Download Inverted pyramidal neurons in chimpanzee sensorimotor cortex are

Som atosensory & M otor Research 1999; 16(1): 49 ± 56
Inverted pyramidal neurons in chim panzee sensorim otor cortex are
revealed by imm unostaining with m onoclonal antibody SM I-32
HUI-XIN QI 1 , N EERAJ JAIN 1 , TOD D M . PREUSS 2 and JO N H. K AAS 1
1
D epartm ent of Psychology, Vanderbilt U niversity, N ashville, TN 37240; 2 D ivision of B ehavioral B iology, University of
Southwestern Louisiana, N ew Iberia R esearch Center N ew Iberia, LA 70560, U SA
Abstract
We used the m onoclonal antibody SM I-32 to label pyram idal cells of sensorimotor cortex in two chimpanzees. The majority
of the pyramidal cells had typical vertically oriented apical dendrites that extended towards the pial surface. A small
population of pyramidal cells varied from this orientation, so that the apical dendrites were 20 Æ
or more from radial, and
were often inverted, extending away from the pial surface. W hen numbers of non-inverted and inverted pyramidal cells were
compared, less than 1% were found to be inverted.
Key words: Anthropoid prim ate , Pan, som atosensor y cortex , imm unohistochem istr y
Introduction
Pyramidal neurons in the neocortex of m am m als
norm ally extend their apical dendrites towards the
pial surface. Van der Loos (1965), however, described cells that deviate from this typical configuration.
In a Golgi study of the visual cortex in rabbits, he
estim ated that som e 15 ± 20% of pyram idal cells had
apical dendrites that deviated 20 Æ
or m ore from the
norm al orientation, w ith com pletely inverted orientations the m ost frequent of the atypical cells.
Small num bers of non-upright pyram idal cells were
also recognized in G olgi preparations from rats, cats,
and m onkeys. Van der Loos argued that the nonupright pyram idal cells were errors rather than a
m orphological adaptation to a functional role. T hus,
he concluded that ª the existence of disorientated
pyramids m ay be explained by assum ing that, in the
turm oil of m igration to, and alignm ent of the cells in,
their definitive cortical sites, a few cells, perhaps not
surprisingly so, becom e m isaligned.º In support of
this hypothesis, larger proportions of inverted pyram idals are described in certain pathological studies
that affect cell m igration, such as the reeler m utant
m ouse (Landrieu and G offinet, 1981). In addition,
inverted pyram ids are thought to be m ore com m on
in the deeper layers (Ferrer et al., 1986; van
Brederode and Snyder, 1992; Einstein and Fitzpatrick, 1991), w hich develop the earliest. O thers
indicate that the functional significance of inverted
pyramidals is unknow n, holding out the possibility
that they may play a unique functional role (van
Brederode and Snyder, 1992). O ne type of unusual
pyramidal neuron, the M artinotti cell, with atypically
oriented apical dendrites and vertically ascending
axons (T Èom b Èol, 1984; Ferrer et al., 1986), m ay well
be a specialized type of neuron (Prieto et al., 1994).
W hile inverted pyramidals have been observed by a
number of investigators in mice, rats, rabbits, cats,
and even humans (see Feldman 1984), little is
known about the frequency of their occurrence, the
locations in cortex where they occur, and the
prevalence am ong different species. M ost reports
suggest that they are less frequent than indicated by
Van der Loos (1965), w ith Parnavelas (1977) estim ating that they represent approxim ately 1% of
pyramidal cells in the sensorim otor cortex of rats.
T he rarity of observations on inverted pyram idal
cells is undoubtedly related to the difficulty of
obtaining suitable Golgi m aterial from large am ounts
of cortex. This difficulty can now be circum vented by
staining pyram idal cells im m unohistochemically. A
m onoclonal antibody to neurofilam ent protein, SMI32, labels the cells body and dendrites of a large
subset of pyram idal cells in a G olgi-like m anner
(Cam pbell and M orrison, 1989, Hof et al., 1995a;
1995b; 1996; N im chinsky et al., 1996; Preuss et al.,
1997). In such preparations, it is relatively easy to
exam ine the orientations of the apical dendrites of a
large number of SM I-32 im m unoreactive neurons.
