Neonatal nipple preference and maternal cradling laterality in wild Taihangshan macaques (Macaca mulatta tcheliensis)

Lateralized behavior is considered an observable phenotype of cerebral functional asymmetry and has been documented in many mammalian species. In the present study, we examined evidence of lateralization in neonatal nipple contact, maternal cradling, and the relationship between these two behaviors during the first 12 weeks of life in wild Taihangshan macaques (Macaca mulatta tcheliensis). The results showed that across our sample of nine mother–infant dyads: (1) Seven of nine neonates exhibited a significant left-side nipple preference during the first 12 weeks of life, whereas eight of nine mothers displayed a significant right-side cradling preference; (2) at the population level, there was a significant preference for left nipple contact by neonatal Taihangshan macaques and a significant right-hand maternal cradling preference; (3) at the population level, there was a nonsignificant negative correlation between neonatal nipple preference and maternal cradling bias; and (4) the strength of individual neonatal nipple preference and maternal cradling laterality were not correlated. We conclude that asymmetry in nipple contact of Taihangshan macaques occurs early in behavioral development. Given that infant Taihangshan macaques are able to nurse and cling unassisted to their mothers within a few days after birth, it appears that the infant rather than its mother is responsible for determining a nipple-side preference. Our results indicating a left-side nipple bias in 78% of wild neonatal Taihangshan macaques are most consistent with the heartbeat hypothesis.     

非人灵长类动物雌性携抱婴儿与婴儿吸乳偏好的研究进展

灵长类雌性动物在携抱婴儿时会表现出一种方向偏好,同时,婴儿在吸乳时也会表现出方向偏好.相关研究表明,这两类偏好与灵长类大脑不对称性及其功能的进化有着极其紧密的联系.此方面的研究作为灵长类偏好行为研究的重要关注点之一,在国外已得到了较好的发展,在国内尚处于萌芽阶段.由于多种影响因素的存在,非人灵长类已有的研究结果间存在一定差异.     

Laterality in Maternal Cradling and Infant Positional Biases: Implications for the Development and Evolution of Hand Preferences in Nonhuman Primates

Left-sided maternal cradling has been widely reported in human populations. In this paper, I review the evidence of laterality in maternal cradling and infant positional biases in non-human primates. The review revealed some evidence of population-left sided cradling in great apes but little consistency in bias was found among Old and New World monkeys. Very little data have been reported in prosimians. I further describe how asymmetries in either maternal cradling or infant positional biases may explain individual and species differences in hand preference.     

Jamaican Symmetry Project: long-term study of fluctuating asymmetry in rural Jamaican children.

Fluctuating asymmetry, small deviations from perfect bilateral symmetry, is negatively correlated with health and positively correlated with sexual selection in human adults, but the accumulation, persistence, and fitness implications of asymmetries during childhood are largely unknown. Here, we introduce the Jamaican Symmetry Project, a long-term study of fluctuating asymmetry and its physical and behavioral correlates in rural Jamaican children. The project is based on an initial sample of 285 children (156 boys and 129 girls), aged 5 to 11 years. We describe the design of the project and the methodology of measuring 10 paired morphometric traits. All traits except hand width showed fluctuating asymmetry. Fluctuating asymmetries of the legs tended to be related and were less than half as great as fluctuating asymmetries of the arms and ears. Therefore the legs may show high developmental stability resulting from selection for mechanical efficiency. A fluctuating asymmetry composite score revealed that boys have significantly lower fluctuating asymmetry than girls and that this effect resides mainly in the elbows. There were significant positive relationships between composite fluctuating asymmetry and age, height, and weight, but multiple regression analyses showed that age was negatively related to fluctuating asymmetry, whereas body size was positively correlated. These findings are compared with results from recent English studies.     

