Male chacma baboon (Papio ursinus) sexual arousal: Mediation by visual cues from female conspecifics

(1) The changes in masturbatory behavior for nine adult males exposed to, but not allowed to contact, naturally cycling stimulus females were quite similar to the changes in perineal swelling shown by these females. (2) Serum testosterone concentrations of seven adult males exposed to a cycling stimulus female were related to their masturbatory behavior, with high levels occurring during the female's follicular phase. (3) Graded estradiol benzoate treatments of ovariectomized stimulus females revealed individual dosage levels below which there was no positive effect on the occurrence of visually stimulated male masturbation. (4) The present series of experiments documents the importance which visual cues have in the sexual interactions of this particular species.     

Clinical and EEG phenotypes of epilepsy in the baboon (Papio hamadryas spp.)

Spontaneous seizures have been reported in several baboon subspecies housed at the Southwest Foundation for Biomedical Research (SFBR), including Papio hamadryas anubis as well as cynocephalus/anubis and other hybrids. This study classified clinical and electroencephalographic (EEG) phenotypes in these subspecies based upon interictal and ictal findings, as well as photosensitivity, by scalp EEG. One hundred baboons underwent 1-h EEG studies with photic stimulation (PS), 49 with previously witnessed seizures and 51 without. The animals were classified according to these electroclinical phenotypes: presence or absence of interictal epileptic discharges (IEDs), seizures and photoparoxysmal or photoconvulsive responses. Effects of age, gender, and species on EEG phenotypes were also examined. Six discrete electroclinical phenotypes were identified. Generalized IEDs of 2-3, 4-6, and/or 6-7Hz were identified in 67 baboons. Epileptic seizures were recorded in 40 animals, including myoclonic and generalized tonic-clonic seizures. Thirty-three animals were photosensitive. Although the prevalence of IEDs and seizures were similar in seizure and asymptomatic animals, photosensitivity was more prevalent in the seizure animals (p=0.001). P.h. anubis/cynocephalus hybrids were more likely to be photosensitive than P.h. anubis (p=0.004). The reliable characterization of distinct epileptic phenotypes in this pedigreed colony is critical to the success of future genetic analyses to identify genetic factors underlying their epilepsy.     

The development of the facial nerve in baboon embryos (Papio sp.)

The arrangement of the facial nerve was studied in 21 baboon embroys and fetuses, 2.6–36.0 mm crown-rump length, (25–54 days fertilization age) and one adult. The head and neck regions of eight specimens were reconstructed graphically or with wax. The extramedullary part of the right nerve was traced microscopically and its configuration mapped. In early embryos (11–36 somites, 2.6–6.0 mm) the facial part of the facioacoustic primordium is either in close proximity or contacts the second arch epibrachial placode. It becomes a separate nerve (6.9–16.5 mm embryos) as the geniculate ganglion forms and the placode disappears. The first branches are the chorda tympani and greater petrosal. The pars intermedia and chorda tympani are large at 9 mm and the parent nerve terminates distally as a loose network of intermingling fibers. In 14.8–16.3 mm embryos connections are established with the deep petrosal and maxillary, and the tympanic, vagus and lingual nerves. Peripheral branches course into the occipital, cervical and mandibular regions. Between 18.3 and 36.0 mm the temporofacial and cervicofacial rami become evident and peripheral branches also extend into temporal, zygomatic and buccal regions. Communications are formed with branches of the auriculotemporal, zygomatic, infraorbital, buccal, mental, transverse cervical and great auricular nerves. Branches to the temporal and zygomatic areas lag in development.     

First evidence of population-level oro-facial asymmetries during the production of distress calls by macaque (Macaca mulatta) and baboon (Papio anubis) infants

Infant distress calls are vocal communicative signals present in most animals. In nonhuman primates, they correspond to critical vocalizations for caregiving and contribute to the socio-emotional development of the individual. To our knowledge, no systematic study on the development of oro-facial hemispheric specialization in nonhuman primates infants is available. Thus, we proposed to assess to what extend emotional behaviors underlying distress calls in macaques and in baboons younger than 1 year of age may express lateralization. For the first time, a population-level cerebral lateralization was found for screaming and cooing calls in macaques and for the moaning call in baboons. However, differences in patterns of lateralization were found between the two vocalizations produced by macaques (for cooing, the left-side of the mouth opened widest than the right one and for screaming, a preference toward the right side of the mouth was noticed) as well as a sex effect for cooing. Our findings are discussed within the comparative literature in order to comprehend the ontogenetic and phylogenetic changes of hemispheric specialization for emotions in the primate order.     

