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Science: Ewe-turn for maternal behaviour

Pregnant ewes hate everything about lambs. Yet suddenly, an hour after
giving birth, the mother has formed an enduring bond with her lambs. She
has learnt to recognise her offspring by their smell, and she will accept
no others 鈥� behaviour that makes it difficult to foster orphan lambs. Neuroscientists
have now unravelled the dramatic changes in the brain that underlie the
making of this olfactory memory (Science, vol 256, p 833).

Three researchers collaborated to investigate how a ewe鈥檚 brain changes
to accommodate her need to recognise her own lamb: Keith Kendrick, at the
Agriculture and Food Research Council鈥檚 Institute of Animal Physiology and
Genetics at Babraham near Cambridge, Frederic Levy, at the National Institute
for Agricultural Research at Nouzilly, France and Barry Keverne of the University
of Cambridge.

To track down the neurophysiological changes, the researchers inserted
electrodes into the the olfactory bulb, the part of the sheep鈥檚 brain that
first receives information about odours. When Kendrick took recordings from
the bulb鈥檚 mitral cells, in pregnant ewes, he got no response to lamb odours,
although the cells responded enthusiastically to the smell of favourite
foods such as nuts or hay. Kendrick then made recordings from the same animals
four days after they had given birth. Now, 60 per cent of the mitral cells
responded preferentially to the odour of any lamb, and a small subset of
cells responded even more vigorously to the smell of the ewe鈥檚 own lamb.
鈥榃e found quite dramatic changes in the primary processing structures in
the brain as a result of the animal giving birth,鈥� says Kendrick.

To discover why this dramatic reorganisation takes place, the biologists
investigated the biochemical changes within the neural circuitry using a
technique known as in vivo microdialysis. This approach allows researchers
to monitor tiny changes in the neurotransmitters 鈥� chemical messengers which
nerve cells use to communicate with one another. A probe inserted into the
olfactory bulb picks up the overspill from neuronal communications in the
spaces around nerve cells. Because different nerve pathways in the olfactory
bulb rely on different neurotransmitters, this technique reveals which
cells have been active.

Kendrick and his colleagues measured the neurochemistry of the olfactory
bulb at five-minute intervals: before, during and after a mother had smelt
a lamb. Two types of neurotransmitters released by cells within the olfactory
bulb seemed to be intimately involved in the recognition process: the excitatory
amino acid glutamate and the inhibitory transmitter GABA.

Before birth, smelling a lamb produced no changes in these neurotransmitters.
And similarly, 24 hours after birth, smelling an alien lamb left these neurotransmitters
unmoved. But both GABA and the glutamate increased when a mother smelt her
own lamb. 鈥楾his appears to be part of the system that allows a mother to
make the discrimination between her own and alien lambs,鈥� says Kendrick.
The glutamate-releasing mitral cells appear to excite the GABA-containing
granule cells, which then feedback to inhibit the mitral cells. After birth,
the granule (GABA) cells seem to become more sensitive to glutamate released
by the mitral cells.

One further pathway, the centrifugal projections into the olfactory
bulb, is also a player in this neuronal drama. These neurons release two
other neurotransmitters, noradrenaline and acetylcholine. After birth, the
levels of all four sorts of transmitters go up, in what Kendrick says is
a 鈥榤ajor activation of all systems鈥�. During this surge of neurochemical
activity, the ewe forms the crucial olfactory bond with her lamb. 鈥榃hile
it is not clear what role all the different neurotransmitter changes play
in the formation of memory, we have established that noradrenaline is important,鈥�
Kendrick says. But during 鈥榬ecall鈥� 鈥� when the bonded ewe is later presented
with lamb smells and has to remember which is her own 鈥� neurochemical changes
are more specific and only GABA and glutamate levels rise.

This research suggests that the processes going on in a sheep鈥檚 olfactory
bulb as she gives birth provides a model for the study of memory and learning.
鈥榃e see the same kind of plasticity that everyone is talking about in studies
of spatial memory involving the brain鈥檚 hippocampus,鈥� Kendrick says. 鈥楳other
nature may have been quite conservative in the design of basic mechanisms
of memory and learning.鈥�

The research also has practical value for farmers struggling with recalcitrant
sheep. The neuroscientists have discovered that the whole range of neuronal
and behavioural changes surrounding birth are triggered by the messages
sent from the vagina and cervix to the brain. By mechanically stimulating
a ewe鈥檚 vagina and cervix, farmers can convince a new mother to form a bond
with another lamb, without forgetting her own lambs. 鈥榃e鈥檙e pleased the
work is of agricultural value. We began to try to understand the neurochemistry
and physiology of maternal behaviour in sheep to try to solve the farmers鈥�
difficulties with orphan lambs,鈥� says Kendrick.