On Disturbances of Interhemispheric Interaction in Psychopathologic States (Development of Ideas of L.Ya. Balonov and V.L. Deglin)

The current state of the problem of changes of brain functional asymmetry in psychopathology is reviewed from the point of view of disorders of interhemispheric interaction as the main chain in genesis of affective disorders and schizophrenia. Based on studies of individual activation of the left and right hemispheres as well as on evaluation of cognitive activity, it is shown that psychopathology is accompanied by a disorder of hemispheric interaction with shift of the interhemispheric activation balance towards the right hemisphere in depression and towards the left hemisphere in maniacal states and paranoid schizophrenia. Changes of the activation balance lead to disorder of cognitive activity and human adaptation in the environment. A conclusion is made that disinhibition of subcortical and brainstem structures in psychoses occurs not only vertically, but also horizontally, when the complementary and superpositional interaction of hemispheres shifts to the evolutionary earlier reciprocal type of interaction with domination of cognitive functions of the right hemisphere in depression and of the left hemisphere in the maniacal state and schizophrenia.     

Pre- and Post-Natal Maternal Depressive Symptoms in Relation with Infant Frontal Function,Connectivity, and Behaviors

This study investigated the relationships between pre- and early post-natal maternal depression and their changes with frontal electroencephalogram (EEG) activity and functional connectivity in 6- and 18-month olds, as well as externalizing and internalizing behaviors in 24-month olds (n = 258). Neither prenatal nor postnatal maternal depressive symptoms independently predicted neither the frontal EEG activity nor functional connectivity in 6- and 18-month infants. However, increasing maternal depressive symptoms from the prenatal to postnatal period predicted greater right frontal activity and relative right frontal asymmetry amongst 6-month infants but these finding were not observed amongst 18-month infants after adjusted for post-conceptual age on the EEG visit day. Subsequently increasing maternal depressive symptoms from the prenatal to postnatal period predicted lower right frontal connectivity within 18-month infants but not among 6-month infants after controlling for post-conceptual age on the EEG visit day. These findings were observed in the full sample and the female sample but not in the male sample. Moreover, both prenatal and early postnatal maternal depressive symptoms independently predicted children’s externalizing and internalizing behaviors at 24 months of age. This suggests that the altered frontal functional connectivity in infants born to mothers whose depressive symptomatology increases in the early postnatal period compared to that during pregnancy may reflect a neural basis for the familial transmission of phenotypes associated with mood disorders, particularly in girls.     

Hemispheric participation in the shaping of spatial-motor asymmetry in visual recognition in rats

Asymmetry of movement direction was found in Wistar rats at establishing of motor alimentary conditioned reflex to simultaneously presented visual stimuli. In the course of learning the asymmetry weakened on the whole, but some individuals retained right- or left side preference. The analysis of asymmetry change before and after unilateral cortical inactivation revealed a special role of right hemisphere influences for the formation of right-side preference and of the left hemisphere--for the choice of the left direction. The lack of asymmetry was observed at the presence of the influences from the left hemisphere cortex depressing ipsilateral nigro-striate system and activating the contralateral one. Influences of the cortex of both hemispheres reduce the absolute value of the asymmetry coefficient; the left hemisphere has a special significance for manifestation of temporal asymmetry parameters. Photic interference is a factor modulating the asymmetry. It reduces the right hemisphere activity more than that of the left one; it intensifies right hemisphere influences, contributes to the involvement of the transcallosal conduction channel in the formation of spatial-motor asymmetry.     

Hand preference and tool use in wild chimpanzees

The hand preference of chimpanzees in their natural habitat was studied at Bossou, Republic of Guinea, West Africa. The quantitative difference in left/right hand use was small in food picking and carrying. In contrast, the chimpanzees employed either the right or left hand in nutcracking behavior using a pair of stones. All adults and many adolescents and juveniles utilized one hand exclusively for holding a hammer stone. Left hand preference was more prevalent among adults. However, when adolescents and juveniles were included, there was no significant bias in the ratio of left/right handers. Nut-cracking behavior requires long-term learning of the fine manipulation of stones and nuts by both hands. Each hand has a separate role, and the hands work together in nut cracking. The differential and complementary use of both hands may be a prime factor promoting exclusive hand preference in chimpanzees comparable to that of humans.     

