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On the neural control of mammalian vocalization
135
TINS -June 1981
On the neural control of mammalian vocalization
either cluster for any given defective if the two pigments have identical absorption spectra the observer is a dichromat; if the two are slightly different, the observer is an anomalous trichromat. This perspective therefore requires a U. JOrgensand D. Ploog closer examination of the way visual pigments of a given class - including the most ubiquitous-rhodopsin - differ in the eye of one individual from that of another. The term vocalization is used here to denote all categories oflaryngeally produced, speciesIndeed, the microspectrophotometric specific communications, with the exception o f language. This definition includes not only analysis of rhodopsin in frog retinas has animal calls but also human nonverbal sounds such as laughing, crying, moaning, etc. as already yielded observations consistent well as emotional intonations used in the ex 9ression o f rage, tenderness, fright or triumph. with this view, though much chemistry is Mammalian vocalization is to a large extent genetically pre-programmed -the basic acousneeded to shed light on the molecular basis tic patterns do not need to be learnt. It has been found that a number o f structures crucial for of this variance. Can this provide the key to the production o f speech (e.g. sensorimotor cortex, thalamus, cerebellum) are not needed a question that, until now, has baffled the for vocalization while, conversely, brain structures which are not thought to play any role in imagination of even the most gifted biol- the production o f learnt utterances (e.g. limb& cortex, amygdala, hypothalamus) clearly ogist: what are the details of the evolution- have some control. The folio wing report attempts to describe the neural control mechanisms ary processes from which the four visual for vocalization in the form o f a hierarchically organized system. pigments of the human retina have emerged beginning (as they must certainly Mammalian vocalization involves the co- the upper cervical spinal cord. Thus, even have begun) with a primitive ancestor ordination of respiratory, laryngeal and at the lowest functional level vocalization whose eyes had only a single visual pig- articulatory (supra-laryngeal) movements. involves an extensive system reaching from ment? The motoneurones responsible for the pons to the lower spinal cord. respiratory movement lie in the anterior If one cuts the brain stem in a cat or dog Reading list horn of the cervical, thoracic and upper immediately rostral to the trigeminal 1 Alpern, M. (1979) J. Physiol. (London) 288, lumbar spinal cord, those controlling glotmotor nucleus (i.e. at the rostral end of the 85-105 tis closure are found in the nucleus 'phomatory motoneurone pool'), the ani2 Alpern, M. and Moelter, J. (1977) J. Physiol. ambiguus, whilst neurones responsible for mals become mute. Clearly, the neuronal (London) 266, 647-675 the control of articulatory movements are information exchange occurring between 3 Alpern, M. and Pugh, E. N., Jr (1977) J. Physiol. (London) 266, 613-646 localized in the trigeminal motor nucleus, the cranial motor nuclei, spinal respiratory 4 Alpern, M. and Torii, S. (1968) J. Gen Physiol. facial nucleus, rostral nucleus ambiguus, motoneurones and the somatosensory 52,717-737; 738-749 hypoglossal nucleus and anterior horn of information entering via the lower brain 5 A lpern, M. and Wake, T. (1977)L Physiol. (London) 266, 595-612 6 Baker, H. D. and Rushton, W. A. H. (1963)L Physiol. (London) 168, 31-33 7 Bastian, B. L. (1976)Ph.D. dissertation, University of Michigan 8 Bowmaker, J. K. and DartnalL H. J. A. (1980)./. Physiol. (London) 298, 501-511 9 Koenig, A. and Dieterici, C. (1886)S. B. Akad. Wiss, Berlin, 1886, 805-829 10 Ruddock, K. H. and Naghshineh, S. (1974) Mod. Probl. Ophth. 13,210-214 11 Rushton, W. A. H. (1963)Z Physiol. (London) 168, 345-359; 360-373; 374--388; ( 1 9 6 5 ) Z Physiol. (London) 176, 24-37; 38--45 12 Stiles, W. S. and Butch, J. M. (1955) Opt. Acta 2, 176--181 Mathew Alpern is at the Vision Research Laboratory, Box 56, Michigan University, Ann Arbor, MI 48109, U.S.A.
