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Positional behavior of long-tailed macaques (Macaca fascicularis) in northern Sumatra.

Although the majority of extant primates are described as "quadrupedal," there is little information available from natural habitats on the locomotor and postural behavior of arboreal primate quadrupeds that are not specialized for leaping. To clarify varieties of quadrupedal movement, a quantitative field study of the positional behavior of a highly arboreal cercopithecine, Macaca fascicularis, was conducted in northern Sumatra. At least 70% of locomotion in travel, foraging, and feeding was movement along continuous substrates by quadrupedalism and vertical climbing. Another 14-25% of locomotion was across substrates by pronograde clambering and vertical clambering. The highest frequency of clambering occurred in foraging for insects, and on the average smaller substrates were used in clambering than during quadrupedal movement. All postural behavior during foraging and feeding was above-substrate, largely sitting. Locomotion across substrates requires grasping branches of diverse orientations, sometimes displaced away from the animal's body. The relatively low frequency of across-substrate locomotion appears consistent with published analyses of cercopithecoid postcranial morphology, indicating specialization for stability of limb joints and use of limbs in parasagittal movements, but confirmation of this association awaits interspecific comparisons that make the distinction between along- and across-substrate forms of locomotion. It is suggested that pronograde clambering as defined in this study was likely a positional mode of considerable importance in the repertoire of Proconsul africanus and is a plausible early stage in the evolution of later hominoid morphology and locomotor behavior.

Animals↗

Directional asymmetry in the forelimb of Macaca mulatta.

Asymmetry was investigated in the forelimbs of 150 rhesus monkey (Macaca mulatta) skeletons using measurements of right and left humerii, radii, ulnae, second metacarpals, and femora. Seven of the ten forelimb dimensions were larger on the right than on the left side. Paired t-tests revealed that the mean of the right side was significantly larger than that for the left for two measurements of the ulna and two of the humerus. No measurement was significantly larger on the left than on the right side. These results indicate a small but significant asymmetry in the forelimb bones of rhesus monkeys and, as is the case for humans, the direction of asymmetry favors the right side. Our findings are consistent with an interpretation of hypertrophy of certain muscles and opens the question of whether rhesus monkeys preferentially use their right forelimbs for manipulative tasks that require manual dexterity, as is the case for humans. These forelimb skeletal asymmetries are discussed in light of the recent literature on cortical asymmetry and handedness in nonhuman primates.

Animals↗

Endocranial suture closure in rhesus macaques (Macaca mulatta).

Endocasts from skulls of 330 rhesus monkeys (Macaca mulatta) of known age are scored for closure of nine bilateral and three unilateral sutures or segments of sutures. A variety of tests reveals a strong relationship between age and stages of suture closure, although increasingly broad confidence intervals prevent sutures from being very useful for precisely aging older macaques. The order in which endosutures begin to close, as well as that in which closure is finally achieved, is determined for macaques, and these sequences compared to those for endosutures of humans (Todd and Lyon, 1924). The basilar suture is the earliest to close, while the masto-occipital and rostral and caudal squamosal sutures achieve closure quite late in both species. On the other hand, humans and macaques differ in their schedules for the sphenofrontal suture and in the initiation of closure for the rostral portion of the squamosal suture. Two sutures close significantly sooner on the right than on the left side (the rostral squamosal and masto-occipital) and asymmetry favoring closure of the right lateral lambdoid suture also approaches significance at the 0.05 level. No sutures close significantly sooner on the left side. It is suggested that macaque sutures may close from the inside out, that endosutures are more sensitive than ectosutures for detecting sequences in which cranial sutures begin to close, and that directional asymmetries in suture closure of macaques may be related to minor asymmetries in brain/skull shape (petalias).

Age Determination by Skeleton↗

Morphology of the pubis and preauricular area in relation to parity and age at death in Macaca mulatta.

