Mother–infant bonding and the evolution of mammalian social relationships

May combine two claims.

OT is a neuropeptide that plays a fundamental role in maternalism, acting centrally to promote maternal care and peripherally to promote parturition and milk let-down.

“OT is a neuropeptide that plays a fundamental role in maternalism, acting centrally to promote maternal care and peripherally to promote parturition and milk let-down (Keverne & Kendrick 1992; Kendrick 2000).”

• cites Keverne & Kendrick 1992Not checked yet

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• cites Kendrick 2000Not checked yet

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May combine two claims.

In monkeys and apes there has been a degree of emancipation from hormonal determinants of behaviour: maternal care occurs even without priming by pregnancy hormones, and much Old World primate sexual activity is non-reproductive and occurs outside periods of fertility.

“There has also been a degree of emancipation from hormonal determinants of behaviour; maternal care occurs even in the absence of priming by pregnancy hormones, and much of Old World primate sexual activity is non-reproductive occurring outside the periods of fertility.”

May combine two claims.

Females form strong social bonds with their infants, and female-female relationships are strongly affiliative, especially among matrilineal kin which often assist with infant care.

“Females therefore form strong social bonds with their infants and female–female relationships are also strongly affiliative, especially among matrilineal kin which often assist with infant care (Hrdy 1999).”

• cites Hrdy 1999Not checked yet

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May combine two claims.

Hormonal changes accompanying mating and parturition induce changes in expression of neuropeptides including β-endorphin, CRF, OT and AVP, which are thought to be critically important in mediating maternal and other social behaviours.

“The hormonal changes which accompany these events induce changes in the expression of a range of neuropeptides (e.g. β-endorphin, corticotrophin-releasing factor (CRF), oxytocin (OT) and arginine vasopressin (AVP)) that are thought to be critically important in the mediation of maternal and other social behaviours (Keverne & Curley 2004; Curley & Keverne 2005).”

• cites Keverne & Curley 2004Not checked yet

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• cites Curley & Keverne 2005Not checked yet

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May combine two claims.

With the evolutionary increase of neocortex in monkeys and apes, there has been a corresponding increase in the complexity of social relationships and bonding strategies together with significant redundancy in hormonal priming for motivated behaviour.

“With the evolutionary increase of neocortex seen in monkeys and apes, there has been a corresponding increase in the complexity of social relationships and bonding strategies together with a significant redundancy in hormonal priming for motivated behaviour.”

May combine two claims.

Trophoblast cells of the placenta produce steroids and hormonal peptides that regulate growth and development of the placenta and enter the maternal circulation to adapt maternal physiology, metabolism and behaviour.

“The cells of this lineage are responsible for the production of steroids and hormonal peptides which not only regulate growth and development of the placenta, but also enter the maternal circulation to adapt maternal physiology, metabolism and behaviour (Heap 1994).”

• cites Heap 1994Not checked yet

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May combine two claims.

In monkeys and apes, olfactory recognition and olfactory inputs to brain areas concerned with social reward are downregulated, and recognition is based on integration of multimodal sensory cues requiring an expanded neocortex, particularly the association cortex.

“Olfactory recognition and olfactory inputs to areas of the brain concerned with social reward are downregulated and recognition is based on integration of multimodal sensory cues requiring an expanded neocortex, particularly the association cortex.”

May combine two claims.

In a minority of mammals (less than 5%), ecological conditions make promiscuous male strategies disadvantageous, and males form a partner preference bond with females, defend them from intruders, and participate in parental care.

“In a minority of mammals (less than 5%) ecological conditions are such that promiscuous male strategies are disadvantageous, and here males form a partner preference (bond) with females, defend them from intruders, and participate in parental care (Kleiman 1977).”

• cites Kleiman 1977Not checked yet

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May combine two claims.

In the majority of small-brained mammals, including rodents, formation of a maternal or partner preference bond requires individual recognition by olfactory cues, activation of neural mechanisms concerned with social reward by these cues, and gender-specific hormonal priming for behavioural output.

“In the majority of small-brained mammals (including rodents), the formation of a maternal or partner preference bond requires individual recognition by olfactory cues, activation of neural mechanisms concerned with social reward by these cues and gender-specific hormonal priming for behavioural output.”

May combine two claims.

With cortical brain expansion in monkeys and apes, there has been an increase in the complexity of social relationships and a decreased dependency on olfactory communication.

“With the cortical brain expansion seen in monkeys and apes, there has been an increase in the complexity of social relationships and a decreased dependency on olfactory communication (Curley & Keverne 2005).”

• cites Curley & Keverne 2005Not checked yet

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May combine two claims.

The majority of mammals are small-brained, with a high ratio of limbic to cortical structures, and regulation of their social relationships requires individual recognition by olfactory cues.

“The majority of mammals are small-brained (i.e. they have a high ratio of limbic to cortical structures), with the regulation of social relationships requiring individual recognition by olfactory cues.”

Probably not a substantial claim: may not pass S3 (load-bearing), S4 (based). May combine two claims.

The majority of small-brained mammals such as rodents are altricial and produce relatively large numbers of offspring per litter that are deaf, blind and helpless at birth and severely deficient in motor control and temperature regulation.

“The majority of small-brained mammals such as rodents are altricial and produce relatively large numbers of offspring in each litter that are deaf, blind and helpless at birth, and severely deficient in motor control and temperature regulation.”

May combine two claims.

The hormones of pregnancy, under the control of the foetal placenta, inhibit sexual behaviour, promote feeding behaviour, develop the mammary glands and prime the brain for maternal care, which is then triggered by parturition.

“The hormones of pregnancy, under the control of the foetal placenta, inhibit sexual behaviour, promote feeding behaviour, develop the mammary glands and prime the brain for maternal care (figure 1), which is then triggered by parturition (Keverne 2005).”

• cites Keverne 2005Not checked yet

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May combine two claims.

