On the Inheritance of Direction and Degree of Asymmetry

Collins, Robert L.

doi:10.1016/b978-0-12-286480-3.50009-4

Cited by 161 publications

(135 citation statements)

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“…Like handedness in humans, paw preference in mice, as assessed in a food-reaching task, has been widely used as a robust index of functional brain asymmetry to dissect out the genetic and physiological mechanisms underlying lateralization (Cabib et al, 1995;Collins, 1975Collins, , 1985Denenberg et al, 1991;Nielsen et al, 1997;Nosten et al, 1989;Signore et al, 1991b).…”

Section: Introductionmentioning

confidence: 99%

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Constitutive Hyperdopaminergia is Functionally Associated with Reduced Behavioral Lateralization

Morice

Denis

Macario

et al. 2004

Neuropsychopharmacol

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According to the dopamine (DA) hypothesis of schizophrenia and the strong evidence for decreased cerebral lateralization in schizophrenic patients, we postulated that hyperactivity of the dopaminergic system could be associated with a reduced behavioral lateralization in mice. Mice lacking the dopamine transporter (DAT) gene were used as a genetic model of persistent hyperdopaminergia. The DAT null mutation was transferred on C57BL/6JOrl (B6) and DBA/2JOrl (D2) inbred backgrounds for more than 10 generations of backcrossing to derive three DAT strains, B6, D2, and B6 Â D2(F 1 ). Adult mutant mice of the three DAT strains and their littermates were tested for paw preference using Collins' protocol. Our results demonstrated that, whatever the genetic background, persistent hyperdopaminergia directly impairs the degree of lateralization without affecting the direction. Our results support the degree of lateralization as a good candidate phenotype to further improve genetic analysis of cerebral lateralization in normal and pathological conditions. Neuropsychopharmacology Keywords: schizophrenia; direction and degree of asymmetry; paw preference; knockout mice; cocaine INTRODUCTIONAnomalies in behavioral, neuroanatomical, and neurophysiological asymmetry have been widely documented in schizophrenic patients, supporting lateralization as a good candidate symptom that could contribute to clarifying schizophrenia heterogeneity (Leboyer et al, 1998). A metaanalysis of 19 studies on schizophrenia showed that the prevalence of non-right-handedness was significantly higher in patients than in healthy subjects (Sommer et al, 2001). Similarly, in the meta-analysis of three prospective followup studies, pre-schizophrenic subjects were significantly more often non-right-handed than the general population (Sommer et al, 2001). Furthermore, in vivo imaging studies of schizophrenia have provided evidence that the right-left asymmetry of the dopamine (DA) synthesis capacity and of the dopamine transporter (DAT) binding in the caudate are both lost in antipsychotic-naive patients (Hietala et al, 1999(Hietala et al, , 1995Hsiao et al, 2003;Laakso et al, 2000). In addition, neuroleptics are able to change the balance of hemispheric activity, thus improving left-hemispheric attentional processes (for a review, see Gruzelier, 1999), and a recent study demonstrated that haloperidol-induced downregulation of DA synthesis was significantly greater in the left than in the right striatum (Grunder et al, 2003). Finally, a highly significant correlation was reported between depressive symptoms in antipsychotic-naive schizophrenia and DA synthesis capacity in the left striatum (Hietala et al, 1999).Taken together, these data support the hypothesis of a potential link between cerebral lateralization and schizophrenia, and suggest that abnormal asymmetry of the dopaminergic transmission could be one of the key neurobiological substrates for this functional relationship. Based on the DA hypothesis of schizophrenia, which attributes the positive sc...

