Exp. Brain Res. 26, 203-214 (1976)
Experimental Brain Research 9 by Springer-Verlag1976
Reinforcing Concomitants of Electrically Elicited Vocalizations U. Jtirgens Max-Planck-Institute for Psychiatry, Kraepelinstr, 2, D - 8000 Miinchen 40, Federal Republic of Germany
Summary. In 38 squirrel monkeys 251 vocalization-producing electrode positions were tested for their positive and negative reinforcing properties. Two groups of vocalization-producing brain areas could be distinguished: One group in which the electrically elicited vocalization was independent of the accompanying reinforcement effect, and a second group in which vocalization and reinforcement effect were correlated. The first group included the anterior cingulate gyrus, the adjacent supplementary m o t o r area, gyrus rectus, ventromedial edge of the capsula interna, caudal periaqueductal gray and adjacent parabrachial region. The second group consisted of the caudatum, septum, substantia innominata, amygdala, inferior thalamic peduncle, stria terminalis, midline thalamus, ventral and periventricular hypothalamus, substantia nigra, rostral periaqueductal gray, dorsolateral midbrain t e g m e n t u m and lateral medulla. It is hypothesized that the first group contains predominantly or exclusively " p r i m a r y " Vocalization substrates; the second group is thought to be composed mainly of structures whose stimulation yields vocalization secondarily due to stimulus induced motivational changes.
Key words: Vocalization - Self-stimulation - Squirrel m o n k e y Abbreviations
a: nucl. accumbens aa: area anterior amygdalae ab: nucl. basalis amygdalae ac: nucl. centralis amygdalae al: nucl. lateralis amygdalae an: nucl. anterior thalami anl: ansa lenticularis aq: substantia grisea centralis bc: brachium conjunctivum ca: nucl. caudatus cc: corpus callosum cen: nucl. centralis superior tegmenti cent: centrum medianum
ci: capsula interna cin: cingulum ch claustrum coa: commissura anterior coli: colliculusinferior cols: colliculussuperior csp: tractus cortico-spinalis db: fasciculusdiagonalis Brocae dbc: decussatio brachii conjunctivii f: fornix gc: gyrus cinguli gh corpus geniculatum laterale gm: corpus geniculatum mediale
204 gp: globus pallidus gr: gyrus rectus gs: gyrus subcallosus h: campus Foreli ha: nucl. habenularis hi: tractus habenulo-interpeduncularis hip: hippocampus hya: area hypothalamica anterior hyl: area hypothalamica lateralis hyv: nucl, ventromedialis hypothalami in: nucl. interpeduncularis lap: nucl. lateralis posterior thalami lay: nucl. ventralis lateralis thalami le: lemniscus lateralis lem: lemniscus medialis lm: fasciculus longitudinalis medialis m: corpus mamillare md: nucl. medialis dorsalis thalami mt: tractus mamillo-thalamieus nst: nucl. striae terminalis oi: nucl. olivaris inferior o1: fasciculus olfactorius Zuckerkandl os: nucl. ofivaris superior p: pedunculus cerebri pmc: brachium pontis po: griseum pontis pro: area praeoptica
U. Jfirgens pu: nucl. pulvinaris thalami put: putamen re: formatio reticularis rep: nucl. reticularis tegmenti pontis rub: nucl. ruber s: septum sin: stria medullaris sn: substantia nigra st: stria terminalis sto: stria olfactoria lateralis subt: subthalamus tec: tractus tegmentalis centralis trz: corpus trapezoideum va: nucl. ventralis anterior thalami vpl: nucl. ventralis postero-lateralis vpm: nuel. ventralis postero-medialis zi: zona incerta II: tractus opticus IIch: chiasma nervorum opticorum III: n. oculomotorius and nucl. n. oculomotorii IV: n. and nucl. n. trochlearis VI: n. abducens and nucl. n. abducentis VII: nucl. n. facialis VIII: nucl. cochlearis IX: n. hypoglossus
Introduction V o c a l i z a t i o n can b e elicited b y e l e c t r i c a l s t i m u l a t i o n w i t h i n a r e l a t i v e l y large p a r t of t h e s q u i r r e l m o n k e y ' s b r a i n (Jiirgens a n d Ploog, 1970). T h e g r e a t n u m b e r o f r e s p o n s i v e a r e a s a n d t h e i r close r e l a t i o n to t h e l i m b i c s y s t e m suggest t h a t n o t all o f t h e m r e p r e s e n t " s p e c i f i c " v o c a l i z a t i o n areas. T h e o r e t i c a l l y , t h e r e a r e two possibilities as to h o w e l e c t r i c a l b r a i n s t i m u l a t i o n p r o v o k e s v o calization: O n e is t h a t t h e e l e c t r i c a l stimulus d i r e c t l y triggers t h e m o t o r - c o - o r d i n a t i n g m e c h a n i s m s for p h o n a t i o n ( p r i m a r y v o c a l r e s p o n s e ) ; t h e o t h e r is t h a t t h e electrical stimulus p r o d u c e s a m o r e o r less specific m o t i v a t i o n a l c h a n g e w h i c h l e a d s i n d i r e c t l y to a v o c a l u t t e r a n c e ( s e c o n d a r y v o c a l r e s p o n s e ) . T h e p r e s e n t s t u d y is an a t t e m p t to e s t a b l i s h such a d i s t i n c t i o n b y testing all vocaliz a t i o n - p r o d u c i n g b r a i n s t r u c t u r e s for t h e i r p o s i t i v e a n d n e g a t i v e r e i n f o r c i n g p r o p e r t i e s . T h e h y p o t h e s i s u n d e r l y i n g this s t u d y a s s u m e s t h a t t h e r e is a high p r o b a b i l i t y t h a t e l e c t r i c a l l y - e l i c i t e d m o t i v a t i o n a l c h a n g e s s t r o n g e n o u g h to ind u c e v o c a l i z a t i o n as a s e c o n d a r y r e a c t i o n do h a v e positive o r n e g a t i v e r e i n f o r c ing qualities. M o r e specifically s t a t e d : A n i n c r e a s e in m o t i v a t i o n w i t h o u t t h e p o s s i b i l i t y o f p e r f o r m i n g t h e a d e q u a t e c o n s u m m a t o r y act (e. g., b e c a u s e o f a l a c k o f the g o a l o b j e c t ) is a s s u m e d to b e n e g a t i v e l y r e i n f o r c i n g ; a d e c r e a s e in m o t i v a t i o n (drive r e d u c t i o n ) is a s s u m e d to b e p o s i t i v e l y r e i n f o r c i n g 1. Conse1 The fact that there are hypothalamic electrodes yielding self-stimulation as well as increments in feeding motivation is not an argument against these assumptions as it was shown by Huston (1971, 1972) that the electrically evoked motivation to feed and to self-stimulate (in the absence of food) actually represent independent stimulus effects.