Formation of social relationships requires familiarity, which for kin is brought about by prolonged contact involving licking and grooming.

“The formation of these relationships requires familiarity, which for kin is brought about by prolonged contact involving licking and grooming.”

May combine two claims.

The medial amygdala is important for social recognition in mice, and infusions of OT into the medial amygdala of mice with a targeted deletion of the OT gene restore olfactory social recognition.

“The medial amygdala is also important for social recognition in mice, and infusions of OT into the medial amygdala of mice with a targeted deletion of the OT gene restores olfactory social recognition (Ferguson et al. 2000, 2001).”

• cites Ferguson et al. 2000, 2001Not checked yet

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May combine two claims.

To select against milk stealing, maternal care in ungulates becomes exclusive within 1-2 h of parturition, and strange non-related young that try to suckle are violently rejected.

“To select against this, maternal care becomes exclusive within 1–2 h of parturition, and any strange non-related young that try to suckle are violently rejected.”

May combine two claims.

Although the olfactory bulb has no oxytocinergic terminals, it has an abundance of OT receptors.

“Although the OB has no oxytocinergic terminals there is an abundance of OT receptors.”

Probably not a substantial claim: may not pass S4 (based).

Grazing mammals such as ungulates live in relatively large social groups that are constantly on the move in search of food.

“Grazing mammals, such as ungulates, live in relatively large social groups that are constantly on the move in search of food.”

Probably not a substantial claim: may not pass S3 (load-bearing), S4 (based). May combine two claims.

Most ungulate mothers are seasonal breeders, producing synchronized births with only one or two offspring in any one year.

“Most ungulate mothers are seasonal breeders, producing synchronized births with only one or two offspring in any one year.”

May combine two claims.

In altricial rodents, removal of individual offspring produces no obvious signs of behavioural loss, and even removing the whole litter results in the female returning to oestrus within a few days, followed rapidly by mating and further pregnancy.

“Indeed, the removal of individuals produces no obvious signs of behavioural loss, and even removing the whole litter results in the female returning to oestrus within a few days, following which mating and a further pregnancy rapidly ensue.”

May combine two claims.

The neural mechanisms that serve selective bonding in sheep require a maternal motivational state dependent on the hormones of pregnancy and a recognition memory primarily dependent on olfactory cues.

“The neural mechanisms that serve this selective bonding require a maternal motivational state, which is dependent on the hormones of pregnancy, and a recognition memory, which is primarily dependent on olfactory cues.”

May combine two claims.

Most altricial mammals produce large litters and fail to distinguish between individual offspring.

“Most altricial mammals produce large litters and fail to distinguish between individual offspring.”

May combine two claims.

Ungulate young are born precocial, capable of maintaining their own body temperature and able to stand and walk soon after birth.

“The young are born precocial, capable of maintaining their own body temperature and able to stand and walk soon after birth.”

May combine two claims.

The amygdala has reciprocal connections with the nucleus accumbens, and both structures show enhanced neural activation in rodents following exposure to biologically significant odours.

“The amygdala has reciprocal connections with the NAcc, and both structures show enhanced levels of neural activation in rodents following exposure to biologically significant odours (Moncho-Bogani et al. 2005).”

• cites Moncho-Bogani et al. 2005Not checked yet

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May combine two claims.

Male partners generally do not stay attached after mating, and because mother-offspring interaction depends closely on maternal hormones, the mother-infant bond is restricted until weaning.

“Male partners generally do not stay attached after mating, and owing to the close dependence of mother–offspring interaction on the maternal hormones, the mother–infant bond is restricted until weaning.”

May combine two claims.

OT synthesized in hypothalamic neurons is released into the brain at birth, facilitating olfactory recognition of offspring, aiding parturition and stimulating the onset of maternal care.

“OT, synthesized in the hypothalamic neurons, is released into the brain at birth, facilitating olfactory recognition of offspring (Keverne et al. 1993), aiding parturition (Neumann et al. 1996) and stimulating the onset of maternal care (Keverne et al. 1993).”

• cites Keverne et al. 1993Not checked yet

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• cites Neumann et al. 1996Not checked yet

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May combine two claims.

In mate recognition by the female, formation of the familiar relationship requires sexual activity, which can only occur when the female is in oestrus.

“In the context of mate recognition by the female, the formation of this familiar relationship requires sexual activity, which can only occur when the female is in oestrus.”

May combine two claims.

OT receptors are particularly notable in both the shell and core of the nucleus accumbens, and lesions to these areas impair maternal retrieval and prevent the rewarding experience of maternal care from being carried forward to subsequent mother-pup interactions.

“OT receptors are particularly notable in both the shell and the core of the NAcc, and lesions to these areas have shown that maternal retrieval is impaired and the rewarding experience of maternal care is not carried forward to subsequent mother–pup interactions (Lee et al. 1999; Numan et al. 2005).”

• cites Lee et al. 1999Not checked yet

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• cites Numan et al. 2005Not checked yet

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May combine two claims.

OT infusion directly into the olfactory bulb enhances maternal care and increases the frequency and amplitude of spontaneous excitatory post-synaptic currents of granule cells by both pre- and postsynaptic mechanisms, a process integral to olfactory recognition memory.

“OT infusion directly into the OB enhances maternal care and increases both the frequency and the amplitude of spontaneous excitatory post-synaptic currents of granule cells (Yu et al. 1996b) by both pre- and postsynaptic mechanisms, a process integral to olfactory recognition memory (Dluzen et al. 1998, 2000; Engelmann et al. 1998; Osako et al. 2001).”

• cites Yu et al. 1996bNot checked yet

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• cites Dluzen et al. 1998, 2000Not checked yet

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• cites Engelmann et al. 1998Not checked yet

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May combine two claims.

Small-brained female rodents form bonded social relationships with their offspring and with mates, both regulated by odour cues and both short-lived.

