Journal of Comparative Physiology A

, Volume 197, Issue 4, pp 329–337 | Cite as

Oxytocin changes primate paternal tolerance to offspring in food transfer

Original Paper

Abstract

Oxytocin facilitates social recognition in rats and mice, onset of maternal behavior in virgin mice and formation of pair bonds without copulation in prairie voles. However, the relationship between this peptide and paternal behavior in primates remains largely unknown. We investigated whether oxytocin affects paternal behavior in common marmosets. In these primates, fathers as well as mothers take care of their infants, and transferring food to the infants is one of their more obvious caretaking behaviors. We tested whether oxytocin and an oxytocin receptor antagonist affect the transfer of food to offspirng by fathers. After intracerebroventricular infusion of the vehicle, oxytocin, or the oxytocin receptor antagonist, the fathers’ behavior, including picking up food, transferring food to the offspring, and refusing to transfer food to the offspring, was analyzed. Compared with the vehicle, oxytocin reduced the frequency of refusal. This was not caused by reduction of appetite. Although the oxytocin receptor antagonist did not change the frequency of refusal behavior of the fathers statistically significant manner, these observations suggest that the tolerance of the adult male marmoset toward its offspring as shown by the transfer of food is increased by oxytocin administered into the central nervous system.

Keywords

Primate Oxytocin Marmoset Paternal behavior Social behavior 

Introduction

Recent accumulating evidence has indicated that oxytocin, a nine-amino acid peptide, is involved in human social cognition and behavior (Heinrichs et al. 2009). In particular, oxytocin enhances facial emotion recognition (Domes et al. 2007) and memory for positive social information (Guastella et al. 2008; Rimmele et al. 2009), reduces negative evaluation of faces (Petrovic et al. 2008), increases perceived facial trustworthiness (Theodoridou et al. 2009), and promotes actual trusting behavior (Kosfeld et al. 2005; Baumgartner et al. 2008) and altruistic behavior (Zak et al. 2007). These studies were stimulated by rodent studies showing that oxytocin was crucially involved in the regulation of social behavior, such as pair-bonding (Williams et al. 1994; Insel and Hulihan 1995), and social memory (Engelmann et al. 1998; Ferguson et al. 2000).

Oxytocin has been originally known as a hormone that increases contraction of the uterus during labor, stimulates the ejection of milk and controls maternal behavior. Infusion of oxytocin into the ventricle can also initiate maternal behaviors, such as nest building, and licking and retrieving pups in virgin female rats (Pedersen and Prange 1979; Pedersen et al. 1982). In nonhuman primates, oxytocin also increases the affiliative behavior toward infants in rhesus macaque females (Holman and Goy 1995; Boccia et al. 2007). In humans, Feldman et al. (2007) have shown a correlation between maternal behavior and peripheral oxytocin level. The peripheral oxytocin level in the perinatal period was positively related to maternal bonding behavior, including gazing at, vocalization for, positive affect toward and affectionate touching of infants. In addition, a recent study showed that oxytocin receptor genotype was related to the responsiveness of mothers to their toddlers (Bakermans-Kranenburg and van Ijzendoorn 2008). Thus, oxytocin is mainly known to be a promoter of maternal behavior.

A nonapeptide similar to oxytocin that is known to be a promoter of paternal behavior is arginine vasopressin. The infusion of arginine vasopressin into the lateral septum promotes paternal behavior (grooming, crouching, retrieving and contact) (Wang et al. 1994). However, some studies have shown the positive relationship between oxytocin and paternal behavior not only in rodents (Parker et al. 2001; Bales et al. 2004), but also in humans (Feldman et al. 2010). Considering the broad effects of oxytocin on social cognition and these results, it is important to consider the effect of oxytocin on paternal behavior in detail.

Adult males of many primate species, including humans, provide care to infants and juveniles (van Schaik and Paul 1996). In particular, among the callitrichid species, males play an active role (Ingram 1977; Rothe et al. 1993; Yamamoto 1993; Washabaugh et al. 2002; Mills et al. 2004). Categories of male–infant interaction observed in these species are similar to those in humans, such as carrying, protecting, food sharing, grooming, playing and being proximate (Whiten 1987). In addition to the extensive paternal behavior, callitrichids are unusual among primates in that food transfer from adults to offspring is frequently observed (Brown et al. 2004). In longitudinal studies, the frequency of food transfer to infants increased to a maximum around the weaning period and then decreased gradually (Feistner and Price 1990, 2000; Price and Feistner 2001). This pattern is shaped by the begging behavior (approaching and/or calling to take the food) of infants changing with age (Feistner and Price 2000; Price and Feistner 2001) and by the tolerance of adults to such begging behavior (Saito et al. 2008). In our previous study using common marmoset (Callithrix jacchus) families consisting of breeding pairs, older offspring (29–49 weeks old) and younger offspring (7–15 weeks old), both mothers and fathers refused food to older offspring more frequently than younger offspring, and transferred food more often to younger offspring than to older offspring. Thus, the frequency of food transfer from parents to their offspring can be an index of tolerance that changes according to the age of offspring.

