The cingular vocalization pathway in the squirrel monkey

Summary In 39 squirrel monkeys (Saimiri sciureus), the effects of various brain lesions on vocalizations elicited from the precallosal cingulate gyrus were tested. It was found that lesions abolishing the cingular vocalization completely can be traced from the stimulation site continuously down to the laryngeal motoneurons in the nucleus ambiguus. The pathway thus determined (Fig. 4) travels from the precallosal cingulate gyrus through the frontal white matter and enters the internal capsule from a dorsolateral position. The pathway then follows this structure in a medio-caudal direction down to the caudal diencephalon. Here, the effective lesions leave the corticospinal tract and ascend dorsally into the periaqueductal grey. The pathway follows this structure to its end where it sweeps lateral through the parabrachial area and then descends through the lateral pons and ventrolateral medulla to the nucleus ambiguus.In nine of the animals, in addition, the effects of bilateral anterior cingular lesions on vocalizations elicited in other brain areas were tested. It was found that the only vocalization-eliciting area which becomes ineffective after destruction of the anterior cingulate gyrus is the postero-medial orbital cortex.Abbreviations a nucl. accumbens - aa area anterior amygdalae - ab nucl. basalis amygdalae - ac nucl. centralis amygdalae - al nucl. lateralis amygdalae - am nucl. medialis amygdalae - an nucl. anterior thalami - aq griseum centralis - bc brachium conjunctivum - ca caudatum - cb cerebellum - cc corpus callosum - cen nucl. centralis superior Bechterew - ci capsula interna - cin cingulum - cl claustrum - coa commissura anterior - coli colliculus inferior - cols colliculus superior - cop commissura posterior - cr corpus restiforme - csp tractus corticospinalis - db fasciculus diagonalis Brocae - dbc decussatio brachii conjunctivi - f fornix - gc gyrus cinguli - gl geniculatum laterale - gm geniculatum mediale - gp globus pallidus - gr gyrus rectus - gs gyrus subcallosus - h area tegmentalis (Forel) - ha habenula - hi tractus habenulo-interpeduncularis - hip hippocampus - hya hypothalamus anterior - hyv hypothalamus ventromedialis - in nucl. interpeduncularis - lap nucl. lateralis posterior thalami - lem lemniscus medialis - lm fasciculus longitudinalis medialis - m nucl. mammillaris - md nucl. medialis dorsalis thalami - mt tractus mammillothalamicus - nst nucl. striae terminalis - nts nucl. solitarius - oi oliva inferior - ol fasciculus olfactorius (Zuckerkandl) - os oliva superior - p pedunculus cerebri - pmc brachium pontis - po griseum pontis - pro area praeoptica - pu nucl. pulvinaris - put putamen - re formatio reticularis mesencephali - rep nucl. reticularis tegmenti pontis - rl nucl. reticularis lateralis - rub nucl. ruber - s septum - sm stria medullaris - sn substantia nigra - st stria terminalis - sto stria olfactoria lateralis - tec tractus tegmentalis centralis - trz corpus trapezoideum - va nucl. ventralis anterior thalami - ves nucl. vestibularis - vpl nucl. ventralis posterior lateralis th. - vpm nucl. ventralis posterior medialis th. - zi zona incerta - II tractus opticus - IIchde chiasma n. opticorum - III nucl. n. oculomotorii and n. oculomotorius - IV nucl. n. trochlearis - VI n. abducens - VII nucl. n. facialis and n. facialis - VIII n. acusticus - XII nucl. n. hypoglossi     

Projections of the ventrolateral pontine vocalization area in the squirrel monkey

In four squirrel monkeys (Saimiri sciureus), the tracer biotin dextranamine (BDA) was injected into the ventrolateral pons at a site at which injection of the glutamate antagonist kynurenic acid blocked vocalization electrically elicited from the periaqueductal gray (PAG). Anterograde projections could be traced into all cranial motor and sensory nuclei involved in phonation, that is, the nucleus ambiguus, facial, hypoglossal and trigeminal motor nuclei, the motorneuron column in the ventral gray substance innervating the extrinsic laryngeal muscles, the nucleus retroambiguus, solitary tract and spinal trigeminal nuclei. Projections were also found into a number of auditory nuclei, namely the nucleus cochlearis-complex, superior olive, ventral and dorsal nuclei of the lateral lemniscus and inferior colliculus. Furthermore, there were projections into the reticular formation of the lateral and dorsocaudal medulla and lateral pons, into nucleus gracilis, inferior and medial vestibular nuclei, lateral reticular nucleus, ventral raphe, pontine gray, superior colliculus, PAG and mediodorsal thalamic nucleus. Injection of the tracer wheat germ agglutinin-conjugated horseradish peroxidase into the ventrolateral pontine vocalization-blocking area in one animal yielded retrograde labeling throughout the PAG. Injection of BDA into a vocalization-eliciting site of the PAG in another animal yielded projections into the ventrolateral pontine vocalization-blocking area. It is concluded that the ventral paralemniscal area in the ventrolateral pons represents a relay station of the descending periaqueductal vocalization-controlling pathway.     