Fig, 1. Sagittal section o f the squirrel monkey "sbrabt sho wing all areas which yield phonation when stimulated electrically. From the black areas naturally sounding, .wecies-speeific calls can be obtained, the white-dotted areas produce calls which sound artificial. Abbreviations: am: amygdala; aq: periaqueductal grey; c: anterior commissure; ch: chiasma opticum; coli: coliiculus inferior; cols: colliculus superior; f: fornix; gc: gyms cinguli; gr: gyrus rectus: m: mamillary body; rod: mediodorsal thalamic nucleus; oi: in ferior olive; po: [x~ntine grey; re: midbrain reticular formation; s: sept urn; st: stria terminalis.
El',e~icr/Norlh-HLdlantlFJiomcdicalPrc~ I~1
136 stem and spinal cord is not sufficient for spontaneous vocalization; a co-ordinating or facilitating input from a higher cerebral level is also required, In dogs 7 and cats ~ transections rostral to the inferior colliculus do not abolish vocalization, whereas transections caudal to this point do. So does the whole caudal midbrain or only a specific part of it control vocalization? In cats and monkeys it has been shown that animals are muted by lesions limited to the periaqueductal grey and the adjacent tegmentum. Whereas destruction of all the other midbrain structures it has no effect on vocalization ~.~. Apart from these lesion studies, there are a number of additional observations corroborating the importance of the caudolateral periaqueductal region. For instance, electrical stimulation triggers speciesspecific vocalizations from this area. The periaqueductal vocalizations have a shorter latency 4 when compared to those of sounds produced by stimulation of other parts of the brain. In addition, anatomical studies have shown that the periaqueductal vocalization area projects directly to the laryngeal motoneurones in the nucleus ambiguus s. Finally, it has been found that production of periaqueductal vocalization is not dependent on the animal's motivational state. In other words, the vocalizations produced by stimulation of the periaqueductal region are not secondary reactions due to stimulation-induced motivational changes but are directly triggered behavioural patterns 3.
TINS-June
1981
AP1B
(I)
APIO
(ll)
(111)
Brain areas involved
The caudal periaqueductal region is not the only brain area from which vocalization can be obtained by electrical stimulation. Fig. 1 summarises all the areas from which vocalizations can be elicited in the squirrel monkey. These are wide-spread, reaching from the forebrain into the medulla. They Ala-& include parts of the anterior limbic cortex, septum, amygdala, preoptic region, hypothalamus, midline thalamus, ventrolateral midbrain tegmentum and ventrolateral reticular formation of the medulla. All of them yield natural0V) sounding species-specific calls when stimulated electrically - with one exception. Stimulation of the meduallary vocalization area, indicated by the white dots in Fig. 1, produces calls which sound artificial, indiLarynx cating that the stimulation directly affects w~calization-co-ordination structures. In Fig. 2. Scheme of hierarchical control of vocalization: All brain urea~ indicated by a dot yield vocalization when all the other areas, it must be assumed that electrically ~timulated. All lines interconnecting the dot.~ represent onatomically verified direct projection.~ (leading the stimulation interferes with a control in rostrocaudal direction). The dots indicate in (I) the anterior"cingulate gyrt~, in (l l) the b~tsalamygdaloid tu~clel~s, dors'omedid and lateral hypothahonus and midline thalamus, in Illl ) the periaqueth~ctal grey and laterally borderlevel higher than that responsible for the ing tegmentum, in (IV) tile m¢cl. amhiguu,~ and ~urrolmding reticuhlr formotion (tile nltcl, ambigltus it~'elfonly motor-co-ordination. viehls i,solated movement,~ of the voeal fi~lds: phonation can he ohUdned, however, from its immediate vicinity), For Stimulation of the hypothalamus, rnid- fitrther e~planation, see the te~t.
