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Seizure-induced brain damage in
homozygous LGI1
/
mice
No major differences in cortical or hippocampal organization were
evident in Nissl-stained sections prepared before seizure onset at
postnatal day 8 (Fig. 7A–C) or after repeated seizures at postnatal
day 14 (Fig. 7D–F) in LGI1
/
mice (n = 4 for each age) and either
LGI1
+/
(n = 4 for each age) or wild-type (n = 4 for each age)
animals. Cortical lamination was similar, suggesting that the ab-
sence of LGI1 did not affect radial migration of pyramidal cells.
However, at postnatal day 14 we detected an abnormal dispersion
of dentate granule cells in LGI1
/
mice (Fig. 8C). No such dis-
persion was evident in wild-type (Fig. 8A), LGI1
+/
littermates
(Fig. 8B) or in LGI1
/
mice before seizure onset at postnatal
day 8 (Fig. 9A). Granule cell layer thickness was significantly
increased in LGI1
/
mice compared with LGI1
+/
(P53.3E06)
and wild-type (P 5 9.9E05) mice. Granule cell dispersion is asso-
ciated with temporal lobe epilepsy in the human and in experi-
mental models. We next investigated other markers of
epileptogenesis. We assessed expression of glial fibrillary acidic
protein to determine the reactive state of astrocytes in LGI1
/
,
LGI1
+/
and wild-type mice. There was no difference in glial
fibrillary acidic protein staining of tissue from LGI1
/
(n =3,
Fig. 9F), LGI1
+/
(n = 3, Fig. 9E) and wild-type (n = 3, Fig. 9D)
postnatal day 8 pups. In contrast, in LGI1
/
(n = 3) animals at
P14 after repeated seizures, glial fibrillary acidic protein immuno-
reactivity increased, particularly in the hilus of the dentate gyrus
(Fig. 8F, I), while there was no change in LGI1
+/
(n = 3) (Fig. 8E,
H) or wild-type mice (n = 3) (Fig. 8D, G). In temporal lobe epilep-
sies, mossy fibres often sprout to form aberrant recurrent synapses
with dentate granule cells. We used immunostaining against the
zinc transporter 3, present at high levels in mossy fibres to label
synapses (Palmiter et al., 1996). We consistently detected zinc
transporter 3 labelling in the inner molecular layer of the dentate
gyrus of LGI1
/
mice after seizures (postnatal day 14), indicating
the presence of aberrant mossy fibre terminals (n = 4; Fig. 8L, O).
In contrast, no zinc transporter 3 labelling was detected in this
area in LGI1
+/
mice (n = 4, Fig. 8K, N) or wild-type mice (n =4,
Fig. 8J, M), or in any mouse studied at postnatal day 8 (LGI1
/
,
n = 4; LGI1
+/
, n = 4; wild-type, n = 4; Fig. 9G–I). Finally, we asked
whether recurrent seizures caused hippocampal neuronal loss in
LGI1
/
mice. We used Fluoro-Jade C, which is specific for degen-
erating neurons (Schmued et al., 2005). After several seizures,
Fluoro-Jade C labelling revealed a strong neuronal loss in
the CA3 region and a lesser cell death in the CA1 region of
LGI1
/
mice aged postnatal day 14 (n = 3, Fig. 8P-R), but not
in LGI1
+/
or wild-type or postnatal day 8 LGI1
/
mice (not
shown). We note that the number of Fluoro-Jade C-positive
LGI1+/-
Wild-type
Postnatal age (days)
*
1100 μV
1 sec
Wild running Tonic phase
Auditory
stimulus
LGI1+/-
Death
60
50
40
30
20
10
0
P21 P28
% of audiogenic seizures
A
B
Figure 6 Lower threshold for audiogenic seizures in heterozygous LGI1
+/
mice. (A) Variation with age in susceptibility to audiogenic
seizures of LGI1
+/
mice exposed to a sound stimulus (11 kHz, 95 dB) compared with wild-type littermates. At postnatal Day 21,
susceptibility was low, while at postnatal day 28, LGI1
+/
mice exhibit a significant susceptibility to audiogenic seizures compared with
wild-type. *P50.05. LGI1
+/
(n = 25), wild-type (n = 17). (B) Epidural EEG recording in a P28 LGI1
+/
mouse under auditory stimulation.
During the auditory stimulation (dashed arrow), the mouse was immobile and the EEG showed a normal background activity. Later, the
mouse exhibited wild running (associated with movement artifacts), followed by a tonic phase and death (associated with suppression of
brain activity).
LGI1 knockout mice Brain 2010: 133; 2749–2762 | 2757
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