Projections from the cortical larynx area in the squirrel monkey

Summary The projections from the cortical vocal fold area were studied in five squirrel monkeys (Saimiri sciureus) with the aid of the autoradiographie tracing technique. The location of the cortical vocal fold area was determined by exploring the exposed frontal cortex with roving electrodes while examining the larynx for vocal fold adduction. The following projections were found: To the orbital cortex (area 11), dorsomedial frontal cortex (areas 6 and 8), Broca's area (area 44), lower fronto-parietal cortex (areas 6, 4, 3 and 1), fronto-parietal operculum (area 50), insula (areas 14 and 13), caudatum, putamen, claustrum nucl. reticularis th., nucl. ventralis anterior, nucl. ventralis lateralis, nucl. ventralis posteromedialis, nucl. centralis inferior, nucl. centralis lateralis, nucl. medialis dorsalis, nucl. pulvinaris medialis, griseum pontis, nucl. parabrachialis medialis and lateralis, nucl. tr. spinalis n. trigemini and nucl. tr. solitarii.A comparison of this projection system with a previous mapping study for vocalization (Jürgens and Ploog, 1970) revealed that there are two areas yielding vocalization when electrically stimulated which receive direct projections from the cortical larynx area, namely, the cortex around the anterior sulcus cinguli and the parabrachial nuclei at the pons-midbrain transition. The possible relevance of these structures for vocalization is discussed.     

The effect of species-specific vocalization on the discharge of auditory cortical cells in the awake squirrel monkey (Saimiri sciureus)

Summary Action potentials of single auditory cortical neurons of the squirrel monkey were recorded in a chronic, unanesthetized preparation. The responsiveness of units was tested with various types of simple and complex acoustic stimuli in a free field situation. As simple auditory stimuli, bursts of pure tones, clicks, and white noise were utilized. Species-specific vocalizations served as complex, biologically significant stimuli.The data are based on 48 neurons which showed a discrete response to speciesspecific vocalizations. In 63% the response to calls could be predicted from the units' responses to simple stimuli. Thirty-seven percent of the neurons were classified as unpredictable with respect to their responsiveness to vocalizations. The response of most units was restricted to call stimuli which showed similarities in their frequency-time characteristics. About 7% of the 116 units responding to calls were classified as selective responders because they were not excited by any other stimulus tested. It was not possible to single out the acoustic features to which these units responded.Peter Winter died in an skiing accident in March, 1972.     

Vocalization-correlated single-unit activity in the brain stem of the squirrel monkey