Reinforcing Concomitants of Vocalization
205
q u e n t l y , all v o c a l i z a t i o n - p r o d u c i n g b r a i n s t r u c t u r e s w h i c h d o n o t s h o w a n y connection with specific reinforcement effects would be candidates for the above-mentioned group of "specific"vocalization areas.
Methods Thirty-eight squirrel monkeys (Saimiri sciureus) were used as subjects. The animals were provided with platforms cemented onto the skull in a stereotaxic operation. The platforms contained up to 16 electrode guides through which the electrodes were implanted in the awake, chair-restrained animal. Electrodes consisted of teflon-insulated stainless steel wires (0.15 mm ~ ) protruding from uninsulated stainless steel tubes (0.4 mm ~ ) for 1 ram; at the tip the insulation was scraped off for 0.5 mm. The screws anchoring the platform served as indifferent electrodes. Stimulation current consisted of biphasic rectangular pulses of 10, 30 or 70 Hz, 1 or 3 msec pulse duration and an intensity up to 0.4 mA. Each electrode was lowered millimeter by millimeter until a position was found whose stimulation yielded vocalization. The electrode was then affixed to the platform, and tests for self-stimulation were begun. The self-stimulation situation consisted of a shuttle-box-like arrangement with a rear compartment and a front compartment which alternately received stimulation for 2-5 rain in a random but altogether balanced manner. As the animal was at all times free to move from one compartment to the other, it determined by its momentary place within the cage whether or not it received stimulation. The animal's presence in one or the other compartment was registered by infra-red light contacts. The stimulation was delivered via leads and a mercury swivel commutator (Anschel, 1968) which allowed free movement throughout the 22-rain session. Each electrode position was tested with three different types of stimulus presentations: a) continuous stimulation (stimulation lasts as long as the animal remains in the compartment under stimulation; b) interrupted stimulation in a 0.2-Hz rhythm (2.5 sec stimulation on - 2.5 sec stimulation off); c) interrupted stimulation in a ca. 0.7-Hz rhythm (0.7 sec stimulation on - 0.7 sec stimulation off). Furthermore, the majority of electrode positions was tested with three different intensities: sub-threshold, threshold and above threshold for vocalization. Each type of stimulus configuration was repeated three times, so that usually 27 sessions per electrode position were held. Evaluation of the data was carried out by calculating the percentage of time the animal received stimulation in relation to the total duration of the session. Five categories were formed: < 20% high negative reinforcement, 2 0 - 3 9 % low negative reinforcement, 50 _+ 10% neutral, 61-80% low positive reinforcement, > 80% high positive reinforcement. The category "neutral" means that either the stimulation has no reinforcing quality or the positive and negative effects are of about equal magnitude (Roberts, 1958). In order to distinguish the latter two subcategories, the number of changes from one compartment to the other was registered and, furthermore, the leverpressing procedure was introduced in addition to the shuttle-box-test in approximately one-third of the tested electrode positions (0.7-sec trains of stimulation per lever press). Sites yielding less than 50 lever presses per 10 rain and showing neutral shuttle-box behaviour (50 + 10%) with all types of stimulus presentations were considered as having no reinforcing qualities. The limits of the neutral category (40-60%; < 50 lever presses/10 rain) were settled according to the results of control sessions without stimulation. The experiments were completed by the histological verification of the stimulated brain loci (freeze-cutting, combined luxol fast blue - nuclei fast red staining). All elicited calls were recorded on tape and analysed spectrographically (Kay sonagraph). For a comprehensive description of the squirrel monkey's calls the reader is refered to Winter et al. (1966) and Schott (1975). A detailed analysis of the relationship between call type and reinforcement effect is under way (Jtirgens, in prep.).
Results Altogether, 251 electrode positions were tested. Their anatomical distribution a n d r e i n f o r c e m e n t e f f e c t s c a n b e s e e n i n F i g u r e s 1 - 4 . T h e s y m b o l s i n t h e s e fig-
206
U. Jiirgens AP 20
AP 21
AP18 AP19
API7
AP16
1 Figs. 1-4. Diagrams of the squirrel monkey's brain with vocalization-producingelectrode positions tested for reinforcement effects. 9 high negative reinforcement; ~ low negative reinforcement; neutral in shuttle-box test, lever pressing > 50/10 rain or not tested; ID neutral in shuttle-box test, lever pressing < 50/10 min; (~ low positive reinforcement; 9 high positive reinforcement; ~ positive and negative reinforcement, depending upon stimulus parameters
ures refer to the shuttle-box tests; the lever-pressing results will be dealt with in the text whenever they are of relevance. All symbols refer to threshold intensity or, if not tested, to above-threshold intensity. If different types of stimulus presentations (continuous versus interrupted, 0.7/0.7 sec versus 2.5/2.5 sec) yielded different results, those data were entered on the diagrams which showed the greatest deviation from "neutral" (50 + 10%). Each symbol represents the average of at least three sessions. The most rostral vocalization-eliciting area is the anterior cingulate gyrus ( A P 2 1 - 1 8 ) ; its typical call is a soft cackling. If one compares the reinforcing effects within this area, it is seen that the same call can be accompanied by highly negative reinforcement, or by highly positive reinforcement, or by intermediate reinforcing effects. Furthermore, there is no correlation between the relative place of the electrode tip within that general area and the reinforcement effect. True neutral loci were not found, as ,all the non-aversive electrode positions tested for lever-pressing yielded rates of above 120/10 rain.