秦岭川金丝猴雌性携抱偏好与婴儿吸乳偏好

为了揭示婴儿吸乳偏好以及母猴携抱偏好发育过程,对具有不同生育背景的出生一周的婴儿吸乳偏好和母亲携抱偏好进行了研究。采用扫描取样法,对32 对母婴(7 个初次生育雌性及其婴儿,25 个多次生育雌性及其婴儿)的雌性携抱婴猴偏好行为,及其婴猴的吸乳偏好行为进行了记录。经对比和相关分析检验,结果显示,初次生育雌性的婴儿在吸乳时出现群体水平上的左侧偏好(t₍₆₎ = - 3.731,P = 0.010),再次生育雌性的婴儿没有出现群体水平的吸乳偏好(t₍₂₄₎ = 0.854,P = 0.402);初次生育的雌性会出现群体水平上的左侧携抱偏好(t₍₆₎ = - 3.890,P = 0.008),再次生育的雌性没有群体水平的偏好方向存在(t₍₂₄₎ = 1. 955,P = 0.062);同母婴儿绝大部分(8/9)会出现相反方向的吸乳偏好(N1 = 8,N2 = 1,P = 0.039)。这表明,再次生育经历会影响秦岭川金丝猴新生婴儿的吸乳偏好进而影响雌性的携抱偏好。     

Sex differences in left-side infant holding: Results from “family album” photographs

Humans tend to cradle infants on the left side of the body. However, it is controversial as to whether left-side cradling is characteristic of women and not of men. Photographic surveys of women and men holding infants have suffered because of underrepresentation of men and lack of accurate information of infants' age. Sampling from “family albums” overcomes these difficulties. A sample of photographs of 1119 women and 577 men indicated (a) left-holding frequencies of 61% women and 47% men, (b) women tended to pose with younger infants, (c) left-side holding was greatest for very young infants (3 months or less) but women showed consistently higher left-side holding for all infant age groups, (d) the distribution of frequency of cradling per individual is skewed towards left-holding for women but for men it is rectangular or perhaps skewed towards right-holding, and (e) there may be family trends in left-holding for women.     

First wild evidence of neonate nipple preference and maternal cradling laterality in Old World monkeys: a preliminary study from Rhinopithecus roxellana

Although captive or free-ranging settings offer a more controlled environment for assessing non-human primate laterality, research on wild populations provides evidence of how laterality is affected by natural environmental conditions and, thus may yield potential insights into the evolution of laterality. This study of Sichuan snub-nosed monkeys (Rhinopithecus roxellana) constitutes the first report on asymmetric patterns of early mother-infant interactions among Old World monkeys in the wild. It was found that neonate nipple preference and maternal cradling laterality are both evident on the individual level. Although there is no significant group-level preference direction, the group preference strength on both measures is evident. Moreover, neonate nipple preference is not significantly correlated with maternal cradling laterality on either LBI scores or the direction (LBI scores: r=0.174, p=0.632; direction: r=0.624, p=0.054). Taken together, it is possible to suggest that wild R. roxellana show independent orientation laterality from the first week of life.     

Hand preferences of captive chimpanzees (Pan troglodytes) in simple reaching for food

We examined chimpanzee hand preference in simple reaching for food, with special reference to manipulative patterns and the developmental shift. We observed 80 captive chimpanzees, ranging from 1 to 25 years old. We also studied the manipulative patterns (grip- types) of 70 individuals as they reached for raisins scattered randomly on the floor. We employed LQ score as a measure of hand preference and designated the subjects right- handers (or left- handers) if they used their right hands (left hands) above chance level. Although the numbers of right- handers and left- handers are almost equal, the distribution of the strength is not symmetrical in both groups. Strong preference was exhibited by more left- handers than right- handers. Subjects > 9 years old exhibited greater hand preference, whereas subjects < 9 years old were ambidextrous. We classified manipulative patterns for reaching into five basic grip- types and analyzed them vis- à- vis age. There is no significant correlation between preferred hand and manipulative patterns. However, adult subjects tended to use an index- and - middle- finger grip with the left hand and to use imprecise grips with the right hand more often than other patterns regardless which hand they preferred. These data demonstrate a developmental shift in hand preference and manipulative patterns and also reveal functional asymmetries between the right and the left hand in Pan troglodytes.     