Summary The brain stems of 17 squirrel monkeys (Saimiri sciureus) were systematically explored for vocalization-related single-unit activity during calls electrically elicited from the periaqueductal grey. Of 12,280 cells tested, 1151 fired in relation to vocalization. Of these, 587 reacted to external acoustic stimuli and started firing after vocalization onset. As most of these cells were located in classical auditory relay structures, they probably represent auditory neurones reacting indirectly to self-produced vocalization due to auditory feedback. Seven cells reacted to acoustic stimuli but fired in advance of self-produced vocalization. These cells were locoated in the pericentral inferior colliculus, dorsal nucleus of the lateral lemniscus, dorsomedial to the ventral nucleus of the lateral lemniscus and immediately lateral to the central grey. They are probably engaged in tuning the auditory system to process self-generated sounds differently from external sounds. 261 neurones reacted to nonphonatory oral movements (chewing, swallowing) and started firing after vocalization onset. These neurones were widely distributed within the brain stem, with the highest density in the spinal trigeminal nucleus and medially adjacent reticular formation. The majority of these cells seem to react to proprioceptive and tactile stimuli generated by phonatory and nonphonatory oral activities. Some of them may exert motor control on muscles that come into play at later stages of phonation. 57 neurones reacted to nonphonatory oral movements but fired in advance of vocalization onset. These neurones were located mainly in the trigeminal motor nucleus, nucl. ambiguus, reticular formation around these nuclei, parabrachial region and lateral vestibular nucleus. Their role in motor control seems to be related to specific muscles rather than specific functions. 100 of the vocalization-related cells showed a correlation with respiration. Expiration-related cells were found in and around the rostral nucl. ambiguus and in the reticular formation dorsal to the facial nucleus. Inspiration-related cells were located in the rostral and caudal nucl. ambiguus regions, ventrolateral solitary tract nucleus and the lateral reticular formation below the trigeminal motor nucleus. Most of these cells probably represent premotor neurones of respiratory muscles and laryngeal motoneurones of the cricothyroid and posterior cricoarytenoid muscles. Finally, a last group of cells was found that was unresponsive to chewing and swallowing movements, quiet breathing and acoustic stimuli, but changed activity during vocalization. 38 of them became active before vocalization and cricothyroid activity, and 101 afterward. Both types were completely intermingled and scattered widely in the brain stem, including the nucl. ambiguus region, solitary tract nucleus, nucl. reticularis parvocellularis and gigantocellularis, parabrachial region, pericentral colliculus inferior, vestibular complex, periventricular grey and laterally adjacent tegmentum. Some of these cells may be related to vocalization in a more specific way.Abbreviations A nucl. annularis - Ab nucl. ambiguus - Apt area praetectalis - BC brachium conjunctivum - BP brachium pontis - Cb cerebellum - CC corpus callosum - Cd nucl. caudatus - Col colliculus inferior - CoS colliculus superior - CRf corpus restiforme - DBC decussatio brachii conjunctivi - DG nucl. dorsalis tegmenti (Gudden) - DR nucl. dorsalis raphae - DV nucl. ventralis n. vagi - FRM formatio reticularis myelencephali - FRP formatio reticularis pontis - FRTM formatio reticularis mesencephali - GC substantia grisea centralis - GL corpus geniculatum laterale - GM corpus geniculatum mediale - GPM griseum periventriculare mesencephali - GPo griseum pontis - H habenula - Hip hippocampus - IP nucl. interpeduncularis - LC locus coeruleus - LL lemniscus lateralis - LLd nucl. dorsalis lemnisci lateralis - LLv nucl. ventralis lemnisci lateralis - LM lemniscus medialis - LP nucl. lateralis posterior thalami - MD nucl. medialis dorsalis thalami - MV nucl. motorius n. trigemini - NC nucl. cochlearis - NCb nucl. cerebelli - NCS nucl. centralis superior - NCT nucl. trapezoidalis - NR nucl. ruber - NST nucl. supratrochlearis - NSV nucl. spinalis n. trigemini - NTS nucl. tractus solitarii - NIII nucl. oculomotorius - NIV nucl. trochlearis - nV nervus trigeminus - NVI nucl. abducens - NVII nucl. facialis - NXII nucl. hypoglossus - OI oliva inferior - PbL nucl. parabrachialis lateralis - PbM nucl. parabrachialis medialis - Pp nucl. praepositus - Pu nucl. pulvinaris oralis - PuL nucl. pulvinaris lateralis - PuM nucl. pulvinaris medialis - Py tractus pyramidalis - PV nucl. principalis n. trigemini - RL nucl. reticularis lateralis - RTP nucl. reticularis tegmenti pontis - SN substantia nigra - ST stria terminalis - Ves nucl. vestibulares - VR nucl. ventralis raphae - IV decussatio n. trochlearis Supported by Deutsche Forschungsgemeinchaft grant Ju 181/1     

Tuning properties of auditory cortex cells in the awake squirrel monkey

Summary Pure tone bursts elicited in primary auditory cortex (AI) cells of the awake squirrel monkey a wide range of response patterns which consisted of one or more excitatory or inhibitory temporal response components. In almost 60% of these cells, response patterns were frequency and/or intensity dependent. Response components such as early and late onset excitation, offset excitation and on-off excitation; as well as tonic excitation or inhibition often varied independently with changes in these stimulus parameters. Individual cells were therefore considered as multiple bandpass filters, and each discrete response component was analyzed separately for its tuning properties. A correlation between best frequencies of the various excitatory components (BEF), and between BEFs and best frequencies of inhibitory components (BIF), in cells which responded with more than one discrete response component, disclosed a significantly higher correlation between BEF/BIF pairs compared with BEF/BEF pairs, presumably reflecting certain lateral inhibition like processes. Applying Q_10dB factor, and Hf-Lf bandwidth at 10 dB above threshold, as measures of the sharpness of response areas, revealed that approximately 65% of all response areas could be defined as narrow by either one of these 2 measures, with no distinction, in that regard, between excitatory and inhibitory components. The average response bandwidths of the narrowly and the broadly tuned components, at 10 dB above threshold, were 0.4±0.18 and 1.42±0.68 octaves respectively. A comparison with the medial geniculate body (MGB) of the squirrel monkey, applying the Hf-Lf measure of sharpness of tuning, showed a significantly higher proportion of narrow response areas in the AI. Narrow response areas in both these regions were equally narrow, whereas the broad response areas of MGB cells were significantly broader. These results suggest a sharpening of response areas throughout the geniculo-cortical transformation.     