We did this in sections of cortex from the brains of
two chim panzees that were processed for SM I-32
Correspondence: Jon H . Kaas, Department of Psychology, Vanderbilt U niversity, 301 W ilson Hall, 111 21st Ave. South, Nashville, TN
37240 USA. Tel: (615) 322 ± 6029; Fax: (615) 343 ± 4342 E-mail: jon.kaas@ vanderbilt.edu
0899 ± 0220/99/01004 9 ± 08 $9.00 € 1999 Taylor & Francis Ltd
50
Hui-X in et al.
antibody as part of a m ore extensive study of the
architecture of sensorim otor cortex. The results
indicated that inverted and other non-upright
pyramidal cells exist am ong the SMI-32 im munoreactive cells of chimpanzee sensorim otor cortex, but
they are rare.
M ethods
M aterial from the brains of two adult chim panzees
(Pan troglodyt es ) were obtained from the N ew Iberia
Research Center, N ew Iberia, LA and Yerkes
Regional Primate C enter, Atlanta, GA. Both anim als
died of natural causes and were perfused within ten
to twenty m inutes of death. T he chim panzees were
perfused transcardially with phosphate buffered
saline (PBS, pH 7.4), followed by 4% paraform aldehyde in 0.1 M phosphate buffer, and subsequently
with 4% paraform aldehyde with 10% sucrose. T he
brains were blocked and post fixed in 4% paraform aldehyde and 10% sucrose in phosphate buffer
for two weeks, and further cryoprotected by im m ersion in buffered 20% and 30% sucrose solutions. T he
blocks of tissue containing sensorim otor cortex were
cut perpendicular to the central sulcus (Fig. 1) or in
a parasagittal plane into 50 m m thick sections w ith a
freezing m icrotom e. Every tenth section was reacted
for SM I-32 prim ary antibody (Sternberger M onoclonals, Inc.) at a 1: 2000 dilution for 40 ± 48 h at 4 Æ
C.
Further details of processing procedures have been
described by Preuss et al. (1997). Remaining series
of the brain sections were processed with other
histochem ical procedures useful for identifying
architectonic boundaries (see Q i et al., 1997). T hese
sections were used to identify boundaries of cortical
areas 4, 3a, 3b, 1 and 2 in the present study.
Brain sections were exam ined with a Zeiss Axioskop m icroscope at 400X m agnification and pyram idal cells were identified. In order to estim ate the
F I G U R E 1. A schematic drawing of the dorsolateral view of
the left hemisphere of a chim panzee brain. The solid line
indicates the plane of sectioning perpendicular to the
central sulcus and corresponds to the section shown in
Figure 2A. cs, the central sulcus extends to the midline;
M , medial; R, rostral.
population of SM I-32 im m unoreactivity (SM I-32-ir)
pyramidal cells that were inverted, a 10 m m 3
10 m m grid was superim posed on layers III, V, and
VI, and pyram idal cells were counted within the grid.
Counts were m ade in a total of 1057 sem irandom ly
selected sam ple fields through the som atosensory
and m otor cortex.
We classified cells as atypical pyram idal cells if they
had triangular cell bodies and long stout apical
dendrites that deviated m ore than 20 Æfrom radial
orientation (follow ing Van der Loos, 1965). W ithin
this class of atypical pyram idal cells, we also distinguished a subclass of inverted pyram idal cells,
which had apical dendrites directed toward deeper
layers of cortex or the white m atter, and basal
dendrites that ascended toward the superficial layers.
D igital im ages were acquired for the purpose of
illustrating inverted pyram idal cells by using a
M icrolumina L eaf digital cam era m ounted on a
N ikon E800 m icroscope. T he digitized im ages were
adjusted for brightness and contrast using Adobe
Photoshop, but they were not otherwise altered.