In this study, we provide data on the effect of oxytocin and an oxytocin receptor antagonist on the transfer of food to offspring by fathers living with their pair mates and offspring. Of course, marmoset fathers exhibit many types of paternal behavior described above; however, these behavioral patterns change in a week and are not stable. We used the food transfer test because of the stability for a few months as shown in our previous study (Saito et al. 2008). In experiment 1, we tested whether oxytocin decreases the frequency of refusal behavior of fathers to older offspring (24–31 weeks old). Since offspring in this age are normally refused food by fathers, it seemed to be easy to investigate the effect of oxytocin, which was expected to increase the tolerance of fathers. In experiments 2 and 3, we investigated whether an oxytocin receptor antagonist decreases the frequency of food transfer and increases the refusals by fathers to younger offspring (7–16 weeks old). Since fathers are usually willing to share food to offspring at this age, it seemed easy to investigate the effect of oxytocin receptor antagonist that was expected to decrease the tolerance of fathers. Moreover, oxytocin is known to affect food intake (Arletti et al. 1989). Therefore, as we were concerned with the possibility that the anorexigenic effect of oxytocin affects the food transfer behavior of fathers, we examined this effect by testing fathers alone in experiment 4.

Methods

Animals and housing conditions

Six adult male common marmosets (weight, 344–507 g; aged 3–6 years) were used. They were housed at the National Institute of Neuroscience, National Center of Neurology and Psychiatry (NCNP), Japan. Each of these monkeys was the breeding male of a family consisting of a breeding pair and one or two twin litters of their offspring. The adult males were tested behaviorally with one of the twins alternately.

The marmosets were fed the CLEA New World monkey diet (CMA-1M) between 1030 and 1230 hours. From Monday to Saturday, supplementary foods, steamed sweet potatoes, bananas and yogurt were fed between 1500 and 1830 hours. Experiments were conducted in the animals’ home cages between 1430 and 1630 hours before the supplementary feeding. Water was available ad libitum, and the monkey diet (CMS-1M) was available until immediately before the experiments.

Surgery

To implant a guide cannula (22 gauge, 11 mm, Plastics One, Inc.) into the lateral ventricle, the monkey was anesthetized with an intramuscular injection of ketamine (7.5 mg kg−1) and an intraperitoneal injection of pentobarbital sodium (15–20 mg kg−1) and placed into a stereotaxic apparatus. A supplementary mixture of ketamine (7.5 mg/kg−1) and dexmedetomidine hydrochloride (0.15 mg kg−1) was injected into the muscle during surgery. Antibiotics were administered postoperatively for >1 week to prevent infection. The location of the lateral ventricle was estimated from magnetic resonance images by referring to the position of ear bars. The placement was confirmed by the presence of cerebrospinal fluid in the lumen of the cannula during the surgery. The placement was also confirmed by the observation that the infusion of angiotensin II (2 nmol/2 μl; Human Peptide Institute, Inc. Osaka, Japan) into the same site in these subjects caused drinking behavior (Wright et al. 1985). This infusion was conducted after a recovery period of 3 days, and the procedure of infusion was the same as the subsequent intracerebroventricular peptide infusion.

Peptide and intracerebroventricular infusion

Solutions of oxytocin (Bachem, Torrance, CA, USA) (1.0 and 5.0 μg/5 μl) and an oxytocin receptor antagonist [(d (CH2)51, Tyr(Me)2, Thr4, Orn8, Tyr-NH29)-Vasotocin] (Bachem) (0.05, 0.5 and 5.0 μg/5 μl) were prepared in buffered, sterile saline for delivery with a single 5-μl injection. About 30 min before behavioral testing, each monkey was removed from his home cage and gently hand restrained. During the intracerebroventricular infusion, the monkey was anesthetized with isoflurane (1.5%). A dummy cannula (Plastics One, Inc) screwed into the guide cannula was removed and replaced with a 28-gauge inner cannula (Plastics One, Inc), attached to a 25-μl Hamilton syringe. Using aseptic techniques, 5 μl of saline or peptide solution was infused into the lateral ventricle over 4 min. The patency of the cannula was determined by the free flow of the injectate. Behavioral testing was conducted 15 min after the completion of infusion.

