Prosimian learning capacities

A survey of the literature on learning by prosimian primates contradicts a traditional view that they are untrainable. They learn simple operants such as bar pressing readily, work well for the usual rewards, and respond in predictable fashion on schedules of partial reinforcement. Two-dimensional visual discriminations involving pattern and brightness also are learned, as are three-dimensional object discriminations. In the area of complex learning, they not only acquire a variety of difficult tasks, but they also reach a final level of performance that is at or near the level of anthropoids. In each of the following areas, at least one experiment is described in which a prosimian species did as well as one or more anthropoid species: object discrimination learning set, discrimination reversal, delayed response, instrumentation, oddity, and relational problems. The anthropoids to which they are most apt to compare favorably are New World monkeys, a group which they resemble physically, especially with respect to degree of manipulativeness, cortical development, and visual acuity.     

Fast and reliable sexing of prosimian and human DNA

Molecular sexing of mammals is normally done by PCR amplification of Y chromosomal fragments, or coamplification of homologous fragments from both sex chromosomes. Existing primers are often unreliable for distantly related species due to mutations in primer regions. Currently there are no published primers for the sexing of prosimian DNA. We show that an existing method (using the zinc finger protein) based on a size difference between the X and Y homologs does not work in prosimians. Multiple alignments of distantly related mammalian species from Genbank and genome databases enabled us to identify conserved regions in the amelogenin gene. Using these conserved regions, we can target species that have no sequence information. We designed a single, conserved primer pair that is useful for fast and reliable molecular sexing of prosimian primates. A single PCR yields two fragments in males and only one in females, which are easily separated with the use of agarose gels. Amplification of separable fragments was successful in seven species of lemurs, as well as humans.     

Learning set formation in a group of Guinea baboons (Papio papio): Importance of the behavioral variable measured

A recent report of one-trial learning in a group of saddle-back tamarins (Saguinus fuscicollis) conflicted with views of learning set formation based on traditional techniques employing isolated subjects. An experiment is reported in which a group of Guinea baboons (Papio papio) was given a series of discrimination and habit reversal tasks. Both one-trial learning and learning set formation occurred. Analysis of spatial behavior revealed that the group learned in a single trial to discriminate stocked from unstocked zones. Improvement in successes (reinforced “digging”) was progressive but not rapid, indicating learning set formation. It appears that outcomes depend on the behavioral variables chosen.     

Intersexual relationships amongst prosimians

Social relationships between the sexes are an important parameter of group structure and the disperison of breeding individuals within the habitat. An attempt is made to present a speculative hypothesis on the origins of female dominance over males in some prosimian species. This hypothesis links metabolic flexibility with the energetic costs of reproduction in males as well as females. A greater investment in measurements of energy expenditure in the field may return valuable information on prosimian breeding systems, methods of dispersion and population biology.     

Mirror-Directed Social Behaviors of Garnett's Greater Bush Baby (Otolemur garnettii)

Many diurnal anthropoid species direct social behaviors toward their own mirror-image as though viewing a conspecific. To determine whether a nocturnal prosimian species would behave similarly, we videotaped social responses of 45 Garnett's greater bush babies (Otolemur garnettii) observing mirror-images for the first time, scored them for frequency and duration, and compared them with the same behaviors directed elsewhere in the test apparatus. Males scentmarked more than females did, principally with the hindfoot, and most when in immediate proximity to the mirror. Bush babies displayed bipedal posture and threat gestures when oriented directly toward a mirror from a near position. Orientation toward the mirror also increased the frequency of arched-back postures; however, this behavior was not contingent on proximity to the mirror or visibility of the mirror-image. The differential expression of specific behaviors toward mirror-images by male and female bush babies supports the view that this nocturnal prosimian, thought to be dependent on olfaction and audition for communication, is capable of specific recognition by visual cues alone.     

Patterns of sexual dimorphism in body weight among prosimian primates.