Some adult human females show bone resorption (pitting) at the dorsal aspect of the pubis and preauricular area of the ilium. The etiology of pelvic bone resorption is attributed alternatively to reproduction and to pelvic anatomy. While most researchers infer that pelvic pitting is related to reproduction, only a few studies are based on women of known parity. Degree of pubic resorption is directly associated with both parity (Suchey et al.: Am. J. Phys. Anthropol. 51:517-539, 1979; Bergfelder and Hermann: J. Hum. Evol. 9:611-613, 1980) and age (Suchey et al.: Am. J. Phys. Anthropol. 51:517-539, 1979). The relationship between parity and degree of resorption of the preauricular area is equivocal, found to be significant by Dunlap (A Study of the Preauricular Sulcus in a Cadaver Population, Ph.D. dissertation, East Lansing, Michigan State University, 1981) but not by Spring et al. (Am. J. Phys. Anthropol. 79:247-252, 1989); both studies report that age is not associated with resorption of the preauricular area. Other mammals evidence public resorption, but the morphology of the preauricular area is less well known. This study addresses the issue on the etiology of pelvic bone resorption using a sample of Macaca mulatta (the free-ranging population from Cayo Santiago) for which parity and age at death are known for all specimens. The following results are reported. Resorption of the pubis is common among females but infrequent among males. Contrary to Rawlins (Am. J. Phys. Anthropol. 42:477-488, 1975), the degree of pubic resorption in female macaques is significantly related to both parity and age at death.(ABSTRACT TRUNCATED AT 250 WORDS)

Age Factors↗

Myelinated fibers of the deep branch of the ulnar nerve at the wrist in bonnet monkeys (Macaca radiata) and some of its branches to the hand.

In order to estimate the peripheral nervous correlates concerning the motor performance of the hand, the myelinated fibers of the deep ulnar nerve and some of its branches to the intrinsic muscles of the monkey (Macaca radiata) hand have been enumerated and their caliber spectra plotted. The content of the myelinated sensory fibers in the deep ulnar nerve was found to be 70% of the total. This high figure is attributable to the fact that 25-50% of the myelinated fibers in the deep ulnar nerve are destined to innervate the joints of the hand. Approximately 50% of the myelinated fibers in nerves to the intrinsic muscles of the hand were sensory.

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Coronary artery distribution in bonnet monkeys (Macaca radiata).

Full use of nonhuman primates as a model for coronary vascular disease has been hampered by several factors, including the limited availability of detailed coronary anatomic data. This study was undertaken to identify the gross coronary arterial anatomy of the Bonnet monkey (Macaca radiata). The hearts of sixteen adult male Bonnet monkeys were subjected to postmortem coronary angiography and gross morphological examination. The main left coronary artery divided into the left anterior descending coronary artery (LAD) and the left circumflex coronary artery (LCA). The posterior descending coronary artery (PDCA) arose from the LCA in 31% of the cases and from the right coronary artery (RCA) in 56% of the hearts. Hearts from two animals (13%) had paired arteries, arising from the LCA and RCA, located in the posterior interventricular groove. The arterial supply to the sinoatrial node originated from the LCA in 69% of the animals and from the RCA in the remainder. The atrioventricular node was supplied by a branch of the RCA in 69% of the animals and from the LCA in the remainder. The coronary anatomy of the bonnet monkey resembles that of man more closely than does the dog in terms of origin of the PDCA, supply of the sinoatrial and atrioventricular nodes, and perfusion of the interventricular septum. The Bonnet monkey may therefore be a useful model for certain specific pathophysiological studies on the coronary circulation.

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Venous distribution of superficial cervical region in rhesus (Macaca mulatta) monkey.

The superficial veins of the cervical region in over 50 Macaca mulatta monkeys were studied. We found, in addition to the external jugular vein, another major vein, which we have termed jugular accessory. It is comparable in size and runs ventral to the external jugular vein. It commenced at the angle of the mouth, ran in a groove on the dorsal aspect of the submandibular gland, and descended on the surface of the sternocleidomastoid muscle where it was connected to the external jugular vein by a short transverse twig. It then descended toward the clavicle, crossed it ventrally, and immediately joined the cephalic vein. The resultant common vein pierced the thoracic wall between the clavicle and first rib and joined the external jugular and axillary veins, producing the subclavian vein. It was the jugular accessory and the external jugular, being connected as described, that formed an "H"-shaped system.