l
TINS - June 1981
conditioning task. Single-unit recording studies reveal that there are neurones in the anterior cingulate cortex which change their activity 200-800 ms prior to vocalizations made in the conditioning experimentL If these findings are considered together with the somewhat surprising fact that cingulate lesions do not affect 'spontaneous' vocal behaviour (neither acoustic structure nor frequency of occurrence), it may be concluded that the anterior cingulate cortex is probably tion. This requires a facilitatory input from involved in the 'voluntary' control of vocalization. Finally, it may be appropriate to comment briefly on the sensorimotor cortical face area which plays an important part in the verbal vocal behaviour of man but seems to lack importance in animal vocalization. While its destruction causes severe speech disturbances (dysarthria) in man, ablation in the monkey neither changes the Cortical control of voluntary vocalization acoustic structure of vocalizations nor their Among those vocalization-eliciting brain frequency of occurrence (this holds for areas dependent on an intact periaqueduc- spontaneous as well as conditioned vocaltal region, the anterior cingulate cortex izationS). The reason for this discrepancy holds an outstanding position. In contrast probably lies in the fact that speech must be to all the other, secondary, vocalization learnt, whereas monkey vocalizations are areas, there is no relationship here between essentially innate - that is, genetically preelicited call-type and accompanying emo- programmed motor patterns ~°. If this tional state. Indeed, if the animal is able to explanation is correct, then genetically switch on or switch off the brain stimula- pre-programmed vocal patterns in man, tion itself, then depending on the site of such as laughing or crying, should be prestimulation the same call type can be served even after bilateral lesions in the associated with self-stimulation avoidance cortical face area, In fact this has been behaviour or indifference. This implies that found to be the case in patients with the same call type can be accompanied by a pseudobulbar palsy where the lesion bilatpleasurable, aversive or neutral emotional erally interrupts the output of the cortical state 3. In this respect the anterior cingulate face area. These patients are unable to cortex is similar to the periaqueductal reg- utter a single word but show compulsory ion in that the vocalizations cannot be laughing and crying. interpreted as expressions of stimulationWe may summarize the cerebral control induced motivational changes but seem to of mammalian vocalization, and probably represent specific motor responses. nonverbal emotional utterances in man, in In addition to the self-stimulation the following way. The vocalizationresults, there are other observations which control system is organized hierarchically suggest a prominent role for the anterior (Fig. 2). The lowest level being represented cingulate cortex in vocalization control. by the phonatory motoneurones, primary Monkeys trained to vocalize for a food sensory neurones and reticular and spinal reward, are not able to master this task interneurones. Anatomically this level after ablation of the anterior cingulate cor- consists of widely scattered neuronal poputex 8, but can still learn a lever-pressing lations reaching from the rostral pons line thalamus, amygdala and septum also produces vocalization but all show relatively long latencies (> 100 ms), high habituation and a clear correlation between elicited call type and accompanying emotional stateL These vocalizations are probably a consequence of stimulationinduced motivational changes rather than pure motor responses. In addition periaqueductal vocalizations are not affected by lesions in these areas, whereas, calls elicited by stimulation in hypothalamus, etc. are abolished by periaqueductal lesions2. Since the hypothalamus, midline thalamus, and amygdala do not project directly to the cranial motor nuclei involved in vocalization, but they all had a direct projection to the periaqueductal area, it appears that all secondary vocalization areas feed their activity through the periaqueductal region 5.