Noradrenergic and dopaminergic effects of (+)-amphetamine-like stimulants in the baboon Papio anubis

(+)-Amphetamine, (+/-)-ephedrine, and phentermine are commonly used appetite suppressants that release monoamines from nerve cells by acting as substrates for biogenic amine transporters. One key difference among the three drugs is their selectivity for norepinephrine (NE) release vs. dopamine (DA) release. The NE/DA selectivity ratios for these drugs as determined in vitro [(EC50 NE(-1))/(EC50 DA(-1))] are (+/-)-ephedrine (18.6) > phentermine (6.7) > (+)-amphetamine (3.5). The in vitro data suggest that when administered in vivo, these stimulants might differ in their ability to release DA from nerve terminals in the brain. To test this hypothesis, noradrenergic effects (i.e., plasma NE) and dopaminergic effects (i.e., central DA release) were assessed when each drug was administered intravenously (1.5 mg/kg) to anesthetized baboons. Central DA release was determined via positron emission tomography using the method of [11C]raclopride displacement. In the present investigation, high doses of these stimulants increased plasma NE and DA in parallel, but only (+)-amphetamine released central DA from neurons and decreased plasma prolactin. None of the drugs altered plasma amine metabolite levels, indicating no inhibition of monoamine oxidase activity at the administered doses. Plasma drug levels measured in baboons were higher than those measured in human patients taking prescribed doses of the drugs. Viewed collectively, the present data indicate that typical clinical doses of phentermine and (+/-)-ephedrine may not release central DA in humans, a hypothesis that should ultimately be tested in controlled clinical studies.     

Nonpyramidal neurons in the primate basolateral amygdala: A Golgi study in the baboon (Papio cynocephalus) and long-tailed macaque (Macaca fascicularis)

Nonpyramidal GABAergic interneurons in the basolateral nuclear complex (BNC) of the amygdala are critical for the regulation of emotion. Remarkably, there have been no Golgi studies of these neurons in nonhuman primates. Therefore, in the present study we investigated the morphology of nonpyramidal neurons (NPNs) in the BNC of the baboon and monkey using the Golgi technique. NPNs were scattered throughout all nuclei of the BNC and had aspiny or spine-sparse dendrites. NPNs were morphologically heterogeneous and could be divided into small, medium, large, and giant types based on the size of their somata. NPNs could be further divided on the basis of their somatodendritic morphology into four types: multipolar, bitufted, bipolar, and irregular. NPN axons, when stained, formed dense local arborizations that overlapped their dendritic fields to varying extents. These axons always exhibited varying numbers of varicosities representing axon terminals. Three specialized NPN subtypes were recognized because of their unique anatomical features: axo-axonic cells, neurogliaform cells, and giant cells. The axons of axo-axonic cells formed “axonal cartridges,” with clustered varicosities that contacted the axon initial segments of pyramidal neurons (PNs). Neurogliaform cells had small somata and numerous short dendrites that formed a dense dendritic arborization; they also exhibited a very dense axonal arborization that overlapped the dendritic field. Giant cells had very large irregular somata and long, thick dendrites; their distal dendrites often branched extensively and had long appendages. In general, the NPNs of the baboon and monkey BNC, including the specialized subtypes, were similar to those of rodents.     

A primate model of Huntington's disease: behavioral and anatomical studies of unilateral excitotoxic lesions of the caudate-putamen in the baboon

Unilateral caudate-putamen (CP) lesions induced by the glutamate receptor agonist ibotenic acid in baboons produced a neuropathological and behavioral model of Huntington's disease (HD) in the nonhuman primate. Neuropathological evaluation of the lesioned caudate-putamen revealed a neurodegenerative pattern resembling HD. The ibotenic acid-infused CP areas showed a neuronal loss in Nissl-stained sections and a marked astrocytic gliosis by immunohistochemical staining for glial-fibrillary-acidic protein. Acetylcholinesterase fiber staining was severely reduced in the lesioned CP, while afferent dopaminergic fibers, as shown by tyrosine hydroxylase staining, were relatively spared. There was a moderate reduction of met-enkephalin staining in the globus pallidus-pars lateralis ipsilateral to the ibotenic acid lesion, indicating a partial denervation of this structure following the lesion. In the behavioral studies a dyskinetic syndrome with features in common with HD was provoked in the lesioned animals following dopamine receptor agonist administration (1-2 mg/kg apomorphine). The symptoms included hyperkinesia, chorea, dystonia, postural asymmetries, head, and orofacial dyskinesia. The apomorphine test was highly reproducible and individual animals responded with a similar set and incidence of dyskinesia in successive tests. Since the behavioral observations following excitotoxic caudate-putamen damage parallel symptoms in HD patients given dopamine stimulatory drugs, a hypothesis is presented for the observed abnormal movements suggesting that the CP lesions reduce movement thresholds while the activation of dopaminoceptive regions induces dyskinesias.     