“Thus, small-brained female rodents do form bonded social relationships with their offspring and with mates, both of which are regulated by odour cues and both of which are short-lived.”

May combine two claims.

Oestrogen acts through oestrogen receptors ERα and ERβ; ERβ is expressed in hypothalamic neurons that synthesize OT, whereas ERα is required for synthesis of OT receptors in the amygdala.

“Oestrogen acts through the oestrogen receptors ERα and ERβ; ERβ is expressed in the hypothalamic neurons that synthesize OT, whereas ERα is required for synthesis of OT receptors in the amygdala (Patisaul et al. 2003).”

• cites Patisaul et al. 2003Not checked yet

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May combine two claims.

OT release is significant in overcoming neophobia, since OT knockout mice exhibit altered levels of anxiety and intracerebroventricular administration of oxytocin receptor antagonists increases anxiety in female rats.

“OT release is significant in this context too, since it is noteworthy that OT knockout mice exhibit altered levels of anxiety (Mantella et al. 2003; Amico et al. 2004) and intracerebroventricular (icv) administration of oxytocin receptor antagonists increases anxiety in female rats (Neumann et al. 2000).”

• cites Mantella et al. 2003Not checked yet

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• cites Amico et al. 2004Not checked yet

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• cites Neumann et al. 2000Not checked yet

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May combine two claims.

OT release during key life events facilitates social interactions and is required for formation of the olfactory memory that enables social recognition of conspecifics.

“OT release during other key life events similarly facilitates social interactions and is required for the formation of the olfactory memory that enables the social recognition of conspecifics (Dluzen et al. 2000; Ferguson et al. 2000, 2001; Winslow & Insel 2002).”

• cites Dluzen et al. 2000Not checked yet

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• cites Ferguson et al. 2000, 2001Not checked yet

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• cites Winslow & Insel 2002Not checked yet

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May combine two claims.

Primates and other mammals share opioid involvement in maternal care, but the consequences of opioid blockade in small-brained mammals are much greater for the biological aspects of maternal behaviour.

“Primates and other mammals have in common opioid involvement in maternal care, but the consequences of opioid blockade in small-brained mammals are much greater for the biological aspects of maternal behaviour.”

May combine two claims.

The infant is not rejected from suckling, but the mother's usual possessive preoccupation with the infant declines with opioid receptor blockade.

“The infant is not rejected from suckling, but a mother's usual possessive preoccupation with the infant declines with opioid receptor blockade.”

• cites Martel et al. 1993, 1995Not checked yet

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• cites Keverne et al. 1997Not checked yet

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May combine two claims.

Naloxone-treated mothers permit other females to groom their infants, while saline-treated control females are very possessive and protective of their infants from contact with others at this stage.

“Moreover, they permit other females to groom their infants, while saline-treated control females are very possessive and protective of their infants from contact with others at this stage.”

• cites Martel et al. 1993, 1995Not checked yet

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• cites Keverne et al. 1997Not checked yet

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May combine two claims.

Delivery of lambs under peridural anaesthesia blocks central OT release and inhibits maternal behaviour, while subsequent intracerebral infusions of OT restore this behaviour.

“The importance of parturition for the induction of maternal behaviour cannot be emphasized enough, since delivery of lambs under peridural anaesthesia blocks central OT release and inhibits maternal behaviour, while subsequent intracerebral infusions of OT restore this behaviour (Krehbiel et al. 1987; Levy et al. 1992).”

• cites Krehbiel et al. 1987Not checked yet

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• cites Levy et al. 1992Not checked yet

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May combine two claims.

In sheep, OT receptors in the medial amygdala increase at parturition, and intracerebroventricular infusions of OT induce full maternal behaviour and bonding in non-gestant ewes.

“In sheep, OT receptors in the medial amygdala increase at parturition (Broad et al. 1999) and icv infusions of OT induce full maternal behaviour and bonding in non-gestant ewes (Kendrick et al. 1987).”

• cites Broad et al. 1999Not checked yet

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• cites Kendrick et al. 1987Not checked yet

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May combine two claims.

The olfactory recognition process in sheep serves to reject strange lambs, since anosmic ewes are fully maternal both to their own and to strange lambs.

“Although the olfactory recognition process is complex, its function serves to reject strange lambs, since anosmic ewes are fully maternal both to their own and to strange lambs (Baldwin & Shillito 1974; Levy et al. 1995a,b).”

• cites Baldwin & Shillito 1974Not checked yet

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• cites Levy et al. 1995a,bNot checked yet

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May combine two claims.

Disruption of the medial amygdala by lidocaine infusions does not impair bonding and proactive behaviour to the ewe's own lamb, but it does impair expression of rejection behaviour to strange lambs.

“Disruption of the medial amygdala by lidocaine infusions does not impair bonding and proactive behaviour to the ewe's own lamb, but it does impair the expression of rejection behaviour to strange lambs (Keller et al. 2004a,b).”

• cites Keller et al. 2004a,bNot checked yet

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May combine two claims.

In primates, the OT system may also be important in bonding, and in humans peripheral OT release is increased at birth, following female orgasm and exposure to neonatal images or sounds.

“In primates, the OT system may also be important in bonding, and in humans peripheral OT release is increased at birth, following female orgasm and exposure to neonatal images or sounds (McNeilly et al. 1983; Carmichael et al. 1987).”

• cites McNeilly et al. 1983Not checked yet

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• cites Carmichael et al. 1987Not checked yet

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Probably not a substantial claim: may not pass S4 (based).

In Old World monkeys, apes and humans, the hormones of pregnancy, parturition and lactation are not necessary for maternal or alloparental care, as females can be motherly towards infants even without ever being pregnant.

“In Old World monkeys, apes and humans, the hormones of pregnancy, parturition and lactation are not necessary for maternal or alloparental care, as females of these species can be motherly towards infants even without ever being pregnant.”

May combine two claims.