137 (trigeminal nucleus) down to the upper lumbar spinal cord (expiratory motoneurones). Its function is to coordinate respiratory, laryngeal and articulatory activity. However, this level itself is not capable of initiating vocalizathe next level, the caudal periaqueductal grey and laterally adjacent tegmentum (Fig. 2, III). The periaqueductal region probably serves to couple specific motivational states to their corresponding vocal expressions by co-ordinating the diverse external and internal stimuli which normally induce an animal to generate a call. The periaqueductal region receives its input partly from the limbic motivationcontrol areas, such as the hypothalamus, midline thalamus, amygdala, septum (Fig. 2, I1), partly via more direct sensory pathways including collaterals from the spinothalamic tract and projections from superior and inferior colliculus, and partly from the anterior cingulate cortex. This (Fig. 2, I) represents the highest level within the system. While it is dispensable for (involuntary) vocal reactions to emotional stimuli, it is clearly needed for the voluntary control of vocalization.
Reading list 1 Bazen, H. C. and Penfield,W. G. (1922) Brain 45, 185-265 2 Hunsperger, R. W. (1956)Helv. Physiol. Pharrnacol. Acta 14, 70-92 3 Jiirgens,U. (1976) Exp. Brain Res. 26, 203--214 4 Ji.irgens,U. and Ploog, D. (1970)Exp. Brain Res. 10, 532-554 5 J0rgens, U. and Pratt, R. (1979) Brain Res. 167. 367-378 6 Kelly,A. H., Beaton, L. E. and Magoun, H. W. (1946) J, Neurophysiol. 9, 181-189 7 Onodi, A. (1902) Die Anatomie und Physiologie der Kehlkopfnerven, Coblentz,Berlin 8 Sutton, D., Larson, C. and Lindeman, R. C. (1974) Brain Res. 71,61-75 9 Sutton, D., Samson, H. H, and Larson, C. R. (1978) in Recent Advances in Primatology (Chivers, D. J, and Herbert, J. eds), Vol. 1, Academic Press, New York 10 Winter,P., Handley,P., Ploog, D. and Schon, D. (1974) Behaviour 47, 230-239
D. Ploog is director o f the Max-Planck-lnstitute for Psychiatry in Munich (F.R. G. ) and head of the Dept. o f Primate Behaviour. U. Jiirgens is a senior research associate in the Department of Primate Behaviour.
TINS -June 1981
On the neural control of mammalian vocalization
either cluster for any given defective if the two pigments have identical absorption spectra the observer is a dichromat; if the two are slightly different, the observer is an anomalous trichromat. This perspective therefore requires a U. JOrgensand D. Ploog closer examination of the way visual pigments of a given class - including the most ubiquitous-rhodopsin - differ in the eye of one individual from that of another. The term vocalization is used here to denote all categories oflaryngeally produced, speciesIndeed, the microspectrophotometric specific communications, with the exception o f language. This definition includes not only analysis of rhodopsin in frog retinas has animal calls but also human nonverbal sounds such as laughing, crying, moaning, etc. as already yielded observations consistent well as emotional intonations used in the ex 9ression o f rage, tenderness, fright or triumph. with this view, though much chemistry is Mammalian vocalization is to a large extent genetically pre-programmed -the basic acousneeded to shed light on the molecular basis tic patterns do not need to be learnt. It has been found that a number o f structures crucial for of this variance. Can this provide the key to the production o f speech (e.g. sensorimotor cortex, thalamus, cerebellum) are not needed a question that, until now, has baffled the for vocalization while, conversely, brain structures which are not thought to play any role in imagination of even the most gifted biol- the production o f learnt utterances (e.g. limb& cortex, amygdala, hypothalamus) clearly ogist: what are the details of the evolution- have some control. The folio wing report attempts to describe the neural control mechanisms ary processes from which the four visual for vocalization in the form o f a hierarchically organized system. pigments of the human retina have emerged beginning (as they must certainly Mammalian vocalization involves the co- the upper cervical spinal cord. Thus, even have begun) with a primitive ancestor