Behavioral testing

The marmoset fathers’ tolerance toward their offspring was measured in the food transfer test we developed and reported previously (Saito et al. 2008). The monkeys’ home cages were divided into two parts (80 × 60 × 50 cm3) using a mesh partition, and one father and one offspring were enclosed in one side of the cage (Fig. 1a, b). The 5-min test session started with the presentation of 1-cm cubes of steamed sweet potatoes, which was a familiar preferred food for marmosets. The cubes of potatoes were placed on an acrylic board about 10 cm away from the front of the cage, so that only the father could reach the food. During a session, five cubes of potatoes were continuously presented and replenished as needed.
Fig. 1

Experimental setting (a) and animals behaving during the food transfer test (b)

The behavior of both the father and offspring during each test session was videotaped and analyzed later. The occurrences of all of the following behavioral patterns were also recorded. Pickup the father picked up a cube of potato. Interest while the father was in possession of a food item, the offspring approached the father within a distance of 10 cm and looked at the food item. Begging the offspring emitted vocalization while exhibiting interest. The episode of interest and begging ended when the distance between the father and offspring became more than 10 cm, or when the food item had been completely eaten or dropped by the father. Refusal the father moved away from, turned its back on, emitted chattering vocalization defending the food (Epple 1968), or pushed away the offspring showing interest in the food item. Transfer the offspring licked, took a bite from, or took the whole food item being held by the father. Transfer was necessarily preceded by an episode of interest, but not necessarily by begging. Food transfer could occur after a father showed refusal. These behavioral categories almost corresponded to those of Brown et al. (2005) except pickup.

One test set consisted of two behavioral tests conducted on two consecutive days. On the first day, the father was tested with no injection. On the second day, the father was tested after an injection of oxytocin, the oxytocin receptor antagonist or the vehicle. A part of the data from the first day was used to confirm the recovery from anesthesia by comparing them with the data from the second day (see “Statistical analysis”). There was an interval of 1 or 2 days between the test sets.

Experimental design

For experiment 1, five monkeys were used to determine whether oxytocin changes paternal behavior for relatively older (24–31 weeks of age) offspring. Each father received three types of injection: low-dose oxytocin (1.0 μg), high-dose oxytocin (5.0 μg) and vehicle (saline). In experiment 2, four fathers were tested to examine whether the oxytocin receptor antagonist could reduce the tolerance of these fathers to younger (7–16 weeks of age) offspring. They received four types of injection: low-dose oxytocin (1.0 μg), low-dose oxytocin receptor antagonist (0.05 μg), high-dose oxytocin receptor antagonist (0.5 μg) and vehicle. In experiment 3, four fathers were tested with younger (10–16 weeks of age) offspring. They received two types of injection: extra high-dose oxytocin receptor antagonist (5.0 μg) and vehicle. All of these injection types were repeated four times for each monkey. In two of these four trials, each father was tested with one of his twins, and in the other two trials, with the other of his twins. The minimum dose of each peptide was in accordance with those in Winslow and Insel (1991).

In addition, in experiment 4, six fathers were tested alone to investigate the effect of oxytocin on food ingestion, because oxytocin is known to affect food intake (Arletti et al. 1989). They received two types of injection: low-dose oxytocin (1.0 μg) and the vehicle. Each injection type was repeated twice for each monkey. The order of treatment was pseudo-randomized in each experiment. The number of subjects, age of offspring and treatment of each experiment are summarized in Table 1.
Table 1

The experimental design

Experiment

N

IDs of subjects

IDs of offspring

Age of offspring in week

Types of injection

1

5

KY

SG, NR

24–31

 

YN

CH, RK

OT 1.0 μg/5 μl

WN

GU, MU

OT 5.0 μg/5 μl

TR

KI, LL

Vehicle

TM

HN, OL

 

2

4

KY

SG, NR

7–16

OT 1.0 μg/5 μl

YN

CH, RK

OTA 0.05 μg/5 μl

WN

GU, MU

OTA 0.5 μg/5 μl

TR

KI, LL

Vehicle

3

4

KY

BN, RN

10–16

 