On the criteria for automatic recognition of squirrel monkey vocalizations

The problem of classifying squirrel monkey vocalizations has not yet been solved satisfactorily. To this end a system has been designed in which telemetrically-transmitted vocalization signals are automatically recognized by computer. The hardware and software basis for an on-line recognition using zero-crossing analysis has now been developed. Thus, it is now possible to begin computer-controlled experiments with the aim of classifying squirrel monkey vocalizations according to their communicative meaning.     

The laryngeal sensory pathway and its role in phonation. A brain lesioning study in the squirrel monkey

Summary In 10 squirrel monkeys (Saimiri sciureus) uni- or bilateral lesions were placed in the nucl. solitarius, parabrachial nuclei, nucl. ventralis posterior medialis thalami or face area of primary sensory cortex. The effects of these lesions on vocalization were compared with those after transection of the internal branch of the superior laryngeal nerve. It was found that neither the cortical nor thalamic or parabrachial lesions changed the acoustic structure of vocalization. In contrast, destruction of the nucl. solitarius, like transection of the internal branch of the superior laryngeal nerve, affected vocalization severely. It is concluded that the production of species-specific vocalization depends upon a di- or, possibly, tri-synaptic laryngeal reflex control from tactile and proprioceptive laryngeal mechanoreceptors via nucl. solitarius and, possibly, lateral medullary reticular formation to nucl. ambiguus.Abbreviations a amygdala - aq griseum periaquaeductale - bc brachium conjunctivum - ca nucl. caudatus - cb cerebellum - cent centrum medianum - ci capsula interna - cl claustrum - coa commissura anterior - coli colliculus inferior - cols colliculus superior - cr corpus restiforme - csp tractas corticospinalis - f fornix - gp globus pallidus - h campus Foreli - hip hippocampus - hy hypothalamus - lap nucl. lateralis posterior th - lem lemniscus medialis - lm fasciculus longitudinalis medialis - md nucl. medialis dorsalis th - nts nucl. tr. solitarius - oi oliva inferior - os oliva superior - p pedunculus cerebri - pmc brachium pontis - put putamen - rl nucl. reticularis lateralis - rub nucl. ruber - sm stria medullaris - sn substantia nigra - st stria terminalis - va nucl. ventralis anterior th - ves nucl. vestibularis - vpm nucl. ventralis posterior medialis th - II tractas opticus - IIch chiasma opticum - III n. oculomotorius - IV n. trochlearis - VI n. abducens - VII n. facialis - VIII nucl. cochlearis - XII nucl. n. hypoglossi     

Responses to acoustic stimuli of units in the auditory cortex of awake squirrel monkeys

Summary The responses of single units in the superior temporal gyrus of awake squirrel monkeys to tone pips, noise, clicks, and frequency-modulated sounds were recorded with extracellular microelectrodes. A majority of the units responded to acoustic stimulation, pure tone pips being the most effective in terms of the percentage of units responding (71%). No simple catalogue of response types could be elicited. Units varied in terms of the combinations of stimuli to which they were responsive, the frequency range over which pure tones were effective, and the temporal pattern of discharge to different frequencies and different types of stimuli. A substantial majority of units gave precise timed responses to the onset or offset of the stimuli, while a few introduced long delays between the stimulus and the response. With regard to the area studied, acoustic units could be found between stereotaxic coordinates A3 and A10, both on the lateral surface of the hemisphere and in the superior temporal plane, as well as in the caudal insular region. No precise tonotopic organization could be discerned.Peter Winter died in a skiing accident in March, 1972.     

Auditory responsive cortex in the squirrel monkey: neural responses to amplitude-modulated sounds

The neural response to amplitude-modulated sinus sounds (AM sound) was investigated in the auditory cortex and insula of the awake squirrel monkey. It was found that 78.1% of all acoustically driven neurons encoded the envelope of the AM sound; the remaining 21.9% displayed simple On, On/Off or Off responses at the beginning or the end of the stimulus sound. Those neurons with AM coding were able to encode the AM sound frequency in two different ways: (1) the spikes followed the amplitude modulation envelopes in a phaselocked manner; (2) the spike rate changed significantly with changing modulation frequencies. As reported in other species, the modulation transfer functions for rate showed higher modulation frequencies than the phaselocked response. Both AM codings exhibited a filter characteristic for AM sound. Whereas 46.6% of all neurons had the same filter characteristic for both the spike discharge and the phase-locked response, the remaining neurons displayed combinations of different filter types. The discharge pattern of a neuron to simple tone or noise bursts suggests the behaviour of this neuron when AM sound is used as the stimulus. Neurons with strong onset responses to tone/noise bursts tended to have higher phase-locked AM responses than neurons with weak onset responses. The spike rate maxima for AM sound showed no relation to the tone/noise burst discharge patterns. Varying modulation depth was encoded by the neuron's ability to follow the envelope cycles and not by the non-phase-locked spike rate frequency. The organization of the squirrel monkey's auditory cortex has previously been established by an anatomical study. We have added two new fields using physiological parameters. All fields investigated showed a clear functional separation for time-critical information processing. The best temporal resolution was shown by the primary auditory field (AI), the first-temporal field (T1) and the parainsular au ditory field (Pi). The neural data in these fields and the amplitude modulation frequency range of squirrel monkey calls suggest a similar correlation between vocalization and perception as in human psychophysical data for speech and hearing sensation. The anterior fields in particular failed to follow the AM envelopes. For the first time in a primate, the insula was tested with different sound parameters ranging from simple tone bursts to AM sound. It is suggested that this cortical region plays a role in time-critical aspects of acoustic information processing. The observed best frequencies covered the same spectrum as AI. As in the auditory fields, most neurons in the insula encoded AM sound with different filter types. The high proportion of neurons unable to encode AM sound (40.6%) and the low mean best modulation frequency (9.9 Hz) do not support a prominent role of the insula in temporal information processing.     