ReinforcingConcomitantsof Vocalization
207
AP16
API5
cc
l
cl
c~ p~
p i
t
Fig. 2
Three sites in the ventral part of the anterior cingulate gyrus yielded chirping calls instead of cackling; all three sites were highly negatively reinforcing. From the ventral part of the cingulate cackling area there is a band of cackling loci running along the ventromedial part of the capsula interna down into the rostral diencephalon (AP18-9). Its reinforcement effects are comparable to those of the cingulate gyrus, except that there were no highly positive reinforcing effects. Just dorsal to the cingulate cackling sites, in the cortex around and above the sulcus cinguli, there is an area yielding purring calls (AP21-17). This area also shows very heterogeneous reinforcement effects accompanying the same
208
U. Jfirgens
)
Fig. 3
call. In contrast to the cingulate cackling area, one site was found whose stimulation yielded neutral results in the shuttle-box and no self-stimulation in the lever-pressing situation (rate: 2/10 min). At about AP16 there are another three vocalization areas: One in the gyrus rectus, the second in the medial caudate adjacent to the ventricle, and the third along the precommissural fornix in the lateral subcallosal gyrus and medial septum. The gyms-rectus loci again yielded a soft cackling; two of the three sites tested showed neutral self-stimulation effects in the shuttle-box test (lever pressing rate was 36/10 rain in the one ease, the other was not tested); the third position was slightly negatively reinforcing. In the caudate (apart
209
Reinforcing Concomitants of Vocalization
,, 0u 9~
~-2
Fig. 4
from the internal capsular region) only one site was tested which produced a chirping call similar to that of the ventral cingulate gyrus and which was also accompanied by negative reinforcing effects. The precommissural fornix sites produced trilling calls and were all accompanied by positive reinforcing effects. From about the level of the anterior Commissure two bands of vocalization sites could be followed into the amygdala: One leaving the capsula interna ( A P l l ) , entering the inferior thalamic peduncle ( A P l l - 1 0 ) and terminating within the central and basal amygdaioid nuclei (AP9); the other originating (or terminating?) in the nucleus of the stria terminalis and following the latter's course until it too reaches the amygdala. The first band predominantly yielded
Same vocalization different reinforcement 1. anteriQr cingulate gyrus 2. cortex above cingulate sulcus (supplementary motor area) 3. ventromedial edge of internal capsul 9 4. caudal periaqueductal gray 5. pontine parabrachial area 6. hypotl!alamic and tegmental "rebound system"
Vocalization loci without reinforcement effects
1. cortex above cingulate sulcus (supplementary motor area) 2. gyrus rectus 3. pontine parabrachial area
Vocalization threshold below reinforcement threshold
1. anterior cingulate gyrus 2. ventromedial edge of internal capsule
Table 1
septum subst, innominata inferior thalamic peduncle amygdala stria terminalis substantia nigra
caudatum (?) midline tbalamus ventral hypothalamus posterior periventricular hypothalamus 11. rostral periaqueductal gray 12. dorsolateral midbrah~ tegmentum 13. medulla
7. 8. 9. 10.
1. 2. 3. 4. 5. 6.
Vocalization and reinforcement correlated
H
t~
t'-0. C~
t,~
Reinforcing Concomitants of Vocalization
211
cackling calls, and the second purring calls, sometimes interspersed with short shrieks; both bands were exclusively positively reinforcing. In the thalamus, apart from the sites which are grouped around the medial edge of the capsula interna, the only vocalization loci lie within its midline nuclei, mainly in the nucl. centralis medialis (AP9 and 6). These electrode positions, which yielded high-pitched chirping calls, were all negatively reinforcing. Four vocalization areas can be distinguished in the hypothalamus. A soft cackling can be obtained from its dorsomedial part near the inferior thalamic peduncle (AP9); this area is slightly negatively or positively reinforcing. A harsh variant of the cackling call is produced in the posterior periventricular hypothalamus; this variant can be followed all along the periventricular system down into the caudal periaqueductal gray (AP8-1). All electrode positions within this system, except the most caudal ones, were highly negatively reinforcing. The third hypothalamic area yields shrieking calls; the responsive loci lie ventrally, near the optic tract (AP10-9). They, too, were all highly negatively reinforcing. The fourth area, finally, runs from the ventral part of the nucl. striae terminalis through the anteromedial and posterolateral hypothalamus into the ventral tegmental area (Tsai), from where it descends through the midbrain in a position ventrolateral to the periaqueductal gray (AP12-1). The call elicitable from this substrate is a "rebound" growling that only occurs at the end of stimulation and never during stimulation. The reinforcement effects accompanying this call are very heterogeneous, ranging from highly negative to highly positive reinforcement. Because of the complicated relationship between stimulation and vocalization, which makes an interpretation of the self-stimulation results very problematic, this rebound system will not be considered in the following discussion. The midbrain contains four vocalization-producing areas. Two have been mentioned already: The periaqueductal gray and ventrolateral tegmentum; the other two are the substantia nigra (AP7-5) and dorsolateral tegmentum (AP3-1). The latter yielded shrieking and cawing and the former cackling. Both were very uniform with regard to their reinforcing effects - the latter producing only highly negative reinforcement and the former exclusively highly positive reinforcement. In the midbrain-pons transitional zone the periaqueductal cackling loci spread laterally into the parabrachial area just ventrocaudal to the inferior colliculus (AP0-2). This general region is again heterogeneous in its reinforcement effects. It contains truly neutral sites (lever pressing < 10/10 rain). Further caudally there are 16 electrode positions in the lateral medulla (only three are shown in the diagrams; AP -1 and -2) which all produce more or less artificially sounding calls; they were all highly negatively reinforcing.
Discussion
The aim of this study was to obtain clues towards establishing a distinction between directly and indirectly elicited calls. The hypothesis underlying our approach has been mentioned in the Introduction. From this hypothesis it follows
212
U. Jfirgens
that vocalization areas which do not show a correlation between the elicited call and accompanying reinforcement have a high probability of being primary vocalization areas. Three types of such "non-correlation areas" can be found: a) Areas which have a lower threshold for vocalization than for reinforcement: b) areas which have no reinforcing qualities; c) areas which yield a constant call type but varying reinforcement effect. (It must be mentioned here that types a) and b) do not occur in a pure form, i.e., not all electrode positions within an area of type a) or b) show the respective characteristics.) In Table 1 is a survey of the diverse relationships observed. It can be seen that there are two groups of brain structures in which vocalization is clearly independent of any rewarding or punishing side effects. The first group includes the anterior cingulate gyrus with a dorsal extension into the supplementary motor area, a ventral extension into the gyrus rectus and its efferent output following the internal capsule. The second group consists of the caudal periaqueductal gray and the adjacent parabrachial region. As it cannot be totally excluded that vocalizations elicited from these structures are due to stimulus-induced motivational changes independent of reinforcing qualities, further corroboration of the primary nature of these areas is needed. One such corroboration comes from neuroanatomy. In a recent autoradiographic study, the projections of the cortical larynx representation were studied (Jiirgens, 1976). As the vocal cord movements elicitable from this area cannot be explained by motivational factors, overlap of its projections with vocalization-producing areas should be of interest. Despite the great number of projection fields on the one hand and vocalization areas on the other, the only areas of overlap were the cortex around the sulcus cinguli and the pontine parabrachial region. Further support is contained in several other studies. For instance, Sutton et al. (1974) trained rhesus monkeys to obtain food reward by vocalizing; after bilateral ablation of the anterior cingulate region the animals lost their ability to do so. It is known from clinical cases that infarcts within the anterior cingulate region and adjacent supplementary area often causes a pronounced inertia to speak, and in some cases even mutism (for reviews see Botez and Barbeau, 1971; Rubens, 1975). Concerning the caudal periaqueductal gray and adjacent parabrachial area, stimulation studies have shown that all ~animals tested (mammals, as well as birds, reptiles, frogs and fish) do yield vocalization from this region (Magoun et al., 1937; Hunsperger, 1956; Brown, 1965; Schmidt, 1966; Potash, 1970; Delius, 1971; Demski and Gerald, 1974; Kennedy, 1975). Furthermore, in the squirrel monkey the shortest latencies for vocalization are found here (50 msec), and the greatest number of different vocalization types are also obtained from this region. Finally, lesion studies in cats have shown that bilateral destruction of the periaqueductal gray and adjacent tegmentum may cause permanent mutism (Kelly et al., 1946; Adametz and O'Leary, 1959; Skultety, 1965). Therefore, there is ample evidence that the cortex around the anterior cingulate sulcus and the dorsal midbrain-pons transition are indeed crucial substrates for vocal behaviour. These two substrates do not seem to be functionally equivalent, however. Mutism has never been reported in animals after ablation of the anterior cingulate-supplementary area. The latencies are also