There are crucial differences between sheep and small-brained mammals, particularly in the selectivity of the recognition process and how it activates rejection behaviour toward strange lambs.

“However, there are also crucial differences, particularly in the selectivity of the recognition process and how this, in the presence of strange lambs, is able to activate rejection behaviour.”

May combine two claims.

Induction of maternal behaviour in non-pregnant ewes can be established by hormonal priming with oestrogen and progesterone followed by vaginal stimulation, which also induces central OT release.

“Moreover, induction of maternal behaviour in non-pregnant ewes can be established by hormonal priming with oestrogen and progesterone followed by vaginal stimulation, which also induces central OT release. (Keverne et al. 1983; Kendrick et al. 1988)”

• cites Keverne et al. 1983Not checked yet

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• cites Kendrick et al. 1988Not checked yet

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May combine two claims.

The medial prefrontal cortex is particularly important in sheep because, in contrast to small-brained rodents, this heterogeneous region is unusually large and is recognized from primate studies to modulate integrative, attentional and emotional responses that allow emancipation of behaviours from stimulus-response modes and hormonal control.

“The medial prefrontal cortex (mPFC) is particularly important since, in contrast to small-brained rodents, this heterogeneous region is unusually large in the sheep and is recognized from primate studies to play an important role in modulating integrative, attentional and emotional responses which allow the emancipation of behaviours from stimulus response modes and hormonal control.”

May combine two claims.

In sheep, interference with the endogenous opioid system severely impairs maternal behaviour, including suckling, whereas monkeys neglect to show a focused preoccupation with infant care but still permit suckling.

“In sheep, interference with the endogenous opioid system severely impairs maternal behaviour, including suckling, whereas monkeys neglect to show a focused preoccupation with infant care but still permit suckling (Kendrick & Keverne 1989; Martel et al. 1993).”

• cites Kendrick & Keverne 1989Not checked yet

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• cites Martel et al. 1993Not checked yet

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May combine two claims.

Extensive plastic changes occur in the olfactory bulb as a consequence of parturition, and further changes are consequent on lamb exposure and memory formation.

“These studies have further demonstrated that there are extensive plastic changes that occur in the OB as a consequence of parturition, and further changes are consequent on lamb exposure and memory formation (Kendrick et al. 1992, 1997; Keverne et al. 1993; Levy et al. 1995a,b).”

• cites Kendrick et al. 1992, 1997Not checked yet

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• cites Keverne et al. 1993Not checked yet

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• cites Levy et al. 1995a,bNot checked yet

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May combine two claims.

Lesioning the main olfactory system at the level of receptor neurons or at the first neural relay prevents selective recognition but does not impair proactive behaviour associated with maternal care.

“Lesioning of this main olfactory system at the level of receptor neurons or at the first neural relay prevents selective recognition but notably does not impair the proactive behaviour associated with maternal care (Baldwin & Shillito 1974; Levy et al. 1995a,b).”

• cites Baldwin & Shillito 1974Not checked yet

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• cites Levy et al. 1995a,bNot checked yet

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May combine two claims.

During the first weeks of life when infant retrieval is normally very high, naloxone-treated mothers neglect their infants and show little retrieval even when the infant moves a distance away.

“During the first weeks of life when infant retrieval is normally very high, naloxone-treated mothers neglect their infants and show little retrieval even when the infant moves a distance away.”

• cites Martel et al. 1993, 1995Not checked yet

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• cites Keverne et al. 1997Not checked yet

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May combine two claims.

By 1 year of age nearly 50% of children of heroin-addicted women are living away from their biological mothers, and by school age only 12% remain with their biological mothers.

“Nevertheless, the facts are that by 1 year of age nearly 50% of children are living away from their biological mothers, and by school age only 12% remain with their biological mothers (Mayes 1995).”

• cites Mayes 1995Not checked yet

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May combine two claims.

The ventral striatum is involved in reward and also requires the mesolimbic dopamine projection, which detects rewarding stimuli and the ways in which they occur differently from prediction to enable updating of the stimulus.

“This area of the brain is involved in ‘reward’ and also requires the mesolimbic DA projection which detects rewarding stimuli and the ways in which they occur differently from prediction to enable ‘updating’ of the stimulus (Schultz & Dickinson 2000).”

• cites Schultz & Dickinson 2000Not checked yet

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May combine two claims.

During parturition, levels of OT in cerebrospinal fluid increase to 400 pg ml−1 and reach all areas of the brain including the olfactory bulb, where receptors are upregulated during pregnancy.

“Certainly, during parturition, levels of OT in cerebrospinal fluid (CSF) increase to 400 pg ml−1 and reach all areas of the brain including the OB, where receptors are upregulated during pregnancy (da Costa et al. 1996).”

• cites da Costa et al. 1996Not checked yet

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May combine two claims.

Electrophysiological studies of the olfactory bulb have shown changes in the response of mitral cells to lamb odours, and in vivo microdialysis studies have reported altered neurotransmitter release causally linked to the olfactory memory formation underlying selective recognition.

“Electrophysiological studies of the OB have shown changes to occur in the response of mitral cells to lamb odours, while in vivo microdialysis studies have reported altered neurotransmitter release that is causally linked to the olfactory memory formation underlying selective recognition.”

• cites Kendrick et al. 1992, 1997Not checked yet

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• cites Keverne et al. 1993Not checked yet

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• cites Levy et al. 1995a,bNot checked yet

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May combine two claims.

The accessory olfactory system contains the vomeronasal organ (VNO) enclosed in a cartilaginous capsule on the medial surface of the nasal septum, from which neurons convey non-volatile odour (pheromones) signals directly to the brain's hypothalamic and limbic systems.

“The accessory system contains the vomeronasal organ (VNO) enclosed in a cartilaginous capsule on the medial surface of the nasal septum, from which neurons convey non-volatile odour (pheromones) signals directly to the brain's hypothalamic and limbic systems (Keverne 1999).”