Brain stimulation-induced changes of phonation in the squirrel monkey

Summary In 11 squirrel monkeys (Saimiri sciureus), the brain stem was systematically explored with electrical brain stimulation for sites affecting the acoustic structure of ongoing vocalization. Vocalization was elicited by electrical stimulation of different brain structures. A severe deterioration of the acoustical structure of vocalization was obtained during stimulation of the caudoventral part of the periaqueductal grey, lateral parabrachial area, corticobulbar tract, nucl. ambiguus and surrounding reticular formation, facial nucleus, hypoglossal nucleus, solitary tract nucleus and along the fibres crossing the midline at the level of the hypoglossal nucleus. It is suggested that these structures are part of, or at least have direct access to, the motor coordination mechanism of phonation. Complete inhibition of phonation was obtained from the raphe and raphe-near reticular formation.Abbreviations Ab nucl ambiguus - APt area praetectalis - BC brachium conjunctivum - BP brachium pontis - Cb cerebellum - CC corpus callosum - Cd nucl. caudatus - Cf nucl. cuneiformis - Cel nucl. centralis lateralis - Cl claustrum - CM centrum medianum - Cn nucl. cuneatus - Co nucl. cochlearis - CoI colliculus inferior - CoS colliculus superior - CP commissura posterior - CPf cortex piriformis - CRf corpus restiforme - CSL nucl. centralis superior lateralis thalami - CT corpus trapezoideum - DBC decussatio brachii conjunctivi - DG nucl. dorsalis tegmenti (Gudden) - DLM decussatio lemnisci medialis - DPy decussatio pyramidum - DR nucl. dorsalis raphae - DV nucl. dorsalis n. vagi - DIV decussatio n. trochlearis - EP epiphysis - FC funiculus cuneatus - FL funiculus lateralis - FLM fasciculus longitudinalis medialis - FRM formatio reticularis myelencephali - FRP formatio reticularis pontis - FRPc formatio reticularis pontis caudalis - FRPo formatio reticularis pontis oralis - FRTM formatio reticularis mesencephali - FV funiculus ventralis - G nucl. gracilis - GC substantia grisea centralis (periaqueductal grey) - GL nucl. geniculatus lateralis - GM nucl. geniculatus medialis - GP globus pallidus - GPM griseum periventriculare mesencephali - GPo griseum pontis - Hip hippocampus - HL nucl. habenularis lateralis - H habenula - IP nucl. interpeduncularis - LC locus coeruleus - LD nucl. lateralis dorsalis thalami - Lim nucl. limitans - LLd nucl. lemnisci lateralis, pars dorsalis - LLv nucl. lemnisci lateralis, pars ventrali - LM lemniscus medialis - LP nucl. lateralis posterior thalami - MD nucl. medialis dorsalis thalami - MV nucl. motorius n. trigemini - NCS nucl. centralis superior - NCT nucl. trapezoidalis - NMV nucl. mesencephalicus n. trigemini - NR nucl. ruber - NSV nucl. spinalisn. trigemini - NTS nucl. tractus solitarii - NIII nucl. oculomotorius - NIV nucl. trochlearis - NVI nucl. abducens - NVII nucl. facialis - NXII nucl. hypoglossus - OI oliva inferior - OS oliva superior - P nucl. posterior thalami - PbL nucl. parabrachialis lateralis - PbM nucl. parabrachialis medialis - PC depedunculus cerebri - Pd nucl. peripeduncularis - Pg nucl. parabigeminalis - Pp nucl. praepositus - PuI nucl. pulvinaris inferior - PuL nucl. pulvinaris lateralis - PuM nucl. pulvinaris medialis - PuO nucl. pulvinaris oralis - Py tractus pyramidalis - Pv nucl. principalis n. trigemini - R Ab nucl. retroambiguus - RL nucl. reticularis lateralis - RTP nucl. reticularis tegmenti pontis - Sf nucl. subfascicularis - SGD substantia grisea dorsalis - SGV substantia grisea ventralis - SN substantia nigra - ST stria terminalis - St subthalamus - TRM tractus retroflexus (Meynert) - TSc tractus spinocerebellaris - Ves nucl. vestibularis - VL nucl. ventralis lateralis - VPI nucl. ventralis posterior inferior - VPL nucl. ventralis posterior lateralis - VPM nucl. ventralis posterior medialis - VR nucl. ventralis raphae - Zi zona incerta - II tractus opticus - VII n. facialis     