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Characterization of prenatal growth and development in the crab-eating macaque (Macaca fascicularis) by ultrasound.

Diagnostic ultrasound is a valuable tool for the examination of various anatomical structures in vivo. Improvements in technology have increased its effectiveness and provided a noninvasive method for the in utero observation of a variety of structural and functional events. Ultrasound is utilized in our laboratory to monitor a variety of studies during embryonic and fetal development. Basic to these evaluations is the ability to assess normal growth and development. The cynomolgus, or crab-eating macaque (Macaca fascicularis), has been observed in utero by ultrasound from early gestation to term. The earliest detection of implantation is by the identification of a developing gestational sac (GS), which may be visualized on gestational day (GD) 14-15. Positive identification of the GS on GD 16-18 and appearance of the embryo, yolk sac, and cardiac motion on GD 21-25 confirms pregnancy. Once the embryo is evident, measurements of the greatest length (GL) may be used to assess normal growth or to aid in the prediction of gestational age. During the fetal period, a variety of growth parameters aid in fetal evaluation. The gender of the fetus can be accurately identified as early as GD 70-75. An assessment of viability and condition can be determined by the observation of embryonic and fetal heart rates and gross body movement.

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Muscle receptors: content of some of the extrinsic and intrinsic muscles of the larynx in the bonnet monkey (Macaca radiata).

The number of muscle receptors and in particular the muscle spindle content of some of the intrinsic and extrinsic laryngeal muscles was evaluated, using bonnet monkeys (Macaca radiata). The technique of Barker and Ip [J. Physiol. (Lond) 169:73-74, 1963] was used to stain the muscle receptors. The results indicate that the intrinsic laryngeal muscles were devoid of muscle spindles. The extrinsic laryngeal muscles that were examined contain muscle spindles, though their density is less than that reported in the spindle-rich muscles like the rotators of the head and some of the intrinsic muscles of the hand (Cooper in: Structure and Function of Muscle, Vol. I, G.H. Bourne, ed, Academic Press, New York and London, 1960).

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Cardiovascular alterations in Macaca monkeys exposed to stationary magnetic fields: experimental observations and theoretical analysis.

Simultaneous measurements were made of the electrocardiogram (ECG) and the intraarterial blood pressure of adult male Macaca monkeys during acute exposures to homogeneous stationary magnetic fields ranging in strength up to 1.5 tesla. An instantaneous, field strength-dependent increase in the ECG signal amplitude at the locus of the T wave was observed in fields greater than 0.1 tesla. The temporal sequence of this signal in the ECG record and its reversibility following termination of the magnetic field exposure are consistent with an earlier suggestion that it arises from a magnetically induced aortic blood flow potential superimposed on the native T-wave signal. No measurable alterations in blood pressure resulted from exposure to fields up to 1.5 tesla. This experimental finding is in agreement with theoretical calculations of the magnetohydrodynamic effect on blood flow in the major arteries of the cardiovascular system.

Animals↗

Proliferation gradients in the inner ear of the monkey (Macaca mulatta) embryo.

Radioautographic studies were conducted on early developmental stages of the inner ear in monkey (Macaca mulatta) embryos ranging in age from stage 11 to stage 20 (25 to 39 days' gestation) and labeled for one hour with [3H] thymidine. The most active period of proliferation occurred at stage 13, at which time all regions of the otocyst, including the endolymphatic duct, were heavily labeled. In subsequent stages the dorsal portion of the endolymphatic duct failed to incorporate label, whereas proliferation continued in the ventral portion of the duct near its communication with the medial wall of the otocyst. The duct thus appeared to grow upward as a result of cell division from below. Mitotic activity continued in the remainder of the otocyst although there was a progressive temporal decrease in the labeling index. Spatial gradients also occurred, with dorsal and lateral regions less active than ventral and medial ones. As the otocyst differentiated, the cells in various areas became attenuated. These flattened cells were still capable of undergoing cell division, as indicated by the presence of labeled nuclei in all regions of the utricle, saccule, semicircular ducts, and cochlear duct.