Many primatologists believe that there is no sexual dimorphism in body size in prosimian primates. Because this belief is based upon data that came from only a few species and were largely flawed in some aspect of sample quality, I re-examined the extent of sexual dimorphism in body weight, using weights of 791 adult prosimians from 34 taxa recorded over the last 17 years at the Duke University Primate Center. There was no significant sex difference in body weight in 17 species, but males were significantly larger in Nycticebus pygmaeus, Tarsius syrichta, Galago moholi, Galagoides demidovii, Otolemur crassicaudatus and Otolemur garnettii. Moreover, females were significantly larger in Microcebus murinus. Thus, the general lack of sexual dimorphism could be confirmed, notably for lemurs, but prosimians as a group show more variability in sexual size dimorphism than was previously thought. After including previously published data obtained in the wild from 8 additional species, I found significant heterogeneity in the degree of sexual dimorphism at the family level, but only the Indridae and Galagidae were significantly different from each other. Among the prosimian infraorders, the Lorisiformes were significantly more dimorphic than the Lemuriformes. Differences in dimorphism between higher taxonomic groups are discussed in the context of prosimian evolution, concluding that phylogenetic inertia cannot provide a causal explanation for the evolution of sexual dimorphism. The relative monomorphism of most prosimians may be related to allometric constraints and, especially in the Lemuriformes, to selective forces affecting male and female behavioral strategies.     

Kinematic Analysis of Trunk-to-trunk Leaping in <Emphasis Type="Italic">Callimico goeldii</Emphasis>

Leaping to and from vertical trunks is a pattern of locomotor behavior that characterizes the positional repertoire of several prosimian and neotropical primate species. We examined the kinematics of leaping in a group of 6 captive Goeldis monkeys. We introduced a set of 2 wooden, fixed, non-compliant vertical supports in their enclosure and used 2 video cameras set at right angles to document leaping. The supports are 2.5, 6, or 15 cm in diameter and were placed at distances of between 1 and 2 m. We conducted frame-by-frame analyses of 122 leaps. The results indicate that irrespective of distance leaped and the diameter of takeoff and landing substrates, the forelimbs of {Callimico} contacted the landing platform in advance of the hind limbs. Moreover, even when leaping a horizontal distance of 2 m, {Callimico} experienced a downward vertical displacement of only 0.17 m. Several features of the shoulder and forelimb of {Callimico} appear to be associated with enhanced stability at the humeral head and radioulnar joint, and are consistent with the ability to withstand large compressive forces generated when landing on noncompliant substrates. Based on a series of kinematic equations provided by Warren and Crompton (1998a), the mechanical cost of transport in {Callimico} (5.4 m/s^–2) is greater than those of prosimian vertical clingers and leapers. However, compared to other callitrichine primates, {Callimico goeldii} is behaviorally and anatomically specialized for leaping between vertical trunks in the lowest layers of the forest understory.     

Mechanisms of same/different concept learning in primates and avians

Mechanisms of same/different concept learning by rhesus monkeys, capuchin monkeys, and pigeons were studied in terms of how these species learned the task (e.g., item-specific learning versus relational learning) and how rapidly they learned the abstract concept, as the training set size was doubled. They had similar displays, training stimuli, test stimuli, and contingencies. The monkey species learned the abstract concept at similar rates and more rapidly than pigeons, thus showing a quantitative difference across species. All species eventually showed full concept learning (novel-stimulus transfer equivalent to baseline: 128-item set size for monkeys; 256-item set for pigeons), thus showing a qualitative similarity across species. Issues of stimulus regularity/symmetry, generalization from item pairs, and familiarity processing were not considered to be major factors in the final performances, converging on the conclusion that these species were increasingly controlled by the sample-test relationship (i.e., relational processing) leading to full abstract-concept learning.     

The involucrin gene of the galago. Existence of a correction process acting on its segment of repeats

The involucrin gene of the galago, a prosimian, has been cloned and sequenced. The coding region contains a segment of repeats homologous to the segment of repeats in the gene of another prosimian, the lemur, and different from the segments of repeats in the genes of higher primates. The repeats lengths in the two prosimians are similar; and except for a single duplication of a block of repeats in the lemur alone, the number of repeats is the same. However, the nucleotide consensus sequences of the repeats differ between the two species at 3 out of 39 nucleotide positions. The repeats therefore appear to have been modified by a correction process that led toward homogeneity in the repeats of each species while permitting divergence between the two species. The correction process, an example of concerted evolution, has taken place preferentially between adjacent repeats. The numerous differences between the segments of repeats of higher primates and the segments of repeats of lower animals reveal a discontinuity in the evolutionary processes acting on the gene.     