Distribution of central cholinergic neurons in the baboon (Papio papio). I. General morphology

The morphological characteristics of cholinergic neurons in the central nervous system (CNS) of the baboon (Papio papio) were studied by choline acetyltransferase (ChAT) immunohistochemistry and acetylcholinesterase (AChE) pharmacohistochemistry. The distributions of central cholinergic neurons as visualized by these two histochemical techniques were similar in most, but not all regions of the brain and spinal cord. Based upon these observations, central cholinergic neurons that are immunoreactive to ChAT and intensely stained for AChE by the pharmacohistochemical procedure can be divided into four major groups: (1) those in the caudate nucleus, putamen, nucleus accumbens and anterior perforated substance. These ChAT-containing and AChE-intense neurons are large and multipolar, and are scattered throughout these structures. (2) The rostral cholinergic column, which consists of a continuous mass of cholinergic perikarya situated in the medial septal nucleus, nucleus of the diagonal band, and nucleus basalis (Meynert). The ChAT-immunoreactive and AChE-intense cell bodies of the nucleus basalis are a prominent feature in the basal forebrain of the baboon. The labeled neurons are large, multipolar, and hyperchromic and show a tendency to aggregate in cell clusters. These cells are distributed within the full extent of the substantia innominata, often being associated with subcortical fiber networks such as the medullary laminae of the globus pallidus. (3) The caudal cholinergic column, which consists of a continuous group of cholinergic neurons in the caudal midbrain and pontine tegmentum. The rostral component of this group of cells is the nucleus tegmenti pedunculopontinus (subnucleus compacta) and it extends caudally to include the laterodorsal tegmental nucleus. Compared to that in other species the nucleus tegmenti pedunculopontinus in the baboon appears to occupy a relatively greater volume and is composed of a greater number of cholinergic neurons. The cells of the caudal column are large and hyperchromic. (4) Nuclei of origin of somatic and visceral efferents of the cranial nerves (III, IV, V, VI, VII, IX, X, XI, XII) and spinal nerves. In addition to these major cholinergic cell groups, a small population of ChAT-positive and AChE-intense cell bodies can be observed at the floor of the fourth ventricle and in lamina VII and X of the cervical cord. The present findings indicate that although some differences exist, the overall distribution and morphological features of cholinergic cell bodies identified in the baboon brain and spinal cord are similar to those demonstrated previously in investigations of the rhesus monkey and nonprimates.     

EEG and anticonvulsant effects of dipropylacetic acid and dipropylacetamide in the baboon Papio papio

The ability of dipropylacetic acid (DPA) and dipropylacetamide (DPM) to modify EEG and seizure activity was assessed in 4 female and 3 male Papio papio. Doses of 30-60 mg/kg of DPA given at intervals over an 8 h period produced blood levels of 19-44 micrograms/ml which were not protective against intermittent light stimulation (ILS). Administration of 150-200 mg/kg doses at intervals over a 36 h period produced blood levels greater than 150 micrograms/ml and were highly protective against ILS. Similar results were obtained following adminstration of DPM; however, DPM appeared to offer greater protection against ILS. A moderate amount of seizure control was obtained at blood levels of 60-91 micrograms/ml (DPA) and complete blockade occurred at levels greater than 100 micrograms/ml DPA. Background EEG changes were similar following either DPA or DPM and consisted of a striking increase in total spectral power with relative power changes in 10-20 c/sec range, the magnitude of which was related to blood levels of DPA. Both agents produced a quieting effect on behavior without severe depression.     

Cytoarchitecture and intrafrontal connections of the frontal cortex of the brain of the hamadryas baboon (Papio hamadryas).

A study was made of the cytoarchitecture of the lateral and medial frontal cortex in the hamadryas baboon (Papio hamadryas). The frontal corticocortical connections of areas 46, 8, 6, and 4 were investigated by injection of wheat-germ agglutinine conjugated to horseradish peroxiase (WGA-HRP) into different regions of areas 46, 8, and 6. The lateral region of the frontal lobe of the baboon consists of broad areas of motor (area 4), premotor (area 6), and the dorsolateral prefrontal cortex, each of which is further divided into subdivisions with distinct cytoarchitectural features: areas 4a, 4b, 4c; 6aα, 6aβ, 6aγ, 6bα, and 6β; 8A and 8B; 45; 46 and 46ps; 9; 10; and 12. Although the frontal cortex of the baboon brain exhibits the same basic cytoarchitectural features as the frontal corticies of the cercopithecus (campbelli?) (Vogt and Vogt, '19) or the macaque (Walker, '40; Barbas and Pandya, '87, '89), the baboon frontal cortex is very different from that of the macaque and cercopithecus in terms of cytoarchitecture: (1) the baboon frontal cortex has an additional area, termed here “6aγ”, within area 6, which has cytoarchitectural characteristics that are intermediate between those of areas 6 and 8; (2) the aggregation of giant pyramidal cells (> 50 μm. in diameter) is found only in area 4a in the baboon, whereas such aggregates are found in areas 4a and 4b and, occasionally, in area 4c in the macaque; and (3) area 46 of the prefrontal cortex of the baboon can be subdivided into the cortex that surrounds the principal sulcus (area 46) and the upper and lower banks of the principal sulcus (area 46ps). Retrogradely WGA-HRP labeled cells and anterogradely WGA-HRP labeled terminals coexisted in the frontal cortex in a columnar fashion, indicative of a reciprocity among the connections. The frontal cortico-cortical connections of areas 46, 8, 6, and 4 in the hamadryas baboon were organized as follows: (1) areas 46, 8, and 6 were connected to one another, (2) area 4 was connected only to area 6, and (3) these connections showed a gross ventrodorsal topography: the ventral regions of each of areas 46, 8, and 6 were connected more strongly to the ventral than the dorsal regions of the other areas; the dorsal regions of each of areas 46, 8, and 6 were connected more strongly to the dorsal than the ventral regions of the other areas. Moreover, the ventral region of area 6 was more strongly connected to the ventral than to the dorsal region of area 4, whereas the dorsal region of area 6 was more strongly connected to the dorsal than to the ventral region of area 4.     