WN

NU, PU

OTA 5.0 μg/5 μl

TR

ZZ, RK

Vehicle

MS

QQ, JN

 

4

6

KY

 

YN

 

WN

OT 1.0 μg/5 μl

TR

Vehicle

TM

 

MS

 

OT oxytocin, OTA oxytocin receptor antagonist

Statistical analysis

The frequencies of pickup, interest, begging, refusal and transfer during testing after each infusion were analyzed. We constructed a generalized linear mixed model to test the effect of the treatments on the frequency of each behavioral pattern. It was exhibited using R 2.7.0, with a Poisson distribution of errors. Generalized linear models are available for fitting fixed effect models to non-normal data. Mixed models allow both fixed and random effects to be fitted to a model. The inclusion of random effects allows us to model residual correlations due to repeated tests of the same individual (Brown and Prescott 1999). We included father and offspring identity as random effects to avoid pseudoreplication of the same individuals. Intracerebroventricular infusions of peptides were considered as fixed effects. All effects of oxytocin and the oxytocin receptor antagonist were expressed by comparison with those of the vehicle.

To confirm the recovery from isoflurane anesthesia, we constructed a generalized linear mixed model to test the effect of the anesthesia on the frequency of food pickup in the same way as above. Here, we included father identity as a random effect. We used the frequency of pickup with no injection (no anesthesia) and that with injection of saline (anesthesia) in experiment 4. The treatment of anesthesia was a fixed effect.

Results

In experiment 1, the administration of both low (1.0 μg) and high doses (5.0 μg) of oxytocin significantly reduced the frequency of refusal toward older offspring compared with the administration of the vehicle (Fig. 2a, Table 2). Similarly, in experiment 2, the administration of low-dose (1.0 μg) oxytocin reduced the frequency of refusal toward younger offspring compared with that of the vehicle (Fig. 2b, Table 2). Other behavioral patterns of fathers and offspring were not significantly affected by oxytocin administration (Fig. 2a, b, Table 2). These findings clearly show that oxytocin can reduce fathers’ refusal.
Fig. 2

Box plots of number of pickups, interests, beggings, refusals and transfers in each experiment. The horizontal line indicates the median values. The bottom and top of the box show the 25th and 75th percentiles, respectively. The vertical dashedlines indicate one of two things: either the maximum value or 1.5 times the interquartile range of data, whichever is smaller. The circles show the outliers. OT oxytocin, OTA oxytocin receptor antagonist. a Results of experiment 1; fathers tested with older (24–31 weeks) offspring (N = 5). b Results of experiment 2: fathers tested with younger (7–16 weeks) offspring (N = 4). c Results of experiment 3: fathers tested with younger (10–16 weeks) offspring (N = 4). d Results of experiment 4: fathers tested alone (N = 6)

Table 2

A list of the results for the model test of generalized linear mixed model

 

Intercept

OT 1.0 μg

OT 5.0 μg

    

b

SE

z

P

b

SE

z

P

b

SE

z

P

    

Experiment 1: N = 5, repeat four times for each condition/with older (24–31 weeks) offspring

Pickup

2.76

0.07

41.35

<0.001

−0.14

0.08

−1.73

0.08

−0.06

0.08

−0.79

0.43

    

Interest

2.46

0.09

28.53

<0.001

−0.18

0.10

−1.86

0.06

−0.079

0.09

−0.85

0.40

    

Begging

1.46

0.28

5.18

<0.001

−0.22

0.15

−1.445

0.15

−0.10

0.14

−0.67

0.51

    

Refusal

1.96

0.16

12.41

<0.001

−0.30

0.13

−2.379

0.02

−0.25

0.1243

−2.014

0.04

    

Transfer

1.36

0.15

9.16

<0.001

−0.08

0.16

−0.493

0.62

0.19

0.1501

1.29

0.20

    
 

Intercept

OT 1.0 μg

OTA 0.05 μg

OTA 0.5 μg

B

SE

z

P

b

SE

z

P

b

SE

z

P

b

SE

z

P

Experiment 2: N = 4, repeat four times for each condition/with younger (7–16 weeks) offspring