Interhemispheric asymmetry of positive emotional reactions in rats

Interhemispheric asymmetry of positive emotional reactions was studied in rats: satisfaction of drinking need and self-stimulation. Successive inactivation of the hemispheres was carried out by potassium spreading depression. Switching off of the right as well as the left hemispheres symmetrically influenced the whole quantity of the water, drunk by the rats to a full thirst satisfaction, i. e. the magnitude of need. However, at different stages of drinking need satisfaction an interhemispheric asymmetry was observed: under a strong drinking motivation the right hemisphere dominated, under a weak motivation--the left one. Switching off of the right hemisphere lowered the frequency of self-stimulation of the lateral hypothalamus and switching off the left one heightened it, testifying to the dominance of the right hemisphere in the reaction of self-stimulation. This reaction was also characterized by asymmetry of the lateral hypothalamus nuclei; reactivity to hemispheres inactivation (decreasing or increasing of self-stimulation frequency) of the right nucleus was more expressed than that of the left one.     

Physical criteria of pathological processes. I. Change in the functional hemispheric asymmetry at various stages of rheumatic diseases]

The functional interhemispheric asymmetry of brain in patients with systemic rheumatic diseases was estimated by measuring brain direct current potentials. It is shown that different types of functional interhemispheric asymmetry correspond to different stages of systemic rheumatic diseases. At early stages, the left hemisphere asymmetry dominates, at expressed stages, the right hemisphere asymmetry is prevalent, and the terminal stage is characterized by the loss of functional interhemispheric asymmetry.     

Hemispheric asymmetry of the space-motion component of a food-conditioned motor reflex

The preference of movement direction in the process of motor food conditioned reaction has been investigated in rats with intact brain and after unilateral cortical inactivation. It was shown that the degree of motorspatial preference diminished with the maturation of reaction. At the high level of differentiation the valid preference was shown only in 38% of animals investigated but it was absent in the rest of animals. After inactivation of right hemisphere cortex left-side preference occurred in the presence as well as in the absence of the original preference. Inactivation of the left hemisphere cortex is less significant; it influences the original preference of movement direction permanently affecting those animals which normally had evident preference. It is concluded that the right hemisphere cortex plays dominant part in both sensor and motorspatial components of motor food conditioned reaction. It is supposed that the definite relationship exists between the degree of preference of movement direction and the functional asymmetry of cerebral hemispheres.     

Principles and levels of laterality in unimanual and bimanual stone handling patterns by Japanese macaques

The preferential use of one hand over the other is considered the primary behavioral expression of structural and functional asymmetry in cerebral structures, which is a decisive factor in human evolution. We present the first analysis of manual laterality in a form of object play—stone handling (SH) behavior—in a free-ranging group of Japanese macaques. Defined as a stone-directed manipulative activity, and comprised of multiple one-handed SH patterns (e.g., grabbing a stone in one hand and cradling it against its chest), as well as coordinated two-handed SH patterns with manual role differentiation (e.g., holding a stone with one hand and rubbing it with the other), SH behavior is a good candidate for the study of hand lateralization. We systematically followed the methodological framework developed by McGrew and Marchant (1997) to measure and analyze the presence, strength, and direction of manual preference in the performance of SH behavior and in various SH patterns, both at the individual and group level. Some individuals showed a significant manual lateral bias on a single SH pattern (hand preference), whereas others showed consistency in laterality across all or most of the SH patterns they performed (hand specialization). At the group level, we found that, although their collective distribution of left versus right remained random, most subjects were either significantly but incompletely lateralized, or completely lateralized within particular SH patterns (pattern specialization), but not across all SH patterns (no handedness for SH behavior as a whole). As predicted by the task-complexity model, hand specialization and handedness were stronger in the coordinated bimanual SH patterns than in the unimanual patterns. We discuss the implications of our findings for the evolution of manual preferences in noninstrumental object manipulation versus stone tool use in nonhuman primates and hominins.     