Spatial memory during foraging in prosimian primates: Propithecus edwardsi and Eulemur fulvus rufus

A variety of anthropoids travel efficiently from one food source to another, although there is disagreement over how this is accomplished over large-scale space. Mental maps, for example, require that animals internally represent space, geometrically locate landmarks, use true distance and direction, and generate novel shortcuts to resources. Alternately, topological or route-based maps are based on a network of fixed points, landmarks and routes so that one food patch can be linked with another. In this study we describe travel patterns between food sources for two prosimian species found in southeastern Madagascar, Propithecus edwardsi and Eulemur fulvus rufus. Both species are dependent on fruit and have large home range sizes. By comparing interpatch distances, patch size and turning angles, we found that both species prefer nearest neighbor food patches and P. edwardsi travels in relatively straight lines. The amount of backtracking seen in E. f. rufus may be linked to their large group size and dependence on large-crowned fruit trees. We suggest that the goal-oriented foraging of both prosimian species is dependent on a topological or route-based map. These are rare behavioral data relevant to ecological and social contexts of primate cognitive evolution.     

Smells are no surer: rapid improvement in olfactory discrimination is not due to the acquisition of a learning set.

The claim that rats can demonstrate the 'primate-like' learning capacity of learning set formation when trained with olfactory cues, rather than visual or auditory cues, has generated considerable interest in recent years. In this study, the claim is evaluated in detail by using a series of experimental and control procedures to determine whether rats do indeed develop the abstract 'win-stay, lose-shift' strategy which underlies learning set formation in monkeys. We report here that although exposure to a series of novel olfactory discrimination problems gives rise to progressive improvement in the rate of learning, it is not a necessary condition for the development of that rapid learning. Furthermore, even rats which fail to display progressive improvement in olfactory reversal learning show rapid learning on novel olfactory discrimination problems. Each of these findings suggests that although olfactory learning may be rapid, learning set formation does not occur over a short series of problems.     

Anatomies and lifestyles,morphometrics and niche metrics: Tools for studying primate evolution

In recent years, comparative observations of primate anatomies have been extended using measurements and computer analyses: morphometrics. A question then follows. Can we extend field observations of animal lifestyles using measurement and computer analysis, using, in other words, a new «niche metrics», for comparison with the morphometrics of animal anatomies? This has been attempted (Oxnard, Crompton & Lieberman, 1990) by «measuring» 17 lifestyle variables (on locomotion, environment and diet) for 28 prosimian primate species. These data have been analysed by multivariate statistical methods entirely similar to those used in morphometrics. The results define groups of prosimian species that seem not to be related directly with taxonomy and evolution, but with functional adaptation to lifestyle. Comparisons between the morphometric and niche metric results reveal a degree of similarity of species grouping in each that is apparently related to adaptation and remarkably detailed. But further study of both the morphometric and niche metric results suggests that questions pertaining to evolution may also be asked. Thus, both morphometric investigations seeking clusterings of anatomical variables and niche metric studies seeking clustering of higher taxonomic groups of species produce results that seem to be of developmental and phylogenetic rather than directly adaptive import. Through the combination of these two approaches, it may eventually be possible to partition both evolutionary and adaptive components, even though, of course, there must always be overlap between them.     

Social organization of the Milne-Edward's potto

Nocturnal prosimian primates are often seen alone during their nocturnal activities, and are therefore categorized as "solitary". Recent research has shown that these animals actually possess social networks that differ among species. Here we present new information on one of the lesser studied prosimian primates, the potto, derived from fieldwork in Cameroon that employed radiotelemetry and behavioral observations. An analysis of association patterns and home-range overlaps between animals revealed that pottos associated more frequently with conspecifics than expected for a supposedly solitary primate. Certain males and females that were seen together regularly throughout the study, but were not observed to have contact with other pottos of the opposite sex, were labeled as "pairs". These pairs were found to have higher levels of association with each other than with other conspecifics. The only affiliative and sexual behaviors observed between members of the opposite sex occurred within the pairs of pottos. Although given the secretive nature of these primates, the possibility of extrapair copulations cannot be ruled out, their relatively small testis size indicates that sperm competition is not so important for this species.     

培养海马神经元网络学习模型的构建

对于培养的神经元网络而言,学习是外界刺激与网络响应之间联系建立和调控的过程.为构建合适的神经元网络学习模型,采用闭环低频(1 Hz)成对电极的电刺激模拟认知任务,在多通道微电极阵列系统中对培养的海马神经元网络进行训练,使其发生网络层次上的学习行为.经过训练后,神经元网络在刺激后20～80ms内的早期突触后响应明显增加,响应/刺激比(在闭环训练中,电极上任一阶段连续10次刺激的早期突触后响应的个数/10)增大,响应时延减小,并且响应具有选择性,即表明,神经元网络与外界刺激之间已建立可调控的联系,该可调控联系是通过网络的响应来表现的,建立神经元网络与外界刺激之间的可调控联系即网络层次的学习.     