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Section: Introductionmentioning

confidence: 99%

“…These criteria correspond to those used by Collins (1991) to select the two lines for the degree of lateralization. The initial studies in genetically uniform mice have shown that these measures of paw preferences in mice are enduring and not task specific (Betancur et al, 1991;Biddle and Eales, 1996;Collins, 1985;Nosten et al, 1989; Signore et al, 1991a, b). …”

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confidence: 99%

Constitutive Hyperdopaminergia is Functionally Associated with Reduced Behavioral Lateralization

Morice

Denis

Macario

et al. 2004

Neuropsychopharmacol

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“…D. Hopkins, Bales, & Bennett, 1993;Kubota, 1990;Matoba, Masataka, & Tanioka, 1991;Westergaard & Suomi, 1997), and in none of these studies can potential genetic factors be isolated from environmental factors, because the offspring in most of these studies were raised by their biological mothers and, therefore, no specific manipulation of rearing environment was performed. Selectivebreeding studies in mice clearly suggest no genetic basis for the determination of directional biases in paw preferences, although strength of paw preference appears to be under some genetic control (see Collins, 1985, for a review).…”

Section: Introductionmentioning

confidence: 99%

“…The pervasiveness of human right-handedness has led to numerous debates about the mechanisms involved in the expression of hand preference (B. Hopkins & Ronnqvist, 1998). Both genetic models (Annett, 1985;Corballis, 1997;Laland, Kumm, Van Horn, & Feldman, 1995;McManus, 1985;Yeo & Gangestad, 1993) and environmental models (Collins, 1985;Provins, 1997) have been proposed to explain the origin of human hand preference. The principal data in support of a genetic basis for hand preference are that it runs in families (Curt, De Agostini, Maccario, & Dellatolas, 1995;Laland et al, 1995;McGee & Cozad, 1980;McManus & Bryden, 1992) and that offspring typically exhibit patterns of hand preference more similar to their biological parents compared with offspring who have been adopted or raised by stepparents (Carter-Saltzman, 1980;Hicks & Kinsbourne, 1976).…”

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confidence: 99%

Heritability of hand preference in chimpanzees (Pan troglodytes): Evidence from a partial interspecies cross-fostering study.

Hopkins

1999

Journal of Comparative Psychology

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Heritability of hand preference was tested in a sample of 188 chimpanzees (Pan troglodytes). Hand preference was measured by coordinated bimanual actions, and concordance percentages were compared between parents and offspring and siblings. Among siblings, concordance percentages were compared for dyads in which both individuals were raised by chimpanzees, both were raised by humans, or 1 was raised in each environment. The results indicated population-level right hand preferences for coordinated bimanual actions. There were no significant associations in hand preference between parents and offspring. In full and maternal half siblings, concordance in hand preference was significantly greater than chance in mother-and human-reared individuals but not in cross-fostered dyads. The cumulative results suggest that the direction of hand preference is heritable in chimpanzees but the mechanism of transmission is not genetic. Several environmental explanations are proposed to explain the findings, including the potential role of maternal cradling bias and in utero fetal position.Approximately 75% to 90% of modern humans report themselves as being right-handed (Annett, 1985;Porac & Coren, 1981). The general view is that human right-handedness evolved within the past 2 to 5 million years, as evidenced by the archeological data suggesting righthand use in tool use and other activities in early hominids (Bradshaw & Rogers, 1993;Corballis, 1991). The pervasiveness of human right-handedness has led to numerous debates about the mechanisms involved in the expression of hand preference (B. Hopkins & Ronnqvist, 1998). Both genetic models (Annett, 1985;Corballis, 1997;Laland, Kumm, Van Horn, & Feldman, 1995;McManus, 1985;Yeo & Gangestad, 1993) and environmental models (Collins, 1985;Provins, 1997) have been proposed to explain the origin of human hand preference. The principal data in support of a genetic basis for hand preference are that it runs in families (Curt, De Agostini, Maccario, & Dellatolas, 1995;Laland et al., 1995;McGee & Cozad, 1980;McManus & Bryden, 1992) and that offspring typically exhibit patterns of hand preference more similar to their biological parents compared with offspring who have been adopted or raised by stepparents (Carter-Saltzman, 1980;Hicks & Kinsbourne, 1976).In contrast with humans, the historical view has been that nonhuman animals, particularly nonhuman primates, do not exhibit population-level handedness (see Ettlinger, 1988;Warren, 1980). In recent years, behavioral research in a variety of nonhuman primate species has revealed that population-level handedness can be found in some species for certain measures (Bradshaw & Rogers, 1993;Fagot & Vauclair, 1991;W. D. Hopkins, 1996b Studdert-Kennedy, & Lindblom, 1987;Ward & Hopkins, 1993). Notwithstanding, considerable disagreement remains about the interpretation of the findings in nonhuman primates as they pertain to human handedness. For instance, McGrew and Marchant (1997) argued that the evidence for population-level handedness in no...

