Brain Research, 532 (1990) 25-33 25
Elsevier
BRES 15985
Brain abnormalities in immune defective mice
Gordon F. Sherman 1, Lindsay Morrison 2, Glenn D. Rosen 1, Peter O. Behan 2 and
Albert M. Galaburda 1
1Dyslexia Research Laboratory and Charles A. Dana Research Institute, Beth Israel Hospital; Department o f Neurology, Harvard Medical
School, and Beth Israel Hospital, Boston, MA 02215 (U.S.A.) and 2Department of Neurology, University of Glasgow, and Institute of
Neurological Sciences, Southern General Hospital, Glasgow (U.K.)
(Accepted 8 May 1990)
Key words: Autoimmunity; Cerebral cortex; Developmental dyslexia; Dysplasia; Ectopia; Neuronal migration
Mouse strains with or without immune disorders were examined in order to further assess the incidence of brain anomalies in
immune-disordered strains. The brain was examined in Nissl-stained serial sections under a light microscope for the presence of abnormalities,
with specific attention to ectopic collections of neurons in layer I of the neocortex, as reported in the autoimmune New Zealand Black (NZB)
and BXSB strains. The present study was designed to survey additional strains with immune disorders (Snell dwarf, C57BL/6J-nu/nu,
BALB/cByJ-nu/nu, and SJL) and 7 control strains without immune disorders. In addition, we attempted to replicate past findings in the highly
affected BXSB strain and the MRL/1 strain, which develops autoimmune disease, but has a low incidence of brain abnormalities. The largest
number of brain abnormalities (20-40%) were seen in the C57BL/6J-nu/nu, Snell dwarf and BXSB strains. The anomalies in the
C57BL/6J-nu/nu and BXSB mice consisted of ectopic neurons in layer I of the neocortex, whereas the Snell dwarf mice had either neuron-free
areas in the cortex, or rippling of cortical layers II-IV, and one case had agenesis of the corpus callosum. Between 4% and 8% of the mice
from the SJL, MRL/1, and MRL +/+ strains had either neuron-free areas in the cortex or ectopic neurons in layer I. The BALB/cByJ-nu/nu
and control strains did not have any cortical abnormalities. Future studies will be designed to determine whether immune-based alterations
to the developing brain are responsible for the brain anomalies present in immune-disordered strains.
INTRODUCTION
New Zealand Black mice (NZB/BINJ) develop severe
autoimmune disease characterized by abnormalities of
stem cells, macrophages, and T and B lymphocytes, and
by the production of anti-erythrocyte antibodies. Death
usually occurs from hemolytic anemia at 16-17 months a9"
51,52. At least 20% of NZB mice have ectopic collections
of neurons in layer I of the cerebral cortex with dysplasia
of the underlying cortical laminae. Because of similarities
in appearance with ectopias reported in the dyslexic
brain 15"a6, it was suggested that NZB mice would be a
useful model for the study of the anomalies present in the
brains of dyslexics41'42.
The microdysgenesis in the NZB is usually seen in the
somatosensory cortex, and is attributed to an unspecified
disturbance of neuronal migration to the cortex as
described elsewhere 6"11"12"26. These neocortical ectopic
foci display abnormal patterns of local neuronal circuitry
as disclosed by neurofilament stains 43, and increased
numbers and altered location of VIP-positive neurons,
both in the ectopias and in other regions within the
hemisphere containing an ectopia (submitted for publi-
cation). In addition, hippocampal anomalies also attrib-
uted to a disturbance in migration are present in the NZB
m o u s e 33,34.
In a follow-up study designed to determine whether
other autoimmune strains have cortical anomalies 4°, we
found neuronal ectopias in cortical layer I of about 30%
of BXSB autoimmune mice. Most of the ectopic neurons
in the BXSB were present in frontal/motor regions of the
cortex, usually on the left side. The BXSB strain,
originally raised from the mating of a C57BL/6J female
and SB/Le male, develops severe autoimmune disease
consisting of the production of auto-antibodies, prolifer-
ation of B-cells, and immune complex glomeru-
lonephritis 1'5°'52'53. BXSB males die at 5 months of age
while females die at 15 months, which is related to the
presence on the Y chromosome of the Yaa gene that
accelerates immune disease in males 5z.
The presence of anomalies in the NZB and BXSB
prompted us to suggest that an abnormally-functioning
immune system (probably that of the mother, since these
ectopias must occur early) may play an etiologic role in
the production of developmental brain abnormalities.
Not all autoimmune mouse strains, however, show
Correspondence: G.F. Sherman, Department of Neurology, Beth Israel Hospital, 330 Brookline Avenue, Boston, MA, 02215, U.S.A.
0006-8993/90/$03.50 © 1990 Elsevier Science Publishers B.V. (Biomedical Division)