Reinforcing Concomitants of Vocalization
213
much longer in the latter (average 2.2 sec.) It may be assumed, therefore, that the integration of phonetic activity takes place in the caudal midbrain-rostral pons region, whereas the cortex around the cingulate sulcus seems to relate more to the initiation of vocalization, i.e., the preparedness to react vocally in situations which do not have a rigid stimulus-bound reaction characteristic. The fact that the gyrus rectus is also among the brain structures yielding vocalization independent of reinforcement effects is somewhat surprising. So far, no indications of this area having a specific phonetic function exist. We only know that the cingulate cackling area projects heavily into the gyrus rectus (Miiller-Preul3 and Jiirgens, in prep.) and that cackling calls can be evoked all along this connection. Further investigation of the role of this structure in phonation, therefore, is clearly needed. The majority of vocalization-producing brain areas, however, show a correlation between elicited call type and accompanying reinforcement effect. These cases can be interpreted in three different ways: a) The vocalization is a secondary reaction due to stimulus-induced motivational changes (e.g., flight motivation due to stimulus-induced pain); b) vocalization as well as reinforcement effect are triggered directly by the stimulus; a correlation between the two is merely a coincidence; c) vocalization as well as reinforcement effect are triggered directly; both form an integral reaction (e.g., the stimulus elicits an aggressive motivation together with its vocal expression). A fourth possible interpretation, namely, that the reinforcement effect is caused by the vocalization, can be excluded, as in all of the cases but one the threshold for reinforcement was clearly below that for vocalization (the only exception was found in the inferior thalamic peduncle). The latter fact is not an argument against interpretation b), however, as it cannot be excluded that both components of a compound response have different thresholds. A distinction between interpretation a), b) and c) on the basis of the selfstimulation data obviously cannot be made. Other criteria must be taken into consideration, such as the latency of vocalization, the length of the elicited call sequence, its reproducibility, and other characteristics. For instance, the fact that all medullary loci yield a more or less artificial call type suggests that in these cases the stimulus interferes directly with vocalization-specific substrates. On the other hand, the long latency, short duration and bad reproducibility of the calls evoked from the caudatum, septum, substantia innominata and substantia nigra can be taken as a clue that in these areas vocalization is a secondary response. The most problematical cases for interpretation are those which do not give a uniform picture in this respect. This is the case with the stria terminalis, for instance. Vocalization loci within this structure show a long latency and bad reproducibility, but if a call is initiated, it follows stimulation as long as stimulation goes on.
Statement. The study was carried out in accordance with the "Guiding Principles in the Care and Use of Primates" approved by the Council of the American Physiological Society. Acknowledgements. I wish to gratefully acknowledge the encouraging support of Professor D. Ploog and the excellent technical assistance of Miss G. Knott.
214
U. Jfirgens
References Anschel, S.: A commutator and cable for squirrel monkeys. Physiol. Behav. 3, 591-592 (1968) Adametz, J., O'Leary, J.L.: Experimental mutism resulting from periaqueductal lesions in cats. Neurology (Minneap.) 9, 636-642 (1959) Botez, M.J., Barbeau, A.: Role of subcortical structures and particularly of the thalamus in mechanisms of speech and language. Int. J. Neurol. (Montevideo) 8, 300-320 (1971) Brown, J.L.: Vocalization evoked from the optic lobe of a song bird. Science 149, 1002-1003 (1965) Delius, J.D.: Neural substrates of vocalizations in gulls and pigeons. Exp. Brain Res. 12, 64-80 (1971) Demski, L.S., Gerald, J.W.: Sound production and other behavioral effects of midbrain stimulation in flee-swimming toadfish, Opsanus beta. Brain Behav. Evol. 9, 41-59 (1974) Hunsperger, R.W.: Affektreaktionen auf elektrische Reizung im Hirnstamm der Katze. Helv. physiol, pharmacol. Acta 14, 70-92 (1956) Huston, J.P.: Relationship between motivating and rewarding stimulation of the lateral hypothalamus. Physiol. Behav. 6, 711-716 (1971) Huston, J.P.: Inhibition of hypothalamically motivated eating by rewarding stimulation through the same electrode. Physiol. Behav. 8, 1121-1125 (1972) Jiirgens, U.: Projections from the cortical larynx area in the squirrel monkey. Exp. Brain Res. 25, 401-411 (1976) Jiirgens, U., Ploog, D.: Cerebral representation of vocalization in the squirrel monkey. Exp. Brain Res. 10, 532-554 (1970) Kelly, A.H., Beaton, L.E., Magoun, H.W.: A midbrain mechanism for facio-vocal activity. J. Neurophysiol. 9, 181-189 (1946) Kennedy, M.C.: Vocalization elicited in a lizard by electrical stimulation of the midbrain. Brain Res. 91, 321-325 (1975) Magoun, H.W., Atlas, D., Ingersoll, E.H., Ranson, S.W.: Associated facial, vocal and respiratory components of emotional expression: an experimental study. J. Neurol. Psychopath. 17, 241-255 (1937) Miiller-Preuss, P., Jiirgens, U.: Projections from different limbic vocalization areas in the squirrel monkey. (in prep). Potash, L.M.: Vocalizations elicited by electrical brain stimulation in Coturnix coturnix japonica. Behaviour 36, 149-167 (1970) Roberts, W.W.: Both rewarding and punishing effects from stimulation of posterior hypothalamus of cat with same electrode at same intensity. J. comp. physiol. Psychol. 51, 400-407 (1958) Rubens, A.B.: Aphasia with infarction in the territory of the anterior cerebral artery. Cortex 11, 239-250 (19.75) Schmidt, R.S.: Central mechanisms of frog calling. Behaviour 26, 251-285 (1966) Schott, D.: Quantitative analysis of the vocal repertoire of squirrel monkeys (Saimiri sciureus). Z. Tierpsychol. 38, 225-250 (1975) Skultety, F.M.: Mutism in cats with rostral midbrain lesions. Arch. Neurol. (Chic.) 12, 211-225 (1965) Sutton, D., Larson, C., Lindeman, R.C.: Neocortical and limbic lesion effects on primate phonation. Brain Res. 71, 61-75 (1974) Winter, P., Ploog, D., Latta, J.: Vocal repertoire of the squirrel monkey, its analysis and significance. Exp. Brain Res. 1, 359-384 (1966) Received March 17, 1976
Experimental Brain Research 9 by Springer-Verlag1976
Reinforcing Concomitants of Electrically Elicited Vocalizations U. Jtirgens Max-Planck-Institute for Psychiatry, Kraepelinstr, 2, D - 8000 Miinchen 40, Federal Republic of Germany
Summary. In 38 squirrel monkeys 251 vocalization-producing electrode positions were tested for their positive and negative reinforcing properties. Two groups of vocalization-producing brain areas could be distinguished: One group in which the electrically elicited vocalization was independent of the accompanying reinforcement effect, and a second group in which vocalization and reinforcement effect were correlated. The first group included the anterior cingulate gyrus, the adjacent supplementary m o t o r area, gyrus rectus, ventromedial edge of the capsula interna, caudal periaqueductal gray and adjacent parabrachial region. The second group consisted of the caudatum, septum, substantia innominata, amygdala, inferior thalamic peduncle, stria terminalis, midline thalamus, ventral and periventricular hypothalamus, substantia nigra, rostral periaqueductal gray, dorsolateral midbrain t e g m e n t u m and lateral medulla. It is hypothesized that the first group contains predominantly or exclusively " p r i m a r y " Vocalization substrates; the second group is thought to be composed mainly of structures whose stimulation yields vocalization secondarily due to stimulus induced motivational changes.