• cites Keverne 1999Not checked yet

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Probably not a substantial claim: may not pass S3 (load-bearing), S4 (based). May combine two claims.

This licking is an important component of rat maternal behaviours and is thought to be involved in maternal bonding and promotes pup survival.

“This licking is an important component of rat maternal behaviours and is thought to be involved in maternal bonding and promotes pup survival.”

May combine two claims.

Males with the Trp2c mutation fail to show sexual preferences for females and readily mate with other males.

“Males with this mutation fail to show sexual preferences for females and readily mate with other males (Stowers et al. 2002).”

• cites Stowers et al. 2002Not checked yet

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May combine two claims.

There is evidence that cerebrospinal fluid levels of OT are elevated in OCD, and this peptide also plays a fundamental role in many obsessive aspects of maternalism.

“There is also evidence that CSF levels of the neuropeptide, OT are elevated in OCD, and this peptide also plays a fundamental role in many obsessive aspects of maternalism (Leckman et al. 1994).”

• cites Leckman et al. 1994Not checked yet

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May combine two claims.

Updating of infant recognition involves visual cues and prefrontal-ventral striatal pathways that are also intimately linked to the emotional brain via the amygdala.

“This updating of infant recognition involves visual cues and prefrontal–ventral striatal pathways which are also intimately linked to the emotional brain via the amygdala.”

May combine two claims.

Mice selectively lacking heterotrimeric G-proteins of the Gq family (transduction proteins) in vomeronasal receptors do not display any maternal behaviour despite having normal levels of OT and prolactin, and exhibiting normal lactation.

“Moreover, mice selectively lacking heterotrimeric G-proteins of the Gq family (transduction proteins) in vomeronasal receptors do not display any maternal behaviour despite having normal levels of OT and prolactin, and exhibiting normal lactation.”

• cites Wettschureck et al. 2004Not checked yet

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Probably not a substantial claim: may not pass S4 (based). May combine two claims.

The mother-infant bonding process entails obsessive grooming, especially to hands, face and genitalia, by mothers, and these are the morphological traits of infant monkeys that show the greatest changes during development.

“The mother–infant bonding process entails obsessive grooming, especially to hands, face and genitalia, by mothers, and these are the morphological traits of infant monkeys that show the greatest changes during development.”

May combine two claims.

Unlike lesions to the main olfactory system, lesions of the vomeronasal system do not prevent rodents from distinguishing biologically salient differences in odour; however, they do prevent them from employing the salience of these cues to demonstrate a preference.

“Interestingly, unlike lesions to the main olfactory system, lesions of the vomeronasal system do not prevent rodents from distinguishing biologically salient differences in odour; however, they do prevent them from employing the salience of these cues to demonstrate a preference (Pankevich et al. 2004).”

• cites Pankevich et al. 2004Not checked yet

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May combine two claims.

The Trp2c gene encodes a cation channel that enables vomeronasal neurons to generate action potentials, but has become a non-functional pseudogene in primates, as indeed have genes that code for vomeronasal receptors.

“This gene encodes a cation channel that enables vomeronasal neurons to generate action potentials, but has become a non-functional pseudogene in primates, as indeed have genes that code for vomeronasal receptors (Grus et al. 2005; Young et al. 2005).”

• cites Grus et al. 2005Not checked yet

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• cites Young et al. 2005Not checked yet

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May combine two claims.

Components of human behaviour in the post-partum maternal period are influenced by hormones, but they relate to brain areas concerned with reward and not with the direct execution of maternal behaviour per se.

“Hence, there are components of human behaviour that occur in the post-partum maternal period which are influenced by hormones, but interestingly they relate to areas of the brain concerned with reward and not with the direct execution of maternal behaviour per se.”

• cites Williams & Koran 1997Not checked yet

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• cites Labad et al. 2005Not checked yet

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May combine two claims.

The pheromone to which the mother rat's VNO responds is dodecyl propionate, which originates in the pup's preputial gland and stimulates licking of the anogenital region.

“The pheromone to which the mother rat's VNO responds is dodecyl propionate, which originates in the pup's preputial gland and stimulates licking of the anogenital region (Brouette-Lahlou et al. 1999).”

• cites Brouette-Lahlou et al. 1999Not checked yet

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May combine two claims.

The main olfactory system of small-brained mammals (rodents) has over 1200 olfactory receptor genes, the largest mammalian gene family, and incredible sensitivity brought about by a 1000 : 1 convergence of each receptor neuron at the first relay.

“The main olfactory system of small-brained mammals (rodents) has over 1200 olfactory receptor genes, the largest mammalian gene family (Zhang & Firestein 2002), and incredible sensitivity brought about by a 1000 : 1 convergence of each receptor neuron at the first relay (Hellman & Chess 2002).”

• cites Zhang & Firestein 2002Not checked yet

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• cites Hellman & Chess 2002Not checked yet

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May combine two claims.

Through the accessory chemosensory system, pheromone signals are able to change endocrine states (e.g. advance the onset of oestrus) and regulate parental and sexual behaviour.

“Through this chemosensory system, pheromone signals are able to change endocrine states (e.g. advance the onset of oestrus) and regulate parental and sexual behaviour (Brennan & Keverne 2004).”

• cites Brennan & Keverne 2004Not checked yet

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May combine two claims.

Human mothers experience preoccupations and rituals in the context of maternal care, and even before the birth of their baby they are obsessive with cleaning and creating a safe environment.

“Human mothers also experience preoccupations and rituals in the context of maternal care, and even before the birth of their baby they are obsessive with cleaning and creating a safe environment.”

• cites Leckman et al. 1999Not checked yet

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May combine two claims.

Biological odours are rarely simple and the spatial and temporal patterns that can be generated at the first relay have the coding capacity to distinguish individuals in the social group.

