that the vocalization-eliciting sites receive a widespread input, with the heaviest projections coming from the surrounding PAG, dorsomedial and ventromedial hypothalamus, medial preoptic region, substantia nigra pars diffusa, zona incerta and reticular formation of the mesencephalon, pons, and medulla. The heaviest cortical input reaches the PAG from the mediofrontal cortex. Moderate to weak projections come from the insula, lateral prefrontal, and premotor cortex as well as the superior and middle temporal cortex. Subcortical moderate to weak projections reach the PAG from the central and medial amygdala, nucleus of the stria terminalis, septum, nucleus accumbens, lateral preoptic region, lateral and posterior hypothalamus, globus pallidus, pretectal area, deep layers of the superior colliculus, the pericentral inferior colliculus, mesencephalic trigeminal nucleus, locus coeruleus, substantia nigra pars compacta, dorsal and ventral raphe, vestibular nuclei, spinal trigeminal nucleus, solitary tract nucleus, and nucleus gracilis. The input of the periaqueductal vocalization-eliciting regions thus is dominated by limbic, motivation-controlling afferents; input, however, also comes from sensory, motor, arousal-controlling, and cognitive brain areas.

Cortico-cortical projections of the motorcortical larynx area in the rhesus monkey.

The efferent cortico-cortical projections of the motorcortical larynx area were studied in three rhesus monkeys (Macaca mulatta), using biotin dextranamine as anterograde tracer. Identification of the larynx area was made with the help of electrical brain stimulation and indirect laryngoscopy. Heavy projections were found into the surrounding ventral and dorsal premotor cortex (areas 6V and D), primary motor cortex (area 4), the homolog of Brocas area (mainly area 44), fronto- and parieto-opercular cortex (including secondary somatosensory cortex), agranular, dysgranular and granular insula, rostral-most primary somatosensory cortex (area 3a), supplementary motor area (area 6M), anterior cingulate gyrus (area 24c) and dorsal postarcuate cortex (area 8A). Medium projections could be traced to the ventrolateral prefrontal and lateral orbital cortex (areas 47L and O), the primary somatosensory areas 3b and 2, the agranular and dysgranular insula, and the posteroinferior parietal cortex (area 7; PFG, PG). Minor projections ended in the lateral and dorsolateral prefrontal cortex (areas 46V and 8B), primary somatosensory area 1 and cortex within the intraparietal sulcus (PEa) and posterior sulcus temporalis superior (TPO). Due to its close spatial relationship to the insula on the one hand and the premotor cortex on the other, the larynx area shows projections which, in some respects, are not typical for classical primary motor cortex.

Audio–vocal interaction in the pontine brainstem during self-initiated vocalization in the squirrel monkey

The adjustment of the voice by auditory input happens at several brain levels. The caudal pontine brainstem, though rarely investigated, is one candidate area for such audio–vocal integration. We recorded neuronal activity in this area in awake, behaving squirrel monkeys (Saimiri sciureus) during vocal communication, using telemetric single‐unit recording techniques. We found audio–vocal neurons at locations not described before, namely in the periolivary region of the superior olivary complex and the adjacent pontine reticular formation. They showed various responses to external sounds (noise bursts) and activity increases (excitation) or decreases (inhibition) to self‐produced vocalizations, starting prior to vocal onset and continuing through vocalizations. In most of them, the responses to noise bursts and self‐produced vocalizations were similar, with the only difference that neuronal activity started prior to vocal onset. About one‐third responded phasically to noise bursts, independent of whether they increased or decreased their activity to vocalization. The activity of most audio–vocal neurons correlated with basic acoustic features of the vocalization, such as call duration and/or syllable structure. Auditory neurons near audio–vocal neurons showed significantly more frequent phasic response patterns than those in areas without audio–vocal activity. Based on these findings, we propose that audio–vocal neurons showing similar activity to external acoustical stimuli and vocalization play a role in olivocochlear regulation. Specifically, audio–vocal neurons with a phasic response to external auditory stimuli are candidates for the mediation of basal audio–vocal reflexes such as the Lombard reflex. Thus, our findings suggest that complex audio–vocal integration mechanisms exist in the ventrolateral pontine brainstem.

Localization of a vocal pattern generator in the pontine brainstem of the squirrel monkey

Very little is known about the coordination of muscles involved in mammalian vocalization at the level of single neurons. In the present study, a telemetric single‐unit recording technique was used to explore the ventrolateral pontine brainstem for vocalization‐correlated activity in the squirrel monkey during vocal communication. We found a discrete area in the reticular formation just above the superior olivary complex showing vocalization‐correlated activity. These neurons showed an increase in neuronal activity exclusively just before and during vocalization; none of them was active during mastication, swallowing or quiet respiration. Furthermore, the neuronal activity of these neurons reflected acoustic features, such as call duration or syllable structure of frequency‐modulated vocalization, directly. Based on these findings and previously reported anatomical data, we propose that this area serves as a vocal pattern generator for frequency‐modulated call types.