Key words: Vocalization - Self-stimulation - Squirrel m o n k e y Abbreviations
a: nucl. accumbens aa: area anterior amygdalae ab: nucl. basalis amygdalae ac: nucl. centralis amygdalae al: nucl. lateralis amygdalae an: nucl. anterior thalami anl: ansa lenticularis aq: substantia grisea centralis bc: brachium conjunctivum ca: nucl. caudatus cc: corpus callosum cen: nucl. centralis superior tegmenti cent: centrum medianum
ci: capsula interna cin: cingulum ch claustrum coa: commissura anterior coli: colliculusinferior cols: colliculussuperior csp: tractus cortico-spinalis db: fasciculusdiagonalis Brocae dbc: decussatio brachii conjunctivii f: fornix gc: gyrus cinguli gh corpus geniculatum laterale gm: corpus geniculatum mediale
204 gp: globus pallidus gr: gyrus rectus gs: gyrus subcallosus h: campus Foreli ha: nucl. habenularis hi: tractus habenulo-interpeduncularis hip: hippocampus hya: area hypothalamica anterior hyl: area hypothalamica lateralis hyv: nucl, ventromedialis hypothalami in: nucl. interpeduncularis lap: nucl. lateralis posterior thalami lay: nucl. ventralis lateralis thalami le: lemniscus lateralis lem: lemniscus medialis lm: fasciculus longitudinalis medialis m: corpus mamillare md: nucl. medialis dorsalis thalami mt: tractus mamillo-thalamieus nst: nucl. striae terminalis oi: nucl. olivaris inferior o1: fasciculus olfactorius Zuckerkandl os: nucl. ofivaris superior p: pedunculus cerebri pmc: brachium pontis po: griseum pontis pro: area praeoptica
U. Jfirgens pu: nucl. pulvinaris thalami put: putamen re: formatio reticularis rep: nucl. reticularis tegmenti pontis rub: nucl. ruber s: septum sin: stria medullaris sn: substantia nigra st: stria terminalis sto: stria olfactoria lateralis subt: subthalamus tec: tractus tegmentalis centralis trz: corpus trapezoideum va: nucl. ventralis anterior thalami vpl: nucl. ventralis postero-lateralis vpm: nuel. ventralis postero-medialis zi: zona incerta II: tractus opticus IIch: chiasma nervorum opticorum III: n. oculomotorius and nucl. n. oculomotorii IV: n. and nucl. n. trochlearis VI: n. abducens and nucl. n. abducentis VII: nucl. n. facialis VIII: nucl. cochlearis IX: n. hypoglossus
Introduction V o c a l i z a t i o n can b e elicited b y e l e c t r i c a l s t i m u l a t i o n w i t h i n a r e l a t i v e l y large p a r t of t h e s q u i r r e l m o n k e y ' s b r a i n (Jiirgens a n d Ploog, 1970). T h e g r e a t n u m b e r o f r e s p o n s i v e a r e a s a n d t h e i r close r e l a t i o n to t h e l i m b i c s y s t e m suggest t h a t n o t all o f t h e m r e p r e s e n t " s p e c i f i c " v o c a l i z a t i o n areas. T h e o r e t i c a l l y , t h e r e a r e two possibilities as to h o w e l e c t r i c a l b r a i n s t i m u l a t i o n p r o v o k e s v o calization: O n e is t h a t t h e e l e c t r i c a l stimulus d i r e c t l y triggers t h e m o t o r - c o - o r d i n a t i n g m e c h a n i s m s for p h o n a t i o n ( p r i m a r y v o c a l r e s p o n s e ) ; t h e o t h e r is t h a t t h e electrical stimulus p r o d u c e s a m o r e o r less specific m o t i v a t i o n a l c h a n g e w h i c h l e a d s i n d i r e c t l y to a v o c a l u t t e r a n c e ( s e c o n d a r y v o c a l r e s p o n s e ) . T h e p r e s e n t s t u d y is an a t t e m p t to e s t a b l i s h such a d i s t i n c t i o n b y testing all vocaliz a t i o n - p r o d u c i n g b r a i n s t r u c t u r e s for t h e i r p o s i t i v e a n d n e g a t i v e r e i n f o r c i n g p r o p e r t i e s . T h e h y p o t h e s i s u n d e r l y i n g this s t u d y a s s u m e s t h a t t h e r e is a high p r o b a b i l i t y t h a t e l e c t r i c a l l y - e l i c i t e d m o t i v a t i o n a l c h a n g e s s t r o n g e n o u g h to ind u c e v o c a l i z a t i o n as a s e c o n d a r y r e a c t i o n do h a v e positive o r n e g a t i v e r e i n f o r c ing qualities. M o r e specifically s t a t e d : A n i n c r e a s e in m o t i v a t i o n w i t h o u t t h e p o s s i b i l i t y o f p e r f o r m i n g t h e a d e q u a t e c o n s u m m a t o r y act (e. g., b e c a u s e o f a l a c k o f the g o a l o b j e c t ) is a s s u m e d to b e n e g a t i v e l y r e i n f o r c i n g ; a d e c r e a s e in m o t i v a t i o n (drive r e d u c t i o n ) is a s s u m e d to b e p o s i t i v e l y r e i n f o r c i n g 1. Conse1 The fact that there are hypothalamic electrodes yielding self-stimulation as well as increments in feeding motivation is not an argument against these assumptions as it was shown by Huston (1971, 1972) that the electrically evoked motivation to feed and to self-stimulate (in the absence of food) actually represent independent stimulus effects.