“Biological odours are rarely simple and the spatial and temporal patterns that can be generated at this first relay have the coding capacity to distinguish individuals in the social group.”

May combine two claims.

After birth, safety is the major concern and mothers frequently check on their baby even at times when they know the baby is fine.

“After birth, safety is the major concern and mothers frequently check on their baby even at times when they know the baby is fine (Leckman et al. 1999).”

• cites Leckman et al. 1999Not checked yet

  Not checked in the free run.

May combine two claims.

Nursery reared rhesus monkeys deprived of a maternal upbringing demonstrate reduced OT secretion and social behaviours, but show increased aggressive and stereotypical behaviours.

“Nursery reared rhesus monkeys deprived of a maternal upbringing demonstrate reduced OT secretion and social behaviours, but show increased aggressive and stereotypical behaviours.”

• cites Winslow et al. 2003Not checked yet

  Not checked in the free run.

May combine two claims.

In primates, post-partum maternal care also extended mother-infant bonding beyond the period of suckling, thereby increasing selection for visual recognition of offspring when infant mobility required facial recognition at a distance.

“In primates, post-partum maternal care also extended mother–infant bonding beyond the period of suckling, thereby increasing selection for visual recognition of offspring when infant mobility required facial recognition at a distance.”

May combine two claims.

It seems likely that the primary action of the local anaesthetic under these circumstances is to cause a shutdown of neuronal activity in the mPFC which promotes local large increases in inhibitory transmitter concentrations (notably GABA and 5-HT).

“It seems likely that the primary action of the local anaesthetic under these circumstances is to cause a shutdown of neuronal activity in the mPFC which promotes local large increases in inhibitory transmitter concentrations (notably GABA and 5-HT).”

Probably not a substantial claim: may not pass S3 (load-bearing).

Choosing between actions associated with uncertain rewards and punishments in humans is mediated by neural circuitry involving frontal cortex, anterior cingulate and striatum.

“Choosing between actions associated with uncertain rewards and punishments in humans is mediated by neural circuitry involving frontal cortex, anterior cingulate and striatum (Rogers et al. 2004).”

• cites Rogers et al. 2004Not checked yet

  Not checked in the free run.

Probably not a substantial claim: may not pass S3 (load-bearing).

The detection of unfavourable outcomes, response conflict and decision uncertainty elicit overlapping clusters of activation foci in the mPFC.

“Interestingly, the detection of unfavourable outcomes, response conflict and decision uncertainty elicit overlapping clusters of activation foci in the mPFC (Ridderinkhof et al. 2004).”

• cites Ridderinkhof et al. 2004Not checked yet

  Not checked in the free run.

May combine two claims.

The recognition component in this bonding process requires the medial amygdala for bonding to occur, but is not necessary for retrieval of the recognition memory required to reject strange lambs, while the mPFC is necessary for selective rejection but not required for recognition memory of own lamb.

“The recognition component in this bonding process requires the medial amygdala for bonding to occur (Keller et al. 2004b), but is not necessary for retrieval of the recognition memory required to reject strange lambs, while the mPFC is necessary for selective rejection but not required for recognition memory of own lamb (Broad et al. 2002a,b; Keller et al. 2004a,b).”

• cites Keller et al. 2004bNot checked yet

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• cites Broad et al. 2002a,bNot checked yet

  Not checked in the free run.

• cites Keller et al. 2004a,bNot checked yet

  Not checked in the free run.

May combine two claims.

While the mother's brain has been 'maternalized' by the hormones of pregnancy generated by the foetal extra-embryonic placenta, the infant's developing brain requires social stimulation from a mother committed to providing the emotional rewards of suckling, huddling and grooming.

“While the mother's brain has been ‘maternalized’ by the hormones of pregnancy generated by the foetal extra-embryonic placenta, the infant's developing brain requires social stimulation from a mother committed to providing the emotional rewards of suckling, huddling and grooming.”

Probably not a substantial claim: may not pass S3 (load-bearing).

This executive function is believed to facilitate the matching of an appropriate behavioural strategy to rapid changes in task requirements.

“This executive function is believed to facilitate the matching of an appropriate behavioural strategy to rapid changes in task requirements (Bechara et al. 1994, 1996, 2000; Ragozzino et al. 1999a,b).”

• cites Bechara et al. 1994, 1996, 2000Not checked yet

  Not checked in the free run.

• cites Ragozzino et al. 1999a,bNot checked yet

  Not checked in the free run.

May combine two claims.

Following the withdrawal of tetracaine, maternal selectivity returns, showing the olfactory recognition memory to be intact.

“However, following the withdrawal of tetracaine, maternal selectivity returns, showing the olfactory recognition memory to be intact.”

• cites Broad et al. 2002a,bNot checked yet

  Not checked in the free run.

Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

Increased stereotypical behaviours are often classically associated with the disruption of frontal cortical function and often result from an inability to suppress inappropriate behavioural responses.

“Increased stereotypical behaviours are often classically associated with the disruption of frontal cortical function and often result from an inability to suppress inappropriate behavioural responses (Winslow et al. 2003).”

• cites Winslow et al. 2003Not checked yet

  Not checked in the free run.

Probably not a substantial claim: may not pass S3 (load-bearing).

Electrophysiological recordings from normal adult monkeys have shown that the mPFC mediates the achievement of goals.

“Electrophysiological recordings from normal adult monkeys have shown that the mPFC mediates the achievement of goals (Matsumoto & Tanaka 2004).”

• cites Matsumoto & Tanaka 2004Not checked yet

  Not checked in the free run.

May combine two claims.

Arguably, the most significant visual change in Old World primates was the evolution of trichromacy, which occurred at approximately the same time as the pseudogenization of the Old World primate chemosensory genome, allowing individuals to interpret social information such as colourful sexual adornments.