Neurophysiological correlates of brightness discrimination in the lateral geniculate nucleus of the squirrel monkey

Summary Incremental brightness thresholds (DI) were psychophysically determined at several background illumination intensities for three squirrel monkeys. Gross asymmetrical electrodes were then chronically implanted in the lateral geniculate nucleus of the same animals, and activity was recorded in stimulus conditions identical to behavioral testing. Overall activity, recorded through an integrating voltmeter, showed 1. a tendency to decrease as steady background illumination increased, and 2. an abrupt transient increase at both onset and offset to DI test flashes, directly proportional to test flash intensity. Background illumination, in proportion to its intensity, depressed response to a superimposed test flash. Test flashes below intensity DI at the various levels of background illumination produced no measurable response. The quantity DI was shown to be a function of the depressive or inhibitory effect of background illumination on the capacity of the system to respond to transient stimulation. A secondary determinant of DI appeared to be the amount of variability in ongoing neural activity upon which the DI flash is imposed.The author is indebted to the supervisor of her dissertation, Dr. L. R. Pinneo, for introducing her to the recording technique and for his help towards the completion of this work.Now Yerkes Regional Primate Research Center of Emory University, Atlanta, Georgia 30322.This research constitutes the author's Doctoral Dissertation at Florida State University. It was supported by USPHS Grants H=5691, FR=00165 and FR=05235 to Yerkes Laboratories, USPHS Grant FR-00164 and NB 04951-01.     

The effect of superior temporal lesions on the recognition of species-specific calls in the squirrel monkey

Summary Eleven squirrel monkeys (Saimiri sciureus) were trained to discriminate species-specific calls from non-species-specific complex sounds in a go, no-go procedure with social contact as positive reinforcement. The task required that the animals not only responded to a particular call but that this response should be generalized to any squirrel monkey call, whether or not it had been presented previously in training.After having reached a performance level of 75% correct responses in three consecutive sessions, seven animals received bilateral lesions of the auditory cortex; the other four animals served as controls. It was found that small lesions within the superior temporal gyrus did not interfere with the discrimination task. Lesions destroying about three quarters of the auditory cortex led to loss of retention; during retraining the animals did not reach criterion, but performed significantly above chance. These animals were able, however, to master a simplified version of the task where one species-specific call had to be discriminated from one non-species-specific sound. Animals with almost total ablation of the auditory cortex were capable of mastering neither the generalized task nor the simplified version.From these results, together with those of the literature, it is concluded 1) that recognition of complex sounds is not possible after complete auditory cortex ablation, probably because of interference with gestalt-formation processing, and 2) that species-specific calls are processed in the auditory system in the same way as other complex sounds.     

The three-dimensional vestibulo-ocular reflex evoked by high-acceleration rotations in the squirrel monkey

The aim of this study was to determine if the angular vestibulo-ocular reflex (VOR) in response to pitch, roll, left anterior–right posterior (LARP), and right anterior–left posterior (RALP) head rotations exhibited the same linear and nonlinear characteristics as those found in the horizontal VOR. Three-dimensional eye movements were recorded with the scleral search coil technique. The VOR in response to rotations in five planes (horizontal, vertical, torsional, LARP, and RALP) was studied in three squirrel monkeys. The latency of the VOR evoked by steps of acceleration in darkness (3,000°/s² reaching a velocity of 150°/s) was 5.8±1.7 ms and was the same in response to head rotations in all five planes of rotation. The gain of the reflex during the acceleration was 36.7±15.4% greater than that measured at the plateau of head velocity. Polynomial fits to the trajectory of the response show that eye velocity is proportional to the cube of head velocity in all five planes of rotation. For sinusoidal rotations of 0.5–15 Hz with a peak velocity of 20°/s, the VOR gain did not change with frequency (0.74±0.06, 0.74±0.07, 0.37±0.05, 0.69±0.06, and 0.64±0.06, for yaw, pitch, roll, LARP, and RALP respectively). The VOR gain increased with head velocity for sinusoidal rotations at frequencies 4 Hz. For rotational frequencies 4 Hz, we show that the vertical, torsional, LARP, and RALP VORs have the same linear and nonlinear characteristics as the horizontal VOR. In addition, we show that the gain, phase and axis of eye rotation during LARP and RALP head rotations can be predicted once the pitch and roll responses are characterized.This work was supported by NIH grant R01 DC02390     

Social status constrains the stress response in the squirrel monkey.