Reinforcing Concomitants of Vocalization
205
q u e n t l y , all v o c a l i z a t i o n - p r o d u c i n g b r a i n s t r u c t u r e s w h i c h d o n o t s h o w a n y connection with specific reinforcement effects would be candidates for the above-mentioned group of "specific"vocalization areas.
Methods Thirty-eight squirrel monkeys (Saimiri sciureus) were used as subjects. The animals were provided with platforms cemented onto the skull in a stereotaxic operation. The platforms contained up to 16 electrode guides through which the electrodes were implanted in the awake, chair-restrained animal. Electrodes consisted of teflon-insulated stainless steel wires (0.15 mm ~ ) protruding from uninsulated stainless steel tubes (0.4 mm ~ ) for 1 ram; at the tip the insulation was scraped off for 0.5 mm. The screws anchoring the platform served as indifferent electrodes. Stimulation current consisted of biphasic rectangular pulses of 10, 30 or 70 Hz, 1 or 3 msec pulse duration and an intensity up to 0.4 mA. Each electrode was lowered millimeter by millimeter until a position was found whose stimulation yielded vocalization. The electrode was then affixed to the platform, and tests for self-stimulation were begun. The self-stimulation situation consisted of a shuttle-box-like arrangement with a rear compartment and a front compartment which alternately received stimulation for 2-5 rain in a random but altogether balanced manner. As the animal was at all times free to move from one compartment to the other, it determined by its momentary place within the cage whether or not it received stimulation. The animal's presence in one or the other compartment was registered by infra-red light contacts. The stimulation was delivered via leads and a mercury swivel commutator (Anschel, 1968) which allowed free movement throughout the 22-rain session. Each electrode position was tested with three different types of stimulus presentations: a) continuous stimulation (stimulation lasts as long as the animal remains in the compartment under stimulation; b) interrupted stimulation in a 0.2-Hz rhythm (2.5 sec stimulation on - 2.5 sec stimulation off); c) interrupted stimulation in a ca. 0.7-Hz rhythm (0.7 sec stimulation on - 0.7 sec stimulation off). Furthermore, the majority of electrode positions was tested with three different intensities: sub-threshold, threshold and above threshold for vocalization. Each type of stimulus configuration was repeated three times, so that usually 27 sessions per electrode position were held. Evaluation of the data was carried out by calculating the percentage of time the animal received stimulation in relation to the total duration of the session. Five categories were formed: < 20% high negative reinforcement, 2 0 - 3 9 % low negative reinforcement, 50 _+ 10% neutral, 61-80% low positive reinforcement, > 80% high positive reinforcement. The category "neutral" means that either the stimulation has no reinforcing quality or the positive and negative effects are of about equal magnitude (Roberts, 1958). In order to distinguish the latter two subcategories, the number of changes from one compartment to the other was registered and, furthermore, the leverpressing procedure was introduced in addition to the shuttle-box-test in approximately one-third of the tested electrode positions (0.7-sec trains of stimulation per lever press). Sites yielding less than 50 lever presses per 10 rain and showing neutral shuttle-box behaviour (50 + 10%) with all types of stimulus presentations were considered as having no reinforcing qualities. The limits of the neutral category (40-60%; < 50 lever presses/10 rain) were settled according to the results of control sessions without stimulation. The experiments were completed by the histological verification of the stimulated brain loci (freeze-cutting, combined luxol fast blue - nuclei fast red staining). All elicited calls were recorded on tape and analysed spectrographically (Kay sonagraph). For a comprehensive description of the squirrel monkey's calls the reader is refered to Winter et al. (1966) and Schott (1975). A detailed analysis of the relationship between call type and reinforcement effect is under way (Jtirgens, in prep.).
Results Altogether, 251 electrode positions were tested. Their anatomical distribution a n d r e i n f o r c e m e n t e f f e c t s c a n b e s e e n i n F i g u r e s 1 - 4 . T h e s y m b o l s i n t h e s e fig-
206
U. Jiirgens AP 20
AP 21
AP18 AP19
API7
AP16
1 Figs. 1-4. Diagrams of the squirrel monkey's brain with vocalization-producingelectrode positions tested for reinforcement effects. 9 high negative reinforcement; ~ low negative reinforcement; neutral in shuttle-box test, lever pressing > 50/10 rain or not tested; ID neutral in shuttle-box test, lever pressing < 50/10 min; (~ low positive reinforcement; 9 high positive reinforcement; ~ positive and negative reinforcement, depending upon stimulus parameters
ures refer to the shuttle-box tests; the lever-pressing results will be dealt with in the text whenever they are of relevance. All symbols refer to threshold intensity or, if not tested, to above-threshold intensity. If different types of stimulus presentations (continuous versus interrupted, 0.7/0.7 sec versus 2.5/2.5 sec) yielded different results, those data were entered on the diagrams which showed the greatest deviation from "neutral" (50 + 10%). Each symbol represents the average of at least three sessions. The most rostral vocalization-eliciting area is the anterior cingulate gyrus ( A P 2 1 - 1 8 ) ; its typical call is a soft cackling. If one compares the reinforcing effects within this area, it is seen that the same call can be accompanied by highly negative reinforcement, or by highly positive reinforcement, or by intermediate reinforcing effects. Furthermore, there is no correlation between the relative place of the electrode tip within that general area and the reinforcement effect. True neutral loci were not found, as ,all the non-aversive electrode positions tested for lever-pressing yielded rates of above 120/10 rain.