ordination of respiratory, laryngeal and at the lowest functional level vocalization whose eyes had only a single visual pig- articulatory (supra-laryngeal) movements. involves an extensive system reaching from ment? The motoneurones responsible for the pons to the lower spinal cord. respiratory movement lie in the anterior If one cuts the brain stem in a cat or dog Reading list horn of the cervical, thoracic and upper immediately rostral to the trigeminal 1 Alpern, M. (1979) J. Physiol. (London) 288, lumbar spinal cord, those controlling glotmotor nucleus (i.e. at the rostral end of the 85-105 tis closure are found in the nucleus 'phomatory motoneurone pool'), the ani2 Alpern, M. and Moelter, J. (1977) J. Physiol. ambiguus, whilst neurones responsible for mals become mute. Clearly, the neuronal (London) 266, 647-675 the control of articulatory movements are information exchange occurring between 3 Alpern, M. and Pugh, E. N., Jr (1977) J. Physiol. (London) 266, 613-646 localized in the trigeminal motor nucleus, the cranial motor nuclei, spinal respiratory 4 Alpern, M. and Torii, S. (1968) J. Gen Physiol. facial nucleus, rostral nucleus ambiguus, motoneurones and the somatosensory 52,717-737; 738-749 hypoglossal nucleus and anterior horn of information entering via the lower brain 5 A lpern, M. and Wake, T. (1977)L Physiol. (London) 266, 595-612 6 Baker, H. D. and Rushton, W. A. H. (1963)L Physiol. (London) 168, 31-33 7 Bastian, B. L. (1976)Ph.D. dissertation, University of Michigan 8 Bowmaker, J. K. and DartnalL H. J. A. (1980)./. Physiol. (London) 298, 501-511 9 Koenig, A. and Dieterici, C. (1886)S. B. Akad. Wiss, Berlin, 1886, 805-829 10 Ruddock, K. H. and Naghshineh, S. (1974) Mod. Probl. Ophth. 13,210-214 11 Rushton, W. A. H. (1963)Z Physiol. (London) 168, 345-359; 360-373; 374--388; ( 1 9 6 5 ) Z Physiol. (London) 176, 24-37; 38--45 12 Stiles, W. S. and Butch, J. M. (1955) Opt. Acta 2, 176--181 Mathew Alpern is at the Vision Research Laboratory, Box 56, Michigan University, Ann Arbor, MI 48109, U.S.A.
Fig, 1. Sagittal section o f the squirrel monkey "sbrabt sho wing all areas which yield phonation when stimulated electrically. From the black areas naturally sounding, .wecies-speeific calls can be obtained, the white-dotted areas produce calls which sound artificial. Abbreviations: am: amygdala; aq: periaqueductal grey; c: anterior commissure; ch: chiasma opticum; coli: coliiculus inferior; cols: colliculus superior; f: fornix; gc: gyms cinguli; gr: gyrus rectus: m: mamillary body; rod: mediodorsal thalamic nucleus; oi: in ferior olive; po: [x~ntine grey; re: midbrain reticular formation; s: sept urn; st: stria terminalis.
El',e~icr/Norlh-HLdlantlFJiomcdicalPrc~ I~1
136 stem and spinal cord is not sufficient for spontaneous vocalization; a co-ordinating or facilitating input from a higher cerebral level is also required, In dogs 7 and cats ~ transections rostral to the inferior colliculus do not abolish vocalization, whereas transections caudal to this point do. So does the whole caudal midbrain or only a specific part of it control vocalization? In cats and monkeys it has been shown that animals are muted by lesions limited to the periaqueductal grey and the adjacent tegmentum. Whereas destruction of all the other midbrain structures it has no effect on vocalization ~.~. Apart from these lesion studies, there are a number of additional observations corroborating the importance of the caudolateral periaqueductal region. For instance, electrical stimulation triggers speciesspecific vocalizations from this area. The periaqueductal vocalizations have a shorter latency 4 when compared to those of sounds produced by stimulation of other parts of the brain. In addition, anatomical studies have shown that the periaqueductal vocalization area projects directly to the laryngeal motoneurones in the nucleus ambiguus s. Finally, it has been found that production of periaqueductal vocalization is not dependent on the animal's motivational state. In other words, the vocalizations produced by stimulation of the periaqueductal region are not secondary reactions due to stimulation-induced motivational changes but are directly triggered behavioural patterns 3.