Animals↗

The supraoptic nucleus and the supraopticohypophysial tract in the monkey (Macaca mulatta).

The observations here on Golgi material are based on the study of fortunate impregnations in one horizontally sectioned and one frontally sectioned series found in the collection of Golgi preparations of the adult monkey brains (Macaca mulatta) available in this laboratory. The soma of the large supraoptic neurons have jagged protrusions and irregular crevices which give their surfaces a craggy appearance. Also they have a few somatic spines. Their dendrites, which usually arise from two or three dendritic trunks, emerging from the cell body, are moderately branched and have occasional dendritic spines. The axon emerges from a conical elevation either on the soma or a dendrite and is directed towards the supraopticohypophysial tract. In the present material there are a few neurons of the supraoptic nucleus impregnated that are definitely smaller than the larger neurons. They have short beaded axons, ending in the supraoptic nucleus a short distance from their point of origin. In the horizontal sections the supraopticohypophysial tract fibers can be seen passing over the posterior aspect of the optic tract. In the frontal sections, this fan-shaped tract, wide above and constricted below, can be followed into the median eminence. Some of these axons in their intrahypothalamic course have short beaded collaterals. Electron micrographs reveal: (1) endings with spherical synaptic vesicles and endings with flattened synaptic vesicles synapsing on neurosecretory axons in the supraoptic nucleus; (2) a few myelinated fibers containing neurosecretory granules in the intrahypothalamic portion of the supraopticohypophysial tract. As can be seen in both Golgi and electron microscopic preparations the presence of fibrous astrocytes in the supraoptic nucleus and their abundance in the hypothalamic portion of the supraopticohypophysial tract is characteristic of this neurosecretory system. In the nucleus and in the tract processes of the fibrous astrocytes are intimately associated with neurosecretory fibers.

Animals↗

The neurons in the centromedian-parafascicular complex of the monkey (Macaca mulatta): a Golgi study.

The neurons of the nucleus centrum medianum and the neurons of the nucleus parafascicularis were studied in Golgi preparations of the adult monkey (Macaca mulatta). The cell bodies of the prinicipal neurons in the nucleus centrum medianum have a few somatic spines and vary in shape: some are cubical with protruding angles; some are egg-shaped; some are elongated and sausage-shaped. Four to six slightly branched dendrites of unequal thickness radiate from the cell body. Some dendrites extend for nearly 500 microns; all have dendritic spines. In the nucleus parafascicularis there are two varieties of principal neurons: (1) neurons with somatic spines and (2) neurons without somatic spines. The neurons with somatic spines are most numerous. They have polygonal-shaped cell bodies, prominent somatic spines and processes, larger than spines but considerably smaller than dendrites. These processes bear spines and are designated here "microdendrites." Spines and occasionally a "microdendrite" are found on the axon-hillocks. Five to six dendrites of unequal thickness emerge from the cell bodies. Some extend for more than 500 microns; all have prominent dendritic spines. The neurons without somatic spines are relatively few. Usually three exceptionally long, slightly branched dendrites, one apical and two basal, emerge from their elongated, slim cell bodies. Some dendrites extend for more than 800 microns; all have few scattered spines. The Golgi type II neurons found in both of these intralaminar nuclei have small cell bodies and a few, relatively long, undulating dendrites, which bear bulbous dendritic appendages and beaded axon-like processes. Distally on these dendrites, where the appendages and processes are more numerous, the dendritic appendages and axon-like processes form complex entanglements. Distally on these dendrites, where the appendages and processes are more numerous, the dendritic appendages and axon-like processes form complex entanglements. Beaded axons are found on some but not all of the cell bodies. Morphologically these neurons resemble the local interneurons that have been described in various thalamic nuclei.

Animals↗

The basilar pontine gray in the adult monkey (Macaca mulatta): a Golgi study.