“Arguably, the most significant visual change in Old World primates was the evolution of trichromacy (Surridge et al. 2003), which occurred at approximately the same time as the pseudogenization of the Old World primate chemosensory genome (Gilad et al. 2004; Webb et al. 2004), allowing individuals to interpret social information such as colourful sexual adornments.”

• cites Surridge et al. 2003Not checked yet

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• cites Gilad et al. 2004Not checked yet

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• cites Webb et al. 2004Not checked yet

  Not checked in the free run.

May combine two claims.

Tetracaine has effects similar to localized cooling on inhibiting membrane conductance and therefore it is probable that behavioural and neurochemical actions observed with tetracaine infusions result from inhibition of these mPFC neurons disabling their communication with the ventral striatum.

“Tetracaine has effects similar to localized cooling on inhibiting membrane conductance (Luzzati et al. 1999) and therefore it is probable that behavioural and neurochemical actions observed with tetracaine infusions result from inhibition of these mPFC neurons disabling their communication with the ventral striatum.”

• cites Luzzati et al. 1999Not checked yet

  Not checked in the free run.

May combine two claims.

In addition to increasing OT synthesis and OT receptor synthesis in the brain, the hormones of pregnancy also induce pro-opiomelanocortin (POMC) and PPE synthesis in the hypothalamus of sheep and the release of opioids into CSF at parturition.

“In addition to increasing OT synthesis and OT receptor synthesis in the brain, the hormones of pregnancy also induce pro-opiomelanocortin (POMC) and PPE synthesis in the hypothalamus of sheep (Broad et al. 1993a,b) and the release of opioids into CSF at parturition (Wardlaw & Frantz 1983).”

• cites Broad et al. 1993a,bNot checked yet

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• cites Wardlaw & Frantz 1983Not checked yet

  Not checked in the free run.

May combine two claims.

In small-brained rodents, the mPFC matures around day 13-15 post-partum while in the human, this development continues late into adolescence (years 17-21).

“In small-brained rodents, the mPFC matures around day 13–15 post-partum (Diergaarde et al. 2005) while in the human, this development continues late into adolescence (years 17–21; Sowell et al. 2001).”

• cites Diergaarde et al. 2005Not checked yet

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• cites Sowell et al. 2001Not checked yet

  Not checked in the free run.

May combine two claims.

Squirrel monkeys, 4 years after experiencing separations from their mother early during development, generate differences in emotional behaviour, stress physiology and development of the brain, notably in the mPFC.

“Squirrel monkeys, 4 years after experiencing separations from their mother early during development, generate differences in emotional behaviour, stress physiology and development of the brain, notably in the mPFC.”

• cites Lyons & Schatzberg 2003Not checked yet

  Not checked in the free run.

Probably not a substantial claim: may not pass S3 (load-bearing).

Such a response has much in common with the post-partum aggression of rodents initiated by the odour of strange intruders.

“Such a response has much in common with the post-partum aggression of rodents initiated by the odour of strange intruders.”

May combine two claims.

Moreover, inactivating the mPFC does not prevent memory retrieval for generating emotional vocal responses, but prevents the ewe downloading the information necessary for initiating an aggressive motor response via the striatum.

“Moreover, inactivating the mPFC does not prevent memory retrieval for generating emotional vocal responses, but prevents the ewe downloading the information necessary for initiating an aggressive motor response via the striatum (Broad et al. 2002a,b).”

• cites Broad et al. 2002a,bNot checked yet

  Not checked in the free run.

May combine two claims.

In sheep, reversible inactivation of the medial frontal cortex (medial limbic area) using tetracaine infusions is not required for the performance of proactive maternal behaviour or for own lamb recognition.

“However, in sheep, reversible inactivation of the medial frontal cortex (medial limbic area) using tetracaine infusions is not required for the performance of proactive maternal behaviour or for own lamb recognition.”

• cites Broad et al. 2002a,bNot checked yet

  Not checked in the free run.

May combine two claims.

It is clear that the process of infant socialization benefits from this close relationship and, because this occurs during early brain development, mother-infant separations are likely to have long-term consequences.

“It is clear that the process of infant socialization benefits from this close relationship and, because this occurs during early brain development, mother–infant separations are likely to have long-term consequences (Hinde et al. 1978).”

• cites Hinde et al. 1978Not checked yet

  Not checked in the free run.

May combine two claims.

Neither of these areas, when inactivated, impairs maternal behaviour, but they do impair the selective nature of the bond.

“Neither of these areas, when inactivated, impairs maternal behaviour, but they do impair the selective nature of the bond.”

May combine two claims.

In the rat, the mPFC mainly receives a strong olfactory input via the mediodorsal thalamic nucleus, and lesions to this system decrease the frequency with which the mother protects her pups by attacking intruders who threaten to cannibalize her infants.

“In the rat, this area of the cortex mainly receives a strong olfactory input via the mediodorsal thalamic nucleus, and lesions to this system decrease the frequency with which the mother protects her pups by attacking intruders who threaten to cannibalize her infants (Ferreira et al. 1987).”

• cites Ferreira et al. 1987Not checked yet

  Not checked in the free run.

May combine two claims.

Here offspring are mobile within hours of birth and are likely to attempt cross-fostering; therefore mothers need to be selective in their bonding to ensure only their own offspring receives milk.

“Here offspring are mobile within hours of birth and are likely to attempt cross-fostering; therefore mothers need to be selective in their bonding to ensure only their own offspring receives milk.”

Classified as probably not a substantial claim. May combine two claims.

In monogamous species, the term bonding embraces father-infant, mother-father as well as mother-infant, while in large-brained primates it extends beyond the mother-infant to include social cohort, usually of kin related through the matriline.

“Hence, in monogamous species, this terminology embraces father–infant, mother–father as well as mother–infant, while in large-brained primates it extends beyond the mother–infant to include social cohort, usually of kin related through the matriline.”

Probably not a substantial claim: may not pass S3 (load-bearing), S4 (based). May combine two claims.