TINS-June
1981
AP1B
(I)
APIO
(ll)
(111)
Brain areas involved
The caudal periaqueductal region is not the only brain area from which vocalization can be obtained by electrical stimulation. Fig. 1 summarises all the areas from which vocalizations can be elicited in the squirrel monkey. These are wide-spread, reaching from the forebrain into the medulla. They Ala-& include parts of the anterior limbic cortex, septum, amygdala, preoptic region, hypothalamus, midline thalamus, ventrolateral midbrain tegmentum and ventrolateral reticular formation of the medulla. All of them yield natural0V) sounding species-specific calls when stimulated electrically - with one exception. Stimulation of the meduallary vocalization area, indicated by the white dots in Fig. 1, produces calls which sound artificial, indiLarynx cating that the stimulation directly affects w~calization-co-ordination structures. In Fig. 2. Scheme of hierarchical control of vocalization: All brain urea~ indicated by a dot yield vocalization when all the other areas, it must be assumed that electrically ~timulated. All lines interconnecting the dot.~ represent onatomically verified direct projection.~ (leading the stimulation interferes with a control in rostrocaudal direction). The dots indicate in (I) the anterior"cingulate gyrt~, in (l l) the b~tsalamygdaloid tu~clel~s, dors'omedid and lateral hypothahonus and midline thalamus, in Illl ) the periaqueth~ctal grey and laterally borderlevel higher than that responsible for the ing tegmentum, in (IV) tile m¢cl. amhiguu,~ and ~urrolmding reticuhlr formotion (tile nltcl, ambigltus it~'elfonly motor-co-ordination. viehls i,solated movement,~ of the voeal fi~lds: phonation can he ohUdned, however, from its immediate vicinity), For Stimulation of the hypothalamus, rnid- fitrther e~planation, see the te~t.
l
TINS - June 1981
conditioning task. Single-unit recording studies reveal that there are neurones in the anterior cingulate cortex which change their activity 200-800 ms prior to vocalizations made in the conditioning experimentL If these findings are considered together with the somewhat surprising fact that cingulate lesions do not affect 'spontaneous' vocal behaviour (neither acoustic structure nor frequency of occurrence), it may be concluded that the anterior cingulate cortex is probably tion. This requires a facilitatory input from involved in the 'voluntary' control of vocalization. Finally, it may be appropriate to comment briefly on the sensorimotor cortical face area which plays an important part in the verbal vocal behaviour of man but seems to lack importance in animal vocalization. While its destruction causes severe speech disturbances (dysarthria) in man, ablation in the monkey neither changes the Cortical control of voluntary vocalization acoustic structure of vocalizations nor their Among those vocalization-eliciting brain frequency of occurrence (this holds for areas dependent on an intact periaqueduc- spontaneous as well as conditioned vocaltal region, the anterior cingulate cortex izationS). The reason for this discrepancy holds an outstanding position. In contrast probably lies in the fact that speech must be to all the other, secondary, vocalization learnt, whereas monkey vocalizations are areas, there is no relationship here between essentially innate - that is, genetically preelicited call-type and accompanying emo- programmed motor patterns ~°. If this tional state. Indeed, if the animal is able to explanation is correct, then genetically switch on or switch off the brain stimula- pre-programmed vocal patterns in man, tion itself, then depending on the site of such as laughing or crying, should be prestimulation the same call type can be served even after bilateral lesions in the associated with self-stimulation avoidance cortical face area, In fact this has been behaviour or indifference. This implies that found to be the case in patients with the same call type can be accompanied by a pseudobulbar palsy where the lesion bilatpleasurable, aversive or neutral emotional erally interrupts the output of