Transcallosal response (TCR) in the chronic photosensitive baboon preparation, Papio papio. II. Effect of premotor cortical kindling

The chronological pattern of transcallosal response (TCR) and its recovery cycle were studied by single or paired stimulation of the homotopic primary and the secondary (contralateral) cortical site before, during and after primary site premotor cortical kindling in Papio papio. Prior to kindling, the sequential pattern of TCR was early positive (P1), negative (N1), late small positive (P2) and large negative (N2) components. The recovery cycle of both P1 and N1 showed a marked supernormal phase at an inter-stimulus interval of 15-200 msec with a peak at about 30 msec, showing maximal facilitation up to 300%. Kindling, with or without prior low frequency cortical stimulation, resulted in a long-lasting amplitude potentiation of both P1 and N1 and a significant modification of the late components. However, a transient amplitude reduction was noted immediately following completion of stage 5 kindling, presumably due to repeated generalized convulsions. These changes occurred only during primary (kindling), but not secondary, homotopic site stimulation. These findings suggest that a persistently increased callosal transmission is probably due to primary site kindling-induced functional alteration of the synaptic site at the homotopic secondary site cortex. In contrast, the supernormal phase of the TCR recovery cycle was suppressed significantly at the secondary site cortex. Since a similar suppressive effect was observed with a small dose of pentobarbital in naive baboons, kindling is considered to produce enhancement of the inhibitory mechanism. However, a diminished suppressive effect on the supernormality 20 days after the termination of kindling suggests that this suppressive effect is transient. It is probably related to the repeated kindled convulsive seizures rather than to the kindling process itself.     

The influence of cortisone on EEG and seizure activity in the baboon Papio papio.

The ability of cortisone to modify EEG and seizure activity was investigated in the baboon, Papio papio. Acute intramuscular doses (0.5-4 mg/kg) caused a dose-dependent increase in seizure response to a flashing light stimulus. This increase in seizure response was apparent in both seizure duration and the spread of convulsive activity. Along with enhancement of seizures, cortisone was found to cause marked changes in the EEG, ranging from the appearance of interictal paroxysmal activity to alterations in spectral characteristics of the wave forms. Increases in slow waves appeared concomitant with a decrease in fast activity in the 18-25 c/sec range. Since previous studies have indicated that seizure proclivity in the Papio papio is maximal at the time of the day when cortisol excretion rates peak, these findings lend further evidence to the idea that corticosteroids may be involved in the thythmic variation of seizure activity in the baboon.     

Role of the forebrain commissure and hemispheric independence in photosensitive response of epileptic baboon, Papio papio

The effect of monocular intermittent light stimulation (ILS) of either hemivisual field (HVF) of the full visual field (FVF) was examined in Papio papio with or without forebrain bisection. ILS of the HVF or the FVF in non-bisected baboons produced bisymmetrical and bisynchronous spike and wave which was followed by a self-sustained seizure without EEG evidence of hemispheric independence. ILS of the FVF in bisected baboons also produced bilateral spike and wave and self-sustained seizures of a similar nature. With ILS of the HVF in bisected baboons, EEG seizures lateralized largely to the contralateral hemisphere and when the ILS of the HVF was switched to the other eye similarly lateralized spike and wave and a self-sustained seizure were produced in the other hemisphere. These findings suggest that (a) the forebrain commissure, most probably the corpus callosum (and possibly the hippocampal commissure), plays a major but not unique role in the bisynchronization and generalization of the ILS-induced spike and wave and the self-sustained seizures, and (b) each hemisphere possesses independent cerebral excitability to the ILS.