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The molecular basis of monogamy

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The pioneering work in the field of pair bonding by Thomas Insel and his group (Insel and Young 2001, Young and Wang 2004) has documented  the marked rise in the density of the oxytocin receptors all over the entire nuc acumbens and the dorsal striatum of the monogamous prairie vole compared with the polygamous montane vole. The partner preference formation in the mating female prairie vole is blocked through infusions of an oxytocin receptor antagonist  into the nuc accumbens and the prefrontal cortex but not into the dorsal striatum.It is highly interesting that in the monogamous praire vole this marked increase in oxytocin densities is not associated with  any clear increase in the number of oxytocin nerve cell bodies in the hypothalamus and in the medial preoptic area projecting to these areas nor in oxytocin nerve terminal networks  in e.g. the nuc accumbens vs polygamous voles (Lim et al 2004).

We propose that monogamy in the female prairie vole is brought about through an increase in oxytocin volume transmission especially in nuc accumbens but likely also in the prefrontal cortex: volume transmission of signals occurs by the extra-synaptic exchange of materials between neuronsThe mating induced oxytocin release from the sparse plexus of  oxytocin terminals can thus through diffusion and flow of oxytocin in critical limbic regions of the female reach  increased numbers of widespread high affinity oxytocin receptors leading to an increased impact of oxytocin transmission on these networks and the development of social attachment in the female (long distance volume transmission; Fuxe et al 2010, Agnati et al 2010).

There exists  a marked increase in the density of the vasopressin receptor V1a in the ventral pallidum of the monogamous male  prairie vole vs the polygamous montane vole which appear to play a key role for monogamy in the male prairie vole.Thus, microinjections of a V1a antagonist into the ventral pallidum block mating induced pair bonding. In view  of the lack of a corresponding rise of the vasopressin immunoreactive terminals and axons in this region the evidence favours the view that an increase in vasopressin volume transmission in the ventral pallidum mediates monogamy in the  male prairie vole.

Our hypothesis is therefore that pair bonding requires increases in  vasopressin (male) and oxytocin (female) volume transmission in critical limbic regions through increases in high affinity V1a receptor densities in the Ventral pallidum (male) and in oxytocin receptor densities in the   nuc accumbens shell (female). Vasopressin receptors in the ventral pallidum exist also in monogamous mice and primates, whereas they are absent in this region in related rodent and primate species that do not form pair bonds (Insel and Young 2001).

Behavioural differences like pair bonding found in different species of the same genus may thus  be caused by  increasing the extrasynaptic receptor densities in critical limbic circuits for the diffusing volume transmission signals in this case the diffusing oxytocin and vasopressin signals.

Insel and Young. Nature Reviews, Neuroscience. 2001; 2: 129.
Young and Wang. Nature Neuroscience. 2004: 7: 1048.
Lim et al. J Comp Neurol. 2004; 468: 555.
Fuxe et al. Progress in Neurobiology. 2010; 90: 82. 
Agnati et al. Brain Res Review. 2010; 64: 137.

ritratto di Luigi Agnati Luigi Agnati
Fisiologia e neurobiologia, Università di Modena e Karolinska Institute di Stoccolma

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