The olfactory system is deconstructed at the genetic level with total redundancy of the vomeronasal genome and substantial silencing of main olfactory receptor genes.

“The olfactory system is deconstructed at the genetic level with total redundancy of the vomeronasal genome and substantial silencing of main olfactory receptor genes.”

Probably not a substantial claim: may not pass S3 (load-bearing), S4 (based).

However, the way in which these mechanisms are deployed and their relative importance are dependent on the species and in particular on the evolution of the brain.

“However, the way in which these mechanisms are deployed and their relative importance are dependent on the species and in particular on the evolution of the brain.”

May combine two claims.

This area is activated specifically when subjects are asked to form an impression of a person but not when they are asked to form an impression of an inanimate object, suggesting that this region specifically indexes social cognition.

“This area is activated specifically when subjects are asked to form an impression of a person but not when they are asked to form an impression of an inanimate object, suggesting that this region specifically indexes social cognition (Mitchell et al. 2005).”

• cites Mitchell et al. 2005Not checked yet

  Not checked in the free run.

Probably not a substantial claim: may not pass S3 (load-bearing), S4 (based).

With enhanced brain evolution, trichromatic vision in primates has been the dominant sensory system for infant recognition.

“With enhanced brain evolution, trichromatic vision in primates has been the dominant sensory system for infant recognition.”

May combine two claims.

Common to all bonding relationships are hormonal mechanisms, brain reward mechanisms and sensory recognition.

“Common to all bonding relationships are hormonal mechanisms, brain reward mechanisms and sensory recognition (Curley & Keverne 2005).”

• cites Curley & Keverne 2005Not checked yet

  Not checked in the free run.

May combine two claims.

They are lifetime occupations for many primate species, a development that has, in turn, impacted significantly on brain evolution.

“Indeed, they are lifetime occupations for many primate species, a development that has, in turn, impacted significantly on brain evolution.”

May combine two claims.

These distinctions required face recognition and emotional processing which correlated with activation in the visual cortex, temporal pole and amygdala.

“These distinctions required face recognition and emotional processing which correlated with activation in the visual cortex, temporal pole and amygdala (Ranote et al. 2004).”

• cites Ranote et al. 2004Not checked yet

  Not checked in the free run.

May combine two claims.

Moreover, postponing most of cortical brain growth to the post-partum period has also ensured that the brain develops in a social environment which promotes social skills as well as provides experience in alloparenting.

“Moreover, postponing most of cortical brain growth to the post-partum period has also ensured that the brain develops in a social environment which promotes social skills as well as provides experience in alloparenting.”

Probably not a substantial claim: may not pass S4 (based).

Even more significant is the provision of an attachment figure, usually that of the mother, which provides the secure base from which to explore and develop other social relationships.

“Even more significant is the provision of an attachment figure, usually that of the mother, which provides the secure base from which to explore and develop other social relationships.”

May combine two claims.

The interbirth interval is relatively short and the elements of the olfactory recognition memory are carried forward to subsequent births and result in reduced cannibalism.

“The interbirth interval is relatively short and the elements of the olfactory recognition memory are carried forward to subsequent births and result in reduced cannibalism.”

Probably not a substantial claim: may not pass S4 (based).

The evolution of viviparity and the birth of live offspring as opposed to egg production have required consolidation of the mother's in utero investment, resulting in extended post-natal care.

“The evolution of viviparity and the birth of live offspring as opposed to egg production have required consolidation of the mother's in utero investment, resulting in extended post-natal care.”

May combine two claims.

Although recognition is common to all bonded relationships, in nocturnal small-brained altricial mammals this is primarily dependent on olfaction.

“Thus, although recognition is common to all bonded relationships, in nocturnal small-brained altricial mammals this is primarily dependent on olfaction.”

Probably not a substantial claim: may not pass S3 (load-bearing), S4 (based). May combine two claims.

Within weeks of birth, multiple sensory cues, including auditory and visual are used for offspring recognition, which in comparison with nocturnal rodents involves increased deployment of PFC.

“Within weeks of birth, multiple sensory cues, including auditory and visual are used for offspring recognition, which in comparison with nocturnal rodents involves increased deployment of PFC.”

May combine two claims.

In the context of mother-infant bonding, the steroid hormones of pregnancy are virtually redundant in that maternal care can and does occur without pregnancy and parturition, and in humans infant-bonded relationships extend to sister, fathers, aunts and grandparents.

“In the context of mother–infant bonding, the steroid hormones of pregnancy are virtually redundant in that maternal care can and does occur without pregnancy and parturition, and in humans infant-bonded relationships extend to sister, fathers, aunts and grandparents.”

Probably not a substantial claim: may not pass S4 (based). May combine two claims.

Brain growth is energetically costly, and postponing the greater part of this to the post-partum period has not only conserved the energetic demands on mother, but also has enabled brain growth to expand the cranial capacity way beyond the dimensions of the pelvic floor and birth canal.

“Brain growth is energetically costly, and postponing the greater part of this to the post-partum period has not only conserved the energetic demands on mother, but also has enabled brain growth to expand the cranial capacity way beyond the dimensions of the pelvic floor and birth canal.”

May combine two claims.

Medial regions of the frontal cortex appear to contribute to the recognition of different emotions and to the task of forming a 'person impression'.

“Medial regions of the frontal cortex appear to contribute to the recognition of different emotions (Hornak et al. 1996; Shamay-Tsoory et al. 2005) and to the task of forming a ‘person impression’.”

• cites Hornak et al. 1996Not checked yet

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• cites Shamay-Tsoory et al. 2005Not checked yet

  Not checked in the free run.

May combine two claims.

This recognition is not for individual pups, but for the litter as a whole since the pups are immobile and unlikely to cross-foster.

“This recognition is not for individual pups, but for the litter as a whole since the pups are immobile and unlikely to cross-foster.”