The influence of dominance on the pituitary-adrenal and gonadal systems was evaluated in male squirrel monkeys. Basal and stress levels of plasma cortisol and testosterone were determined in eight male pairs across a 5-week period. The data indicated that squirrel monkeys have unusually high levels of steroid hormones in comparison to other species. Dominant males had higher levels of cortisol and testosterone and showed a smaller stress response than did subordinate males.     

Effect of ablation of area postrema on frequency and latency of motion sickness-induced emesis in the squirrel monkey

Twelve young adult squirrel monkeys of the Bolivian subspecies were subjected to continuous counter-clockwise horizontal rotary motion at 25 rpm, together with a simusoidal vertical excursion of 6 in. every 2 sec (0.5 Hz). Each animal was exposed to this motion regimen for a period of 60 min once each week for three consecutive weeks. Following the third weekly motion test bilateral ablation of the area postrema (AP) was performed in eight of the animals by thermal cautery. Two control animals were sham-operated after the third motion test while two additional controls were given the motion tests as noted above but were not operated. The four controls were considered as a single group for statistical analyses of results of the motion tests. After a recovery period of 30 to 40 days, and at a comparable interval in the non-operated controls, each animal was again tested for motion sensitivity for three consecutive weeks. The brains of all of the animals were then fixed by left ventricular cardiac perfusion with Bouin's fluid and processed for histological evaluation of the bilateral AP ablation in comparison with the control brains. Five of the AP-ablated animals postoperatively were completely refractory to the motion stimuli, two exhibited a decreased number of emetic responses, and one exhibited the same number of responses before and after the AP lesions. The controls exhibited no significant difference in emetic sensitivity on the second series of three weekly tests than on the first series. The results of this investigation appear to be in agreement with the observations of Wang and Chinn in the dog [32,33] indicating that the intergrity of the AP (CTZ) is essential to the emetic response to motion.     

Reinforcing concomitants of electrically elicited vocalizations

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 motor 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 tegmentum and lateral medulla. It is hypothesized that the first group contains predominantly or exclusively primary vocalization subtrates; the second group is thought to be composed mainly of structures whose stimulation yields vocalization secondarily due to stimulus induced motivational changes.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 - cl claustrum - coa commissura anterior - coli colliculus inferior - cols colliculus superior - csp tractus cortico-spinalis - db fasciculus diagonalis Brocae - dbc decussatio brachii conjunctivii - f fornix - gc gyrus cinguli - gl corpus geniculatum laterale - gm corpus geniculatum mediale - 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 - lav 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-thalamicus - nst nucl. striae terminalis - oi nucl. olivaris inferior - ol fasciculus olfactorius Zuckerkandl - os nucl. olivaris superior - p pedunculus cerebri - pmc brachium pontis - po griseum pontis - pro area praeoptica - pu nucl. pulvinaris thalami - put putamen - re formatio reticularis - rep nucl. reticularis tegmenti pontis - rub nucl. ruber - s septum - sm stria medullaris - sn substantia nigra - st stria terminalis - sto tria olfactoria lateralis - subt subthalamus - tec tractus tegmentalis centralis - trz corpus trapezoideum - va nucl. ventralis anterior thalami - vpl nucl. ventralis postero-lateralis - vpm nucl. 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     

Canal-otolith interactions driving vertical and horizontal eye movements in the squirrel monkey