the cortical state 3. In this respect the anterior cingulate face area. These patients are unable to cortex is similar to the periaqueductal reg- utter a single word but show compulsory ion in that the vocalizations cannot be laughing and crying. interpreted as expressions of stimulationWe may summarize the cerebral control induced motivational changes but seem to of mammalian vocalization, and probably represent specific motor responses. nonverbal emotional utterances in man, in In addition to the self-stimulation the following way. The vocalizationresults, there are other observations which control system is organized hierarchically suggest a prominent role for the anterior (Fig. 2). The lowest level being represented cingulate cortex in vocalization control. by the phonatory motoneurones, primary Monkeys trained to vocalize for a food sensory neurones and reticular and spinal reward, are not able to master this task interneurones. Anatomically this level after ablation of the anterior cingulate cor- consists of widely scattered neuronal poputex 8, but can still learn a lever-pressing lations reaching from the rostral pons line thalamus, amygdala and septum also produces vocalization but all show relatively long latencies (> 100 ms), high habituation and a clear correlation between elicited call type and accompanying emotional stateL These vocalizations are probably a consequence of stimulationinduced motivational changes rather than pure motor responses. In addition periaqueductal vocalizations are not affected by lesions in these areas, whereas, calls elicited by stimulation in hypothalamus, etc. are abolished by periaqueductal lesions2. Since the hypothalamus, midline thalamus, and amygdala do not project directly to the cranial motor nuclei involved in vocalization, but they all had a direct projection to the periaqueductal area, it appears that all secondary vocalization areas feed their activity through the periaqueductal region 5.
137 (trigeminal nucleus) down to the upper lumbar spinal cord (expiratory motoneurones). Its function is to coordinate respiratory, laryngeal and articulatory activity. However, this level itself is not capable of initiating vocalizathe next level, the caudal periaqueductal grey and laterally adjacent tegmentum (Fig. 2, III). The periaqueductal region probably serves to couple specific motivational states to their corresponding vocal expressions by co-ordinating the diverse external and internal stimuli which normally induce an animal to generate a call. The periaqueductal region receives its input partly from the limbic motivationcontrol areas, such as the hypothalamus, midline thalamus, amygdala, septum (Fig. 2, I1), partly via more direct sensory pathways including collaterals from the spinothalamic tract and projections from superior and inferior colliculus, and partly from the anterior cingulate cortex. This (Fig. 2, I) represents the highest level within the system. While it is dispensable for (involuntary) vocal reactions to emotional stimuli, it is clearly needed for the voluntary control of vocalization.
Reading list 1 Bazen, H. C. and Penfield,W. G. (1922) Brain 45, 185-265 2 Hunsperger, R. W. (1956)Helv. Physiol. Pharrnacol. Acta 14, 70-92 3 Jiirgens,U. (1976) Exp. Brain Res. 26, 203--214 4 Ji.irgens,U. and Ploog, D. (1970)Exp. Brain Res. 10, 532-554 5 J0rgens, U. and Pratt, R. (1979) Brain Res. 167. 367-378 6 Kelly,A. H., Beaton, L. E. and Magoun, H. W. (1946) J, Neurophysiol. 9, 181-189 7 Onodi, A. (1902) Die Anatomie und Physiologie der Kehlkopfnerven, Coblentz,Berlin 8 Sutton, D., Larson, C. and Lindeman, R. C. (1974) Brain Res. 71,61-75 9 Sutton, D., Samson, H. H, and Larson, C. R. (1978) in Recent Advances in Primatology (Chivers, D. J, and Herbert, J. eds), Vol. 1, Academic Press, New York 10 Winter,P., Handley,P., Ploog, D. and Schon, D. (1974) Behaviour 47, 230-239
D. Ploog is director o f the Max-Planck-lnstitute for Psychiatry in Munich (F.R. G. ) and head of the Dept. o f Primate Behaviour. U. Jiirgens is a senior research associate in the Department of Primate Behaviour.