In Golgi preparations of the adult monkey (Macaca mulatta) two types of neurons are distinguished in the pontine gray: (1) larger neurons which impregnate most frequently and (2) smaller neurons which impregnate rarely. The former are judged to be projection neurons with myelinated axons because only the initial segments of their axons impregnate, while the latter are judged to be intrinsic neurons since they appear to participate only in the local circuitry of the pontine gray. The projection neurons show a variety of sizes and shapes and are the equivalent of the large, medium and small neurons that Ramón y Cajal ('09) illustrated in the pons of the 5-day-old infant. Their cell bodies are rounded, polygonal, triangular, egg-, pear-, and spindle-shaped. Some have somatic spines. Usually four to seven dendrites issue from the cell body and as they branch they attentuate. The dendrites have knobby, nodular protuberances which give them a gnarled appearance. Also the dendrites have a few scattered spines. In most instances the dendrites have a wavy recurring pattern. Neurons pressed against the corticospinal, corticopontine fiber bundles frequently have elongated cell bodies and the dendrites sprouting from them form, tight, brush-like arrays. The intrinsic neurons have small ellipssoid or pear-shaped cell bodies and two or three long dendrites, which do not taper. In some impregnations short axons issuing from the cell body were found and in other impregnations several widely separated, shor axon-like processes were found on dendrites. A striking feature of the intrinsic neurons is the presence of stalked dendritic appendages bearing one or more bulbous bodies, 1 to 3 microns in diameter. The intrinsic neurons in no way resemble the hairy or mossy cells with short axis cylinders that Ramón y Cajal (09) described in the pons of the 5-day-old infant. The latter were not found in the present material.

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The structural organization of the inferior and lateral subdivisions of the Macaca monkey pulvinar.

Previous light microscopic studies of Macaca pulvinar have demonstrated that both the inferior and adjacent portion of the lateral pulvinar subdivisions are reciprocally connected to the entire occipital lobe, including striate cortex. They differ in that inferior but not lateral pulvinar receives a projection from the superficial layers of the superior colliculus. In this study, the internal organization of these two subdivisions in compared by relating light microscopic Golgi morphology to the synaptic organization observed by electron microscopy. The Golgi impregnated neurons in inferior and lateral pulvinar are typical of other thalamic nuclei and are not qualitatively different in the two subdivisions. Projections neurons (PN) vary in cell body (15--40 micrometers) and dendritic tree (150--600 micrometers) diameters but bear the same varieties of dendritic appendages; spine-like, hair-like, and knot-like. Local circuit neurons (LCN) have smaller cell body diameters (10--20 micrometers) but can have very large dendritic field diameters (150--600 micrometers). They are best distinguished from PNs by their elaborate dendritic appendages, which have been identified as pre-synaptic dendrites in the EM. LCN axons are infrequently seen. In the EM both subdivisions contain four types of synaptic terminals. RS and RL terminal both contain round symaptic vesicles and make asymmetric synaptic contacts, but are subdivided on the basis of small (RS = 0.09 micrometers) versus large (RL = 2.2 micrometers) cross sectional diameters and organelle content. RLs contact larger caliber dendrites and frequently form synaptic complexes with presynaptic dendrites of LCNs, while RSs contact fine caliber dendrites and rarely take part in synaptic complexes. F terminal and P boutons both contain flat and pleomorphis vesicles and make symmetric synaptic contacts. They are characterized by vesicle number and cytoplasmic density. Fs are infrequently observed in pulvinar compared to P boutons and are of uncertain origin. P boutons can be equated with LCN dendritic appendages and have been identified as pre-synaptic dendrites. The quantitative distribution of each type is very similar in both subdivisions, avveraging RS 85%, RL 5%, F 0.3%, P 8% and unidentified 2%.

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The morphology and connections of the posterior hypothalamus in the cynomolgus monkey (Macaca fascicularis). I. Cytoarchitectonic organization.