Pickup

2.83

0.07

41.82

<0.001

−0.004

0.09

−0.04

0.97

−0.07

0.09

−0.79

0.43

0.004

0.09

0.04

0.97

Interest

2.41

0.10

24.99

<0.001

−0.17

0.11

−1.49

0.14

−0.11

0.11

−0.99

0.32

−0.03

0.11

−0.26

0.79

Begging

0.21

0.41

0.52

0.60

0.19

0.27

0.68

0.50

0.32

0.26

1.2

0.23

0.35

0.23

1.55

0.12

Refusal

0.98

0.34

2.87

0.004

−0.6

0.26

−2.31

0.02

−0.10

0.23

−0.43

0.67

0.01

0.19

0.05

0.96

Transfer

1.98

0.15

13.04

<0.001

0.07

0.13

0.58

0.57

−0.08

0.13

−0.59

0.56

−0.02

0.13

−0.13

0.90

 

Intercept

OTA 5.0 μg

        

b

SE

z

P

b

SE

z

P

        

Experiment 3: N = 4, repeat four times for each condition/with younger (10–16 weeks) offspring

Pickup

2.56

0.09

27.52

<0.001

−0.0001

0.10

0.00

1.00

        

Interest

2.01

0.14

14.83

<0.001

0.04

0.13

0.33

0.75

        

Begging

−2.08

0.73

−2.85

0.004

0.40

0.67

0.59

0.56

        

Refusal

−0.65

0.61

−1.06

0.29

0.55

0.33

1.70

0.09

        

Transfer

1.81

0.10

17.93

<0.001

−0.06

0.15

−0.42

0.67

        
 

Intercept

OTA 5.0 μg

        

b

SE

z

P

b

SE

z

P

        

Experiment 4: N = 6, repeat two times for each condition/alone

Pickup

2.35

0.09

26.39

<0.001

−0.02

0.13

−0.13

0.90

        

OT oxytocin, OTA oxytocin receptor antagonist

In contrast, in experiment 2, neither low (0.05 μg) nor high (0.5 μg) doses of the oxytocin receptor antagonist affected paternal behavior (Fig. 2b, Table 2). Even the extra high dose (5.0 μg) of the oxytocin receptor antagonist did not change paternal behavior patterns toward younger offspring in experiment 3 (Fig. 2c, Table 2). These findings indicate that the specific type of oxytocin antagonist did not affect paternal behavior.

To examine the anorexigenic effect of oxytocin, we determined the frequency of food pickup after administration of low-dose (1.0 μg) oxytocin when the father was alone in experiment 4. The number of food pickups was not significantly changed (Fig. 2d, Table 2).

The anesthesia did not affect the frequency of pickups in experiment 4 (with injection of saline: Median = 10, with no injection: Median = 10.5, Table 3). Therefore, it was considered that subjects recovered from anesthesia in the behavioral tests.
Table 3

The results for the model test of generalized linear mixed model to test the effect of the anesthesia

 

Intercept

Anesthesized

b

SE

z

P

b

SE

z

P

Pickup

2.31

0.09

25.42

<0.001

0.04

0.13

0.32

0.75

N = 6, repeat two times for each condition/alone

Discussion

Father marmosets showed a significant decrease in the number of times they refused both their older and younger offspring in the food transfer test after administration of oxytocin into the central nervous system. Our data suggest that oxytocin makes fathers more tolerant of their offspring in this situation. This is the first study clearly demonstrating a direct effect of oxytocin on a social behavior between fathers and offspring in primates.

As discussed in the introduction, oxytocin is known to be a promoter of maternal behavior rather than paternal behavior, because there is sexual dimorphism of the effects of oxytocin and vasopressin in rodents (Young et al. 1998). In marmosets, fathers show an abundance of vasopressin V1a receptors in their brains compared with individuals who are not fathers (Kozorovitskiy et al. 2006). Until now, there has been little evidence that suggests a relationship between oxytocin and paternal behavior in primates. Although our results do not enable us to distinguish whether oxytocin promoted true paternal behavior or a general tolerance, they raise the possibility that primate paternal behavior is mediated by oxytocin in primates.

We observed that the frequency of actual food transfer from father to offspring did not change after the administration of oxytocin. This result appears to be inconsistent with the hypothesis that oxytocin can stimulate fathers’ caretaking behavior. One possible explanation is that the offspring were not very sensitive to the fathers’ change in tolerance. As we have discussed, in general, the fathers’ level of tolerance depends on the age of the offspring (Saito et al. 2008). Even if the rate of refusal behavior from the father was temporarily reduced by oxytocin administration, the older offspring might not have had the courage to take food from the father who had repeatedly refused them in the past. On the other hand, the fathers might already have been transferring sufficient food to the younger offspring; thus, the effect of oxytocin on the frequency of food transfer to the younger offspring might have been masked by a ceiling effect.