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“…Explaining the pervasive degree of right-handedness in the human species has fostered considerable theoretical debate and empirical investigation. Genetic, biological, and environmental models have been proposed to explain this population-level right-handedness, each with varying amounts of empirical support (Annett, 1999;Collins, 1985;Corballis, 1997;Laland, Kumm, Van Horn, & Feldman, 1995;Previc, 1991;Provins, 1997;Trevarthen, 1996). Equally important are theoretical models proposed to explain the occurrences of left-handedness or non-right-handedness in human populations.…”

Section: Introductionmentioning

confidence: 99%

Birth order and hand preference in chimpanzees (Pan troglodytes): Implications for pathological models of handedness in humans.

Hopkins¹,

Dahl²

2000

Journal of Comparative Psychology

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The effect of birth order on hand preference was assessed in a sample of 154 captive-born chimpanzees. Subjects were classified as first, middle, or latter born using 2 classification criteria based on their birth order. Hand preference was measured using a task that elicited coordinated bimanual actions. Significant birth-order effects were found for both classification criteria, with firstand latter-born subjects exhibiting a lesser degree of right-handedness compared with middle-born subjects. These data suggest that biological rather than sociological factors play a greater role in explaining the observed birth-order effects on hand preference in humans.Approximately 85% to 90% of humans report themselves as being right-handed (Annett, 1985;Porac & Coren, 1981). Explaining the pervasive degree of right-handedness in the human species has fostered considerable theoretical debate and empirical investigation. Genetic, biological, and environmental models have been proposed to explain this population-level right-handedness, each with varying amounts of empirical support (Annett, 1999;Collins, 1985;Corballis, 1997;Laland, Kumm, Van Horn, & Feldman, 1995;Previc, 1991;Provins, 1997;Trevarthen, 1996). Equally important are theoretical models proposed to explain the occurrences of left-handedness or non-right-handedness in human populations. That genetic factors may play a role is supported by the observation that approximately 70% of individuals born to two left-handed parents are right-handed, which is significantly lower than the proportion of fight-handed individuals born to two right-handed parents (McGee & Cozad, 1980;McManus & Bryden, 1992). Genetic explanations account for only part of the variance, however, leaving error or other factors to explain the remaining variability. Rather than emphasize genetic factors, others have suggested that both pre-and postnatal environmental factors play a role in determining non-right-handedness. Such factors include but are not limited to birth season, birth order, maternal age, and prenatal hormones. In these models, righthandedness is perceived as being the normative path of development, and therefore non-righthandedness reflects a deviation from normal development that is due to pathological factors (see Satz, Soper, & Orsini, 1988). Of specific interest to this study are the reports focusing on the effect of birth order on hand preference in humans.Bakan and colleagues (Bakan, 1971;Bakan, Dibb, & Reed, 1973) first reported and theorized about the relationship between birth order and hand preference in humans. Bakan (1971) reported that there was a higher percentage of left-handedness in first-and latter-born offspring (defined as more than 4 birth orders) and postulated that the effects were due to birth trauma experienced by offspring born to primiparous or older women. Bakan (1971) proposed that birth trauma is more likely in women who are giving birth for the first time or for older women who present a higher risk group for prenatal insult. Researchers who ...

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On the Inheritance of Direction and Degree of Asymmetry

Cited by 161 publications

References 29 publications

Constitutive Hyperdopaminergia is Functionally Associated with Reduced Behavioral Lateralization

Constitutive Hyperdopaminergia is Functionally Associated with Reduced Behavioral Lateralization

Heritability of hand preference in chimpanzees (Pan troglodytes): Evidence from a partial interspecies cross-fostering study.

Birth order and hand preference in chimpanzees (Pan troglodytes): Implications for pathological models of handedness in humans.

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