The cytoarchitectonic organization of the posterior hypothalamus of the cynomolgus monkey (Macaca fascicularis) was analyzed in Nissl, Golgi, acetylcholinesterase, and reduced silver preparations. The region consists of a number of cell masses that differ considerably in their discreteness and in the homogeneity of their neuronal populations. The nuclei identified include: the medial mamillary nucleus (in which at least three distinct subdivisions can be recognized--a pars medialis, a pars lateralis, and a pars basalis); the small-celled nucleus intercalatus; the large-celled lateral mamillary nucleus; a single premamillary nucleus; the tuberomamillary nucleus; the posterior hypothalamic nucleus; the caudal extension of the lateral hypothalamic area; the supramamillary area; and the paramamillary nucleus (which appears to correspond to the nucleus of the ansa lenticularis of other workers). As a basis for the subsequent experimental study of the efferent connections of the posterior hypothalamus, the location of each of these cell masses is described and illustrated in a series of low-power photomicrographs, as are the form and distribution of the resident neuronal populations of the various components of the mamillary complex as seen in Golgi preparations.

Animals↗

The morphology and connections of the posterior hypothalamus in the cynomolgus monkey (Macaca fascicularis). II. Efferent connections.

The efferent connections of the posterior hypothalamus have been analyzed autoradiographically in a series of eight cynomolgus monkey (Macaca fascicularis) brains with injections of 3H-amino acids in different regions of the mamillary complex and the surrounding areas. The medial mamillary nucleus was found to project through the mamillothalamic tract to the ipsilateral anteroventral, anteromedial, and interanteromedial nuclei, and by way of the mamillotegmental tract principally to the deep tegmental nucleus (of Gudden). It also appears to contribute fibers to the medial forebrain bundle, some of which reach as far rostrally as the medial septal nucleus. The lateral mamillary nucleus projects through the mamillothalamic tract bilaterally upon the anterodorsal nuclei of the thalamus, and through the mamillotegmental system to the dorsal tegmental nucleus; it also appears to contribute fibers to the medial forebrain bundle. The supramamillary area has extensive ascending and descending connections that are distributed with the medial forebrain bundle to the hypothalamus and rostral midbrain; in addition, it gives rise to an unusually well-defined projection to field CA2 of the hippocampus and to a narrow zone overlying the outer part of the granule cell layer and the adjoining part of the molecular layer of the dentate gyrus. We have not been able to distinguish the connections of the posterior hypothalamic nucleus from those of the caudal part of the lateral hypothalamic area: they both appear to contribute substantially to the ascending components of the medial forebrain bundle, and through its descending projection to the tegmental fields of the midbrain, the nucleus centralis superior of the raphe complex, the locus coeruleus, and the central gray as far caudally as the facial nerve. Their further projections to the spinal cord were not examined. Viewed broadly, and in the light of previous work, our observations confirm, once again, the constancy of the connections of the hypothalamus in the mammalian brain, and the pivotal position that the posterior hypothalamus occupies in the elaborate system of connections that links the limbic areas of the forebrain with the complex of structures that Nauta has aptly designated the "midbrain limbic region."

Animals↗

A stereotaxic atlas of the brain of the cynomolgus monkey (Macaca fascicularis).

Outline drawings of representative frontal sections of the Macaca fascicularis brain are presented in stereotaxic coordinates. The levels extend from the rostral tip of the neostriatum to the posterior end of the deep cerebellar nuclei. The illustrations are based on the photographs of unstained frozen sections of three formalin-fixed brains in which stainless steel needles were inserted to mark the horizontal zero and several anteroposterior positions. The sections were not stained in order to prevent shrinkage. Stereotaxic measurements were taken in situ of the highest points on the cortical surface, the position of the central and lunate sulcus, and of certain landmarks at the base of the cranium in a large number of monkeys. These data along with brain dimensions and the weight of animals are displayed in tables to indicate individual variations and to aid investigators in determining the best stereotaxic coordinates for a given structure. It is recommended that the cortical point of entry for an electrode or needle be routinely noted and be compared to the parameters in the atlas to compensate for deviations in the horizontal plane.

Animals↗