Chemical Senses Vol. 30 No. suppl 1 © Oxford University
Press 2005; all rights reserved
Vomeronasal Mechanisms of Mate Recognition in Mice
Sub-Department of Animal Behaviour, University of Cambridge, Cambridge, UK
Correspondence to be sent to: Peter A. Brennan, e-mail: pab23{at}cam.ac.uk
Key words: accessory olfactory bulb, individuality chemosignals, local field potentials, medial amygdala, pregnancy block
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Introduction |
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 Top Introduction Individuality and the pregnancy...Neural mechanisms of mate...AcknowledgementsReferences |
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The ability of animals to distinguish individual con-specifics influences many aspects of their behaviour, including choice of mate, territorial marking and mother-offspring interactions. In rodents, information about individuality is conveyed by chemical cues in their urine and body secretions. Hence, mice can be trained to discriminate the urine odour of congenic mice that differ only in genes of their major histocompatibility complex (MHC). This ability is likely to be based on MHC-related differences in the profile of urinary volatiles (Singer et al., 1997
), which are sensed by the main olfactory system and generate
statistically different patterns of activity across large populations of neurons in the
main olfactory bulb (Schaefer et al.,
2002). In contrast, individual recognition underlying urine countermarking
behaviour of male mice depends on the profile of major urinary proteins rather than MHC
type (Hurst et al., 2001),
suggesting that mice use different chemosignals for signalling individual identity in
different behavioural contexts. Furthermore, information about the individual identity of
mice can be conveyed by both the main olfactory and vomeronasal systems. Whereas the main
olfactory system is adapted to learn and discriminate small differences in the profile of
airborne volatiles, the vomeronasal system responds to a more limited range of
non-volatile stimuli taken up following direct contact. Moreover, the representation of
individual identity in vomeronasal system appears to differ from that in the main
olfactory system, as individual neurons in the accessory olfactory bulb (AOB), respond
highly selectively to the strain identity of anaesthetized conspecifics (Luo et al., 2003). |
Individuality and the pregnancy block effect |
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TopIntroductionIndividuality and the pregnancy...Neural mechanisms of mate...AcknowledgementsReferences |
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Individuality chemosignals sensed by the vomeronasal system are vital for mate recognition in the pregnancy block effect (Lloyd-Thomas and Keverne, 1982
). This effect is elicited by
exposure of recently mated female mice to male urinary chemosignals from unfamiliar
inbred strains, which blocks the implantation of their developing embryos and leads to
pregnancy failure. Crucially, female mice learn to recognize the strain identity of
urinary chemosignals from the mating male, which subsequently prevents them from blocking
her pregnancy. The strain identity of the pregnancy blocking chemosignals is known to be
influenced by MHC Class I genotype, as chemosignals from congenic males, which differ
from the mating male at only the H2 locus of the MHC, are effective in blocking pregnancy
(Yamazaki et al., 1986).
However, differences in stimulus access and the low level of sequence homology between
main olfactory and vomeronasal receptors (Herrada
and Dulac, 1997;
Matsunami and Buck, 1997;
Ryba and Tirindelli, 1997) suggest
that different types of chemosignal may convey MHC-dependent information in the two
systems. Indeed, recent evidence suggests that MHC class I peptide ligands form a novel
class of chemosignal that convey individuality in the pregnancy block effect (Leinders-Zufall et al., 2004). These
nine-amino acid peptides are products of the proteosomal degradation pathway, and are
able to convey information about strain identity due to the positions of large
hydrophobic side chains of particular amino acids, known as anchor residues, along the
peptide chain. |
Neural mechanisms of mate recognition |
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TopIntroductionIndividuality and the pregnancy...Neural mechanisms of mate...AcknowledgementsReferences |
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The pregnancy block effect is mediated by a relatively direct neural pathway from the vomeronasal receptors to the hypothalamus, via the accessory olfactory bulb (AOB) and corticomedial amygdala (Li et al., 1989
). Activation of this pathway reduces levels of the hormone prolactin,
and the consequent removal of luteotrophic support leads to a fall in progesterone and a
return to oestrus (Bellringer et al.,
1980;
Li et al., 1994). But how can
synaptic changes in this relatively simple neural system account for its ability to learn
about and subsequently recognize the chemosignals of the mating male? A substantial body
of evidence has accumulated that suggests that the neural changes underlying this
chemosensory learning are localized to the AOB, at the first stage of processing of the
vomeronasal information (Kaba and Nakanishi,
1995). The association of elevated noradrenaline levels in the AOB at mating
with the activity of those mitral cells that respond specifically to the mating male
chemosignals is hypothesized to cause a long-lasting increase in gain of their reciprocal
synapses with the inhibitory granule interneurons. This increase in inhibitory control of
the mitral cells can account for the mate recognition by selectively disrupting the
transmission of the mating male’s chemosignal at the level of the AOB, preventing
it from activating the hypothalamic mechanisms that result in pregnancy block (Brennan et al., 1990). Support for this hypothesis has come from neurochemical investigations using in vivo microdialysis in freely behaving mice (Figure 1). We found significantly higher levels of the inhibitory neurotransmitter GABA in the AOB of mated females, in response to their mate’s pheromones, compared to the response of non-mated females that received the same amount of male exposure. This is consistent with an increase in inhibitory feedback acting on the mating male’s chemosignals. Further support has been provided by recent electrophysiological investigations of the AOB and medial amygdala in freely behaving female mice (unpublished data). Local field potentials (LFPs) recorded from the AOB were found to oscillate across a range of frequencies, with a predominant low frequency oscillation of around 4–8 Hz. Such oscillations of neural activity are a common feature of olfactory systems and result from the synchronous depolarization and hyperpolarization of large neuronal populations. We found that the predominant frequency of LFP oscillation in the AOB increased significantly in the 8–12 Hz theta range in response to exposure to male chemosignals, irrespective of strain identity. However, following mating, the urinary cues from the mating male remained effective in increasing the amplitude of the LFP oscillations, in the 8–12 Hz frequency range, whereas there was no increase in response to urinary cues from an unfamiliar male. Furthermore, the frequency of action potentials recorded from neurons in the medial amygdala was on average twice as great in response to urine from an unfamiliar male compared to urine from the mating male, irrespective of the strains of the males that were used. These differential electrophysiological responses to male chemosignals are consistent with a disruption of the mate’s pregnancy blocking signal at the level of the AOB. Although, the role of oscillating neural activity in conveying vomeronasal information is unclear, the newly discovered individuality chemosignals may provide a useful tool for future investigations into the neural basis for mate recognition in the pregnancy block effect.
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P < 0.05, |
Acknowledgements |
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TopIntroductionIndividuality and the pregnancy...Neural mechanisms of mate...AcknowledgementsReferences |
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We would like to thank Carlos de la Riva for his assistance with the HPLC analysis of neurotransmitters. This work was supported by grants from the MRC and BBSRC.
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TopIntroductionIndividuality and the pregnancy...Neural mechanisms of mate...AcknowledgementsReferences |
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