ReinforcingConcomitantsof Vocalization
207
AP16
API5
cc
l
cl
c~ p~
p i
t
Fig. 2
Three sites in the ventral part of the anterior cingulate gyrus yielded chirping calls instead of cackling; all three sites were highly negatively reinforcing. From the ventral part of the cingulate cackling area there is a band of cackling loci running along the ventromedial part of the capsula interna down into the rostral diencephalon (AP18-9). Its reinforcement effects are comparable to those of the cingulate gyrus, except that there were no highly positive reinforcing effects. Just dorsal to the cingulate cackling sites, in the cortex around and above the sulcus cinguli, there is an area yielding purring calls (AP21-17). This area also shows very heterogeneous reinforcement effects accompanying the same
208
U. Jfirgens
)
Fig. 3
call. In contrast to the cingulate cackling area, one site was found whose stimulation yielded neutral results in the shuttle-box and no self-stimulation in the lever-pressing situation (rate: 2/10 min). At about AP16 there are another three vocalization areas: One in the gyrus rectus, the second in the medial caudate adjacent to the ventricle, and the third along the precommissural fornix in the lateral subcallosal gyrus and medial septum. The gyms-rectus loci again yielded a soft cackling; two of the three sites tested showed neutral self-stimulation effects in the shuttle-box test (lever pressing rate was 36/10 rain in the one ease, the other was not tested); the third position was slightly negatively reinforcing. In the caudate (apart
209
Reinforcing Concomitants of Vocalization
,, 0u 9~
~-2
Fig. 4
from the internal capsular region) only one site was tested which produced a chirping call similar to that of the ventral cingulate gyrus and which was also accompanied by negative reinforcing effects. The precommissural fornix sites produced trilling calls and were all accompanied by positive reinforcing effects. From about the level of the anterior Commissure two bands of vocalization sites could be followed into the amygdala: One leaving the capsula interna ( A P l l ) , entering the inferior thalamic peduncle ( A P l l - 1 0 ) and terminating within the central and basal amygdaioid nuclei (AP9); the other originating (or terminating?) in the nucleus of the stria terminalis and following the latter's course until it too reaches the amygdala. The first band predominantly yielded
Same vocalization different reinforcement 1. anteriQr cingulate gyrus 2. cortex above cingulate sulcus (supplementary motor area) 3. ventromedial edge of internal capsul 9 4. caudal periaqueductal gray 5. pontine parabrachial area 6. hypotl!alamic and tegmental "rebound system"
Vocalization loci without reinforcement effects
1. cortex above cingulate sulcus (supplementary motor area) 2. gyrus rectus 3. pontine parabrachial area
Vocalization threshold below reinforcement threshold
1. anterior cingulate gyrus 2. ventromedial edge of internal capsule
Table 1
septum subst, innominata inferior thalamic peduncle amygdala stria terminalis substantia nigra
caudatum (?) midline tbalamus ventral hypothalamus posterior periventricular hypothalamus 11. rostral periaqueductal gray 12. dorsolateral midbrah~ tegmentum 13. medulla
7. 8. 9. 10.
1. 2. 3. 4. 5. 6.
Vocalization and reinforcement correlated
H
t~
t'-0. C~
t,~
Reinforcing Concomitants of Vocalization
211
cackling calls, and the second purring calls, sometimes interspersed with short shrieks; both bands were exclusively positively reinforcing. In the thalamus, apart from the sites which are grouped around the medial edge of the capsula interna, the only vocalization loci lie within its midline nuclei, mainly in the nucl. centralis medialis (AP9 and 6). These electrode positions, which yielded high-pitched chirping calls, were all negatively reinforcing. Four vocalization areas can be distinguished in the hypothalamus. A soft cackling can be obtained from its dorsomedial part near the inferior thalamic peduncle (AP9); this area is slightly negatively or positively reinforcing. A harsh variant of the cackling call is produced in the posterior periventricular hypothalamus; this variant can be followed all along the periventricular system down into the caudal periaqueductal gray (AP8-1). All electrode positions within this system, except the most caudal ones, were highly negatively reinforcing. The third hypothalamic area yields shrieking calls; the responsive loci lie ventrally, near the optic tract (AP10-9). They, too, were all highly negatively reinforcing. The fourth area, finally, runs from the ventral part of the nucl. striae terminalis through the anteromedial and posterolateral hypothalamus into the ventral tegmental area (Tsai), from where it descends through the midbrain in a position ventrolateral to the periaqueductal gray (AP12-1). The call elicitable from this substrate is a "rebound" growling that only occurs at the end of stimulation and never during stimulation. The reinforcement effects accompanying this call are very heterogeneous, ranging from highly negative to highly positive reinforcement. Because of the complicated relationship between stimulation and vocalization, which makes an interpretation of the self-stimulation results very problematic, this rebound system will not be considered in the following discussion. The midbrain contains four vocalization-producing areas. Two have been mentioned already: The periaqueductal gray and ventrolateral tegmentum; the other two are the substantia nigra (AP7-5) and dorsolateral tegmentum (AP3-1). The latter yielded shrieking and cawing and the former cackling. Both were very uniform with regard to their reinforcing effects - the latter producing only highly negative reinforcement and the former exclusively highly positive reinforcement. In the midbrain-pons transitional zone the periaqueductal cackling loci spread laterally into the parabrachial area just ventrocaudal to the inferior colliculus (AP0-2). This general region is again heterogeneous in its reinforcement effects. It contains truly neutral sites (lever pressing < 10/10 rain). Further caudally there are 16 electrode positions in the lateral medulla (only three are shown in the diagrams; AP -1 and -2) which all produce more or less artificially sounding calls; they were all highly negatively reinforcing.
Discussion
The aim of this study was to obtain clues towards establishing a distinction between directly and indirectly elicited calls. The hypothesis underlying our approach has been mentioned in the Introduction. From this hypothesis it follows
212
U. Jfirgens
that vocalization areas which do not show a correlation between the elicited call and accompanying reinforcement have a high probability of being primary vocalization areas. Three types of such "non-correlation areas" can be found: a) Areas which have a lower threshold for vocalization than for reinforcement: b) areas which have no reinforcing qualities; c) areas which yield a constant call type but varying reinforcement effect. (It must be mentioned here that types a) and b) do not occur in a pure form, i.e., not all electrode positions within an area of type a) or b) show the respective characteristics.) In Table 1 is a survey of the diverse relationships observed. It can be seen that there are two groups of brain structures in which vocalization is clearly independent of any rewarding or punishing side effects. The first group includes the anterior cingulate gyrus with a dorsal extension into the supplementary motor area, a ventral extension into the gyrus rectus and its efferent output following the internal capsule. The second group consists of the caudal periaqueductal gray and the adjacent parabrachial region. As it cannot be totally excluded that vocalizations elicited from these structures are due to stimulus-induced motivational changes independent of reinforcing qualities, further corroboration of the primary nature of these areas is needed. One such corroboration comes from neuroanatomy. In a recent autoradiographic study, the projections of the cortical larynx representation were studied (Jiirgens, 1976). As the vocal cord movements elicitable from this area cannot be explained by motivational factors, overlap of its projections with vocalization-producing areas should be of interest. Despite the great