Hemisphere asymmetry of motor-feeding behavior of mice in a multi-alternative symmetrical maze

The behaviour of mice of BALB/c line was studied in a symmetrical multialternative Y-maze: their motor, alimentary and investigating activities as well as spatial-motor asymmetry. In animals with inactivated left hemisphere, as compared to intact ones, the motor and alimentary activities were lowered, and the investigating one augmented. Instead of the weak left-side asymmetry a distinct left-side preference appeared of most Y-maze sections, and right-side preference for approaches to the feeders. Elimination of the right hemisphere did not change the motor activity; the alimentary one decreased and the investigating one augmented, but less than during inactivation of the left hemisphere. On the whole, the right-side asymmetry appeared for all sections. According to all parameters studied, the influence of the left hemisphere on animal behaviour was more expressive and diverse. Spatial preference is formed with participation of influences of both hemispheres. The differences between them are more qualitative than quantitative.     

Hemispheric asymmetry of the nigrostriatal system of the brain in rats genetically predisposed to catalepsy]

Hemispheric asymmetry of nigro-striate system in a strain of rats GC bred from Wistar for a predisposition to cataleptic reaction was studied by means of biochemical and morphological methods. Hemispheric asymmetry was found in GC and Wistar rats with respect to aminopeptidase activity in neurons of caudate nucleus, with a more pronounced left-side increase in GC rats, the asymmetry index being 13.7%. Acetylcholine esterase activity in subcellular particles of caudate nucleus showed an inversion of asymmetry with higher activity in the left hemisphere of Wistar and right hemisphere of GC rats, and asymmetry index of 15.5%. With respect to the number of astroglia cells in S. nigra, and astroglia and oligodendroglia in N. accumbens there was also an inversion of asymmetry in GC rats who had more cells in the structures of the left hemisphere, whereas Wistar rats had more in the right hemisphere. The asymmetry index was high and equal to 29.8% for astroglia in S. nigra, and 17% for astroglia and 21.4% for oligodendroglia in N. accumbens. However, in S. nigra the number of neurons and oligodendroglia cells was equally increased in the right hemisphere in GC and Wistar rats. The data suggest that the mechanism of hereditary pathology of brain nigro-striate system involves both enhancement and inversion of the hemispheric asymmetry.     

Asymmetry of the transcallosal responses in the parietal cortex of kittens in the 1st month of life

In acute experiments on kittens the process of formation of asymmetry of transcallosal responses (TCR) was studied in multiple leads from symmetrical points of the parietal cortex. By the early positive-negative TCR complex, vanishing as a result of callosotomy, predominance of positive components in the right hemisphere was found in 2-7 days kittens, whereas in 8-24 days animals the left hemisphere dominated by both phases of responses. By the late TCR component preserved after section of the callosal body, left-hemispheric asymmetry was found in the elder group of kittens; it was absent in the younger animals. TCR asymmetry in the parietal cortex depended on the sex of the animals. With their age its inversion and enhancement took place. This process is based on the increase of TCR amplitude in the left hemisphere, with no increase in the right hemisphere.     

Changes in Interhemispheric Interaction at the Course Pharmacotherapy of Psychoses

Using graphic tests, preference of space parts and peculiarities of space depth reflection were studied in drawings of in-patients with depression, maniacal state, and paranoid schizophrenia. The examination was performed in the process of the course treatment with neuroleptics and antidepressants. Two opposite patterns of raster filling and space reflection were revealed in the drawings: (1) preference of the left part of space, reflection of objects in the nearest part of space; (2) preference of the right part of space, reflection of the distant part of space. It is suggested that a shift of interhemispheric activation balance towards the right hemisphere occurs in the depressive state, whereas a shift to the left is observed in the maniacal state and paranoid schizophrenia. Psychotropic drugs produce a lateralization effect on cerebral hemispheres: antidepressant amitryptyline leads to a decrease of pathological activation of the right hemisphere, while neuroleptic haloperidol, of pathologic activation of the left hemisphere.