The vestibulo-ocular reflex (VOR) was studied in three squirrel monkeys subjected to rotations with the head either centered over, or displaced eccentrically from, the axis of rotation. This was done for several different head orientations relative to gravity in order to determine how canal-mediated angular (aVOR) and otolithmediated linear (lVOR) components of the VOR are combined to generate eye movement responses in three-dimensional space. The aVOR was stimulated in isolation by rotating the head about the axis of rotation in the upright (UP), right-side down (RD), or nose-up (NU) orientations. Horizontal and vertical aVOR responses were compensatory for head rotation over the frequency range 0.25–4.0 Hz, with mean gains near 0.9. The horizontal aVOR was relatively constant across the frequency range, while vertical aVOR gains increased with increasing stimulation frequency. In the NU orientation, compensatory torsional aVOR responses were of relatively low gain (0.54) compared with horizontal and vertical responses, and gains remained constant over the frequency range. When the head was displaced eccentrically, rotation provided the same angular stimuli but added linear stimulus components, due to the centripetal and tangential accelerations acting on the head. By manipulating the orientation of the head relative to gravity and relative to the axis of rotation, the lVOR response could be combined with, or isolated from, the aVOR response. Eccentric rotation in the UP and RD orientations generated aVOR and lVOR responses which acted in the same head plane. Horizontal aVOR-lVOR interactions were recorded when the head was in the UP orientation and facing toward (nose-in) or away from (nose-out) the rotation axis. Similarly, vertical responses were recorded with the head RD and in the nose-out or nose-in positions. For both horizontal and vertical responses, gains were dependent on both the frequency of stimulation and the directions and relative amplitudes of the angular and linear motion components. When subjects were positioned nose-out, the angular and linear stimuli produced synergistic interactions, with the lVOR driving the eyes in the same direction as the aVOR. Gains increased with increasing frequency, consistent with an addition of broad-band aVOR and high-pass lVOR components. When subjects were nose-in, angular and linear stimuli generated eye movements in opposing directions, and gains declined with increasing frequency, consistent with a subtraction of the lVOR from the aVOR. This response pattern was identical for horizontal and vertical eye movements. aVOR and lVOR interactions were also assessed when the two components acted in orthogonal response planes. By rotating the monkeys into the NU orientation, the aVOR acted primarily in the roll plane, generating torsional ocular responses, while the translational (lVOR) component generated horizontal or vertical ocular responses, depending on whether the head was oriented such that linear accelerations acted along the interaural or dorsoventral axes, respectively. Horizontal and vertical lVOR responses were negligible at 0.25 Hz and increased dramatically with increasing frequency. Comparison of the combined responses (UP and RD orientations) with the isolated aVOR (head-centered) and lVOR (NU orientation) responses, indicates that these VOR components sum in a linear fashion during complex head motion.     

Histochemical studies on the spinal cord of squirrel monkey (Saimiri sciureus)

Summary Detailed histochemical observations have been made on the various components of the spinal cord. The gray matter showed much greater enzymatic activity than the white matter. The neuropil and substantia gelatinosa showed mild G6PD, AChE and BChE activity; moderate SDH, LDH, SE and AC activity; and strong AP, ATPase, and AMPase activity. The pia-arachnoid showed moderate to strong activity of dehydrogenases and phosphatases. The cytoplasm of the neurons and neuronal processes gave moderate to very strong reaction for most of the enzymes except BChE. The areas of synaptic endings show the presence of oxidative enzymes, phosphorylases, ATPase and AMPase. It has been interesting to note that phosphorylases, which have been mostly observed in the cytoplasm, nucleoli and synaptic areas of various neurons and in the neuropil, also show intensely strong reactions in the nuclei of ependymal cells lining the central canal as well as in nuclei of some glial cells.List of Abbreviations used AC Acid phosphatase - AChE Acetyl cholinesterase - AK Alkaline phosphatase - AMPase Adenosine monophosphatase (5 nucleotidase) - AP Amylophosphorylase - ATPase Adenosine triphosphatase - BChE Butyrylcholinesterase - G6PD Glucose-6-phosphate dehydrogenase - LDH Lactic dehydrogenase - MAO Monoamine oxidase - PAS Periodic acid Schiff - SDH Succinic dehydrogenase - SE Simple esterases - UDPG Uridinedephosphoglucose glycogen transferase T.R. Shanthaveerappa in previous publications     

Eye movements and vestibular-nerve responses produced in the squirrel monkey by rotations about an earth-horizontal axis

Summary The eye movements produced by constant-speed rotations about an earth-horizontal axis (EHA) are similar in the alert squirrel monkey to those observed in other species. During EHA rotations, there are persistent eye movements, including a nonreversing nystagmus at lower rotation speeds and either a direction-reversing nystagmus or sinusoidal eye movements at higher rotation speeds. Horizontal eye movements are produced by barbecuespit (yaw) rotations, vertical eye movements by head-over-heels (pitch) rotations. The responses can be viewed as composed of a bias component, reflected in the nonreversing nature of the nystagmus, and a cyclic component, reflected in the periodic modulation of slow-phase eye velocity as head position varies. Vestibular-nerve recordings in the barbiturate-anesthetized monkey indicate that neither semicircular-canal nor otolith afferents give rise to a directionally specific dc signal which can account for the bias component. Apparently the appropriate dc signal has to be constructed centrally from a sinusoidal or ac peripheral input. The otolith organs are a likely source of this peripheral input, although contributions from the semicircular canals and from somatosensory receptors must also be considered. Our results suggest that the directional information required to distinguish rotation direction, rather than being contained in the discharge of individual otolith afferents, is encoded across a population of afferents. Possible sources of such information are the phase differences in the sinusoidal responses of otolith afferents differing in their functional polarization vectors.Supported by Grants NS 01330 from the National Institutes of Health and NGR-14-001-225 from the National Aeronautics and Space Administration