Volume comparisons in the cerebellar complex of primates. I. Ventral pons

Volumes of the ventral pons (VPo) were measured in 82 brains of primates, Scandentia, and Insectivora, and the relative size of the VPo was expressed by size indices. The reference line was through the prosimian average; the mean index of prosimians was set at 1. The taxonomic groups arranged in a sequence of ascending mean VPo indices were: Insectivora (0.04), prosimians (1.00), monkeys (2.55), apes (4.48) and man (9.44). Thus, the VPo of man is more than 9 times larger than that of isoponderous average prosimians, and more than 230 times larger than that of isoponderous "basal' insectivores. The indices may reflect trends and extent of VPo evolution in primate phylogeny.     

Plasma testosterone transport in primates

All primate species, including Old and New World primates and prosimians have a plasma testosterone-estradiol binding globulin (TeBG), which is a glycoprotein and has a similar mobility in polyacrylamide gel electrophoresis. In New World primates the TeBG binding capacity for [3H]testosterone was higher and its affinity lower than in Old World primates. These changes were associated with high unbound plasma testosterone concentrations in these species. Binding parameters of TeBG in prosimian species varied markedly. Thus, in primate evolution TeBG was conserved despite marked differences in binding characteristics. In New World primates changes are associated with high total and unbound testosterone, a finding concordant with alterations of other steroid hormones concentration in these species with "generalized steroid hormone resistance".     

ANT3 and STS are autosomal in prosimian lemurs: implications for the evolution of the pseudoautosomal region

Comparative in situ hybridization in various primate species has revealed a pseudoautosomal location for the human ANT3 gene and an X-specific location for the steroid sulfatase (STS) gene throughout the higher primate species up to the New World monkeys. However, ANT3 and STS map together on an autosome of two prosimian species of the genus Lemur and Eulemur. These results suggest an autosome-to-X/Y translocation after the simians radiated from the prosimians, resulting in a pseudoautosomal location of genes such as ANT3 and STS. In simian primates, STS then became X-specific by a pericentric inversion in the Y chromosome followed by mutational inactivation of the Y allele.     

Birth of a gene: locus of neuronal BC200 snmRNA in three prosimians and human BC200 pseudogenes as archives of change in the Anthropoidea lineage

The gene encoding brain-specific dendritic BC200 small non-messenger RNA is limited to the primate order and arose from a monomeric Alu element. It is present and neuronally expressed in all Anthropoidea examined. By comparing the human sequence of about 13.2 kb with each of the prosimian (lemur 14.6 kb, galago 12 kb, and tarsier 13.8 kb) orthologous loci, we could establish that the BC200 RNA gene is absent from the prosimian lineages. In Strepsirhini (lemurs and lorises), a dimeric AluJ-like element integrated very close to the BC200 insertion point, while the corresponding tarsier region is devoid of any repetitive element. Consequently, insertion of the Alu monomer that gave rise to the BC200 RNA gene must have occurred after the anthropoid lineage diverged from the prosimian lineage(s). Shared insertions of other repetitive elements favor proximity of simians and tarsiers in support of their grouping into Haplorhini and the omomyid hypothesis. On the other hand, the nucleotide sequences in the segment that is available for comparison in all four species reveal less exchanges between Strepsirhini (lemur and galago) and human than between tarsier and human. Our data imply that the early activity of dimeric Alu sequences must have been concurrent with the activity of monomeric Alu elements that persisted longer than is usually thought. As BC200 RNA gave rise to more than 200 pseudogenes, we used their consensus sequence variations as a molecular archive recording the BC200 RNA sequence changes in the anthropoid lineage leading to Homo sapiens and timed these alterations over the past 35-55 million years.     

Learning how to learn: The significance and current status of learning set formation

In honor of the memory ofHarry F. Harlow, this paper reviews the current status of learning set formation, the discovery of which represents one ofHarlow's major contributions to behavioral science. Learning set formation or “learning how to learn” refers to the learning of visual and other types of discrimination problems progressively more quickly as a function of training on a series of such problems. The general procedure thatHarlow used, his original learning set finding, and its significance are described first. A brief review of theories of learning set formation follows. Lastly, the attempt to use learning set formation as a tool for studying comparative behavior is discussed. This article is based on a paper by the author delivered at:A. M. Schrier andS. J. Suomi (cochairs),Primate Behavior: A Symposium in Memory of Harry F. Harlow. Symposium presented at the IXth Congress of the International Primatological Society, Atlanta, Georgia, August 1982.