number of projection fields on the one hand and vocalization areas on the other, the only areas of overlap were the cortex around the sulcus cinguli and the pontine parabrachial region. Further support is contained in several other studies. For instance, Sutton et al. (1974) trained rhesus monkeys to obtain food reward by vocalizing; after bilateral ablation of the anterior cingulate region the animals lost their ability to do so. It is known from clinical cases that infarcts within the anterior cingulate region and adjacent supplementary area often causes a pronounced inertia to speak, and in some cases even mutism (for reviews see Botez and Barbeau, 1971; Rubens, 1975). Concerning the caudal periaqueductal gray and adjacent parabrachial area, stimulation studies have shown that all ~animals tested (mammals, as well as birds, reptiles, frogs and fish) do yield vocalization from this region (Magoun et al., 1937; Hunsperger, 1956; Brown, 1965; Schmidt, 1966; Potash, 1970; Delius, 1971; Demski and Gerald, 1974; Kennedy, 1975). Furthermore, in the squirrel monkey the shortest latencies for vocalization are found here (50 msec), and the greatest number of different vocalization types are also obtained from this region. Finally, lesion studies in cats have shown that bilateral destruction of the periaqueductal gray and adjacent tegmentum may cause permanent mutism (Kelly et al., 1946; Adametz and O'Leary, 1959; Skultety, 1965). Therefore, there is ample evidence that the cortex around the anterior cingulate sulcus and the dorsal midbrain-pons transition are indeed crucial substrates for vocal behaviour. These two substrates do not seem to be functionally equivalent, however. Mutism has never been reported in animals after ablation of the anterior cingulate-supplementary area. The latencies are also
Reinforcing Concomitants of Vocalization
213
much longer in the latter (average 2.2 sec.) It may be assumed, therefore, that the integration of phonetic activity takes place in the caudal midbrain-rostral pons region, whereas the cortex around the cingulate sulcus seems to relate more to the initiation of vocalization, i.e., the preparedness to react vocally in situations which do not have a rigid stimulus-bound reaction characteristic. The fact that the gyrus rectus is also among the brain structures yielding vocalization independent of reinforcement effects is somewhat surprising. So far, no indications of this area having a specific phonetic function exist. We only know that the cingulate cackling area projects heavily into the gyrus rectus (Miiller-Preul3 and Jiirgens, in prep.) and that cackling calls can be evoked all along this connection. Further investigation of the role of this structure in phonation, therefore, is clearly needed. The majority of vocalization-producing brain areas, however, show a correlation between elicited call type and accompanying reinforcement effect. These cases can be interpreted in three different ways: a) The vocalization is a secondary reaction due to stimulus-induced motivational changes (e.g., flight motivation due to stimulus-induced pain); b) vocalization as well as reinforcement effect are triggered directly by the stimulus; a correlation between the two is merely a coincidence; c) vocalization as well as reinforcement effect are triggered directly; both form an integral reaction (e.g., the stimulus elicits an aggressive motivation together with its vocal expression). A fourth possible interpretation, namely, that the reinforcement effect is caused by the vocalization, can be excluded, as in all of the cases but one the threshold for reinforcement was clearly below that for vocalization (the only exception was found in the inferior thalamic peduncle). The latter fact is not an argument against interpretation b), however, as it cannot be excluded that both components of a compound response have different thresholds. A distinction between interpretation a), b) and c) on the basis of the selfstimulation data obviously cannot be made. Other criteria must be taken into consideration, such as the latency of vocalization, the length of the elicited call sequence, its reproducibility, and other characteristics. For instance, the fact that all medullary loci yield a more or less artificial call type suggests that in these cases the stimulus interferes directly with vocalization-specific substrates. On the other hand, the long latency, short duration and bad reproducibility of the calls evoked from the caudatum, septum, substantia innominata and substantia nigra can be taken as a clue that in these areas vocalization is a secondary response. The most problematical cases for interpretation are those which do not give a uniform picture in this respect. This is the case with the stria terminalis, for instance. Vocalization loci within this structure show a long latency and bad reproducibility, but if a call is initiated, it follows stimulation as long as stimulation goes on.
Statement. The study was carried out in accordance with the "Guiding Principles in the Care and Use of Primates" approved by the Council of the American Physiological Society. Acknowledgements. I wish to gratefully acknowledge the encouraging support of Professor D. Ploog and the excellent technical assistance of Miss G. Knott.
214
U. Jfirgens
References Anschel, S.: A commutator and cable for squirrel monkeys. Physiol. Behav. 3, 591-592 (1968) Adametz, J., O'Leary, J.L.: Experimental mutism resulting from periaqueductal lesions in cats. Neurology (Minneap.) 9, 636-642 (1959) Botez, M.J., Barbeau, A.: Role of subcortical structures and particularly of the thalamus in mechanisms of speech and language. Int. J. Neurol. (Montevideo) 8, 300-320 (1971) Brown, J.L.: Vocalization evoked from the optic lobe of a song bird. Science 149, 1002-1003 (1965) Delius, J.D.: Neural substrates of vocalizations in gulls and pigeons. Exp. Brain Res. 12, 64-80 (1971) Demski, L.S., Gerald, J.W.: Sound production and other behavioral effects of midbrain stimulation in flee-swimming toadfish, Opsanus beta. Brain Behav. Evol. 9, 41-59 (1974) Hunsperger, R.W.: Affektreaktionen auf elektrische Reizung im Hirnstamm der Katze. Helv. physiol, pharmacol. Acta 14, 70-92 (1956) Huston, J.P.: Relationship between motivating and rewarding stimulation of the lateral hypothalamus. Physiol. Behav. 6, 711-716 (1971) Huston, J.P.: Inhibition of hypothalamically motivated eating by rewarding stimulation through the same electrode. Physiol. Behav. 8, 1121-1125 (1972) Jiirgens, U.: Projections from the cortical larynx area in the squirrel monkey. Exp. Brain Res. 25, 401-411 (1976) Jiirgens, U., Ploog, D.: Cerebral representation of vocalization in the squirrel monkey. Exp. Brain Res. 10, 532-554 (1970) Kelly, A.H., Beaton, L.E., Magoun, H.W.: A midbrain mechanism for facio-vocal activity. J. Neurophysiol. 9, 181-189 (1946) Kennedy, M.C.: Vocalization elicited in a lizard by electrical stimulation of the midbrain. Brain Res. 91, 321-325 (1975) Magoun, H.W., Atlas, D., Ingersoll, E.H., Ranson, S.W.: Associated facial, vocal and respiratory components of emotional expression: an experimental study. J. Neurol. Psychopath. 17, 241-255 (1937) Miiller-Preuss, P., Jiirgens, U.: Projections from different limbic vocalization areas in the squirrel monkey. (in prep). Potash, L.M.: Vocalizations elicited by electrical brain stimulation in Coturnix coturnix japonica. Behaviour 36, 149-167 (1970) Roberts, W.W.: Both rewarding and punishing effects from stimulation of posterior hypothalamus of cat with same electrode at same intensity. J. comp. physiol. Psychol. 51, 400-407 (1958) Rubens, A.B.: Aphasia with infarction in the territory of the anterior cerebral artery. Cortex 11, 239-250 (19.75) Schmidt, R.S.: Central mechanisms of frog calling. Behaviour 26, 251-285 (1966) Schott, D.: Quantitative analysis of the vocal repertoire of squirrel monkeys (Saimiri sciureus). Z. Tierpsychol. 38, 225-250 (1975) Skultety, F.M.: Mutism in cats with rostral midbrain lesions. Arch. Neurol. (Chic.) 12, 211-225 (1965) Sutton, D., Larson, C., Lindeman, R.C.: Neocortical and limbic lesion effects on primate phonation. Brain Res. 71, 61-75 (1974) Winter, P., Ploog, D., Latta, J.: Vocal repertoire of the squirrel monkey, its analysis and significance. Exp. Brain Res. 1, 359-384 (1966) Received March 17, 1976