We recorded the frequencies of pickup, interest, begging, vocalization, refusal and transfer according to the previous studies (Brown et al. 2005; Saito et al. 2008). In addition to these behavioral categories, food transfer calls emitted by adults are important for successful food transfer to infants in cotton-top tamarins (Joyce and Snowdon 2007). This behavior of fathers might be affected by the administration of oxytocin. However, although we cannot deny the possibility that we could not record food transfer calls because of noise or calls produced by the other animals in the same room, as far as we observed, the fathers emitted few vocalizations except chattering vocalizations of anger. This type of vocalization was observable because of the vibration of breasts.

None of the doses of the oxytocin receptor antagonist we used had an effect on the fathers’ behavior in the food transfer test. We used the same oxytocin receptor antagonist as that centrally administered to the squirrel monkey by Winslow and Insel (1991). Actually, although they considered it a selective oxytocin antagonist, they were also unable to show any effect with administration of oxytocin receptor antagonist. It is possible that the ligand that works well in rodents fails to bind selectively to the oxytocin receptors in primate brains (Toloczko et al. 1997; Boccia et al. 2001). For example, Smith et al. (2010) showed that another oxytocin receptor antagonist reduces the food transfer between paired adult males and females in black-pencilled marmosets. Although we could not compare simply the food transfer of male–female pair and that of father–offspring pair, the oxytocin receptor antagonist (L-368,899) they used might change the fathers’ behavior to offspring.

Alternatively, since it was shown by Bales et al. (2004) that oxytocin receptor antagonists have marked effects on male parenting in voles only when administered simultaneously with vasopressin receptor antagonists, it can be considered that males can use either oxytocin or vasopressin receptor systems to facilitate paternal behavior. In addition to vasopressin, paternal behavior of callitrichid species is correlated with many other hormones, such as testosterone, cortisol and prolactin (Dixson and George 1982; Mota and Sousa 2000; Nunes et al. 2000; 2001; Schradin et al. 2003; Ziegler et al. 2004; Mota et al. 2006). Especially, the causal effect of prolactin has been shown (Ziegler et al. 2009). These candidates might modulate the effect of oxytocin receptor antagonists.

We examined whether oxytocin reduced the frequency of food pickup by fathers to exclude the possibility that they had reduced their refusal behavior because of anorexia. Administration of oxytocin did not change the frequency of food pickup by the fathers, which appears to disagree with a previous report that oxytocin inhibits feeding behavior in rats (Arletti et al. 1989). However, that study investigated the feeding behavior of rats after 21 h of fasting. The effect of oxytocin on feeding behavior may differ in the nondeprived condition under which our study was conducted. Our findings indicate that the decrease in the frequency of refusal was not the result of changes in the fathers’ appetite.

Common marmosets have characteristic behavioral repertoires in addition to food transfer from parents to offspring, such as imitation (Voelkl and Huber 2000, 2007), sharing of food by dominant individuals with subordinates in the group (even those without kin relationships) (Kasper et al. 2008) and unsolicited prosocial behavior (Burkart et al. 2007). These behavioral repertoires may be facilitated by the cooperative breeding system of marmosets (Burkart and van Shaik 2010). Humans are also cooperative breeders (Hrdy 2005). Moreover, human prosocial behavior seems to be controlled by oxytocin (Kosfeld et al. 2005; Zak et al. 2007; Baumgartner et al. 2008). Therefore, we might find factors in common between these species, and investigation of behavioral mechanisms in marmosets could shed light on those of humans.

Notes

Acknowledgments

This study was performed in accordance with the ethical guidelines of the National Institute of Neuroscience, NCNP, under experimental license nos. 2005003 and 2008003 issued by the ethical committee for primate research of NCNP, and adhered to the legal requirements of Japan. This work was supported by the Japan Society for the Promotion of Science, no. 18-04743 (A.S.), CREST, the Japan Science and Technology Agency and a Research Grant (20B-10) for Nervous and Mental Disorders from the Ministry of Health, Labour and Welfare (K.N.).

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Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  1. 1.Department of Cognitive and Behavioral Science, Graduate School of Arts and SciencesThe University of TokyoTokyoJapan
  2. 2.JSPSTokyoJapan
  3. 3.National Institute of Neuroscience, NCNPKodairaJapan
  4. 4.CREST, JSTKawaguchiJapan
  5. 5.Section of Cognitive Neuroscience, Department of Behavioral and Brain Sciences, Primate Research InstituteKyoto UniversityInuyamaJapan

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