Results
T he SM I-32 antibody labeled cell bodies and dendrites of neurons throughout sensorim otor cortex.
T hese cells were concentrated in a deep band
corresponding to layer V and a superficial band of
neurons in the inner half to two-thirds of layer III.
Som e neurons in other layers were labeled as well.
T he great m ajority of these labeled neurons were
clearly pyram idal cells, although nonpyram idal cells
were occasionally labeled. Large num bers of neurons
were labeled in area 4 (Fig. 2A) and in area 3a, while
fewer area 3b neurons were labeled. Areas 1 and 2
(Fig. 3A) had more SM I-32 im m unoreactive neurons than area 3b, but fewer than areas 4 and 3a.
T hese results w ill subsequently be described in m ore
detail (see also Q i et al., 1997).
O f the great num ber of pyram idal cells that were
exam ined in these fields, the vast m ajority were
typical pyram idal cells w ith the long axis of the cell
body oriented perpendicular to the brain surface.
N evertheless, pyram idal cells with atypical orientations were occasionally observed. The m ost com m on
of the atypical pyram idal cells were the inverted
pyramidal cells, such as those shown in Fig. 2B, 2E,
3B and 3C. Other atypical pyram idal cells were not
so perfectly inverted, although they fell within our
classification of inverted. Thus, the apical dendrite of
the neuron in F ig. 2D coursed at a downward angle
about 40 Æ
from radial (i.e., perpendicular to the pia).
Another exam ple of a poorly oriented but inverted
pyramidal neuron is illustrated in Fig. 2C. The
inverted pyram idal cells were m ost often found in
layer VI, but they were present in layers III and V as
well. T he widths of cell bodies ranged from 10 ± 25
m m , and apical dendrites could be traced as far as
400 m m . T he thin axons of these neurons were
Inverted pyramidal cells
51
F I G U R E 2. Photom icrographs of m otor cortex stained with SM I-32 antibody. The pial surface is towards the top in all panels.
(A) A low magnification photomicrograph of a parasagittal section through area 4. Roman num erals indicate the cortical
layers. The arrow indicates an inverted pyram idal cell shown at higher magnification in (B). (B) An example of an inverted
pyramidal cell in layer III of area 4. (C) An inverted pyram idal cell in layer III of premotor cortex. A pyramidal cell with an
atypical orientation is located to the left of the arrow. (D) A poorly oriented inverted pyramidal cell in layer V of area 4. (E) An
inverted pyramidal cell in layer VI of area 4. The locations of cells (B), (C), (D) and (E) are shown in the inset. Scale bars: 200
m m in (A); 50 m m in (B), (C), (D), and (E). Arrows indicate the inverted pyramidal cells. ad, apical dendrite.
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Hui-X in et al.
F I G U R E 3. Photomicrographs of somatosensory areas stained with the SMI-32 antibody. (A) A low magnification
photomicrograph through area 2. Roman numerals denote the six cortical layers. The arrow indicates an inverted pyramidal
cell shown at higher magnification in (B). (B) An example of an inverted pyramidal cell (arrow) in layer VI of area 2. (C)
An inverted pyramidal cell in layer VI of area 3b. (D) Location of the cells shown in (B) and (C). Scale bars: 200 m m in (A);
50 m m in (B) and (C). ad, apical dendrite.
Inverted pyramidal cells
som etim es apparent, but could be traced for only
short distances. Van der Loos (1965) also observed
such atypically oriented pyram idal cells, including
those with apical dendrites extending towards the
pial surface but at an angle. Since m any pyram idal
cells are not perfectly oriented in the radial axis, Van
der Loos (1965) classified pyram idal neurons as
m isoriented if they reached the arbitrary criterion of
being rotated 20 Æ
or m ore from radial. Such a neuron
is shown in Fig. 4A with an apical dendrite that
extended at a 45 Æ
angle from vertical. In contrast, the
neuron in Fig. 4B, started at a slight angle off the
radial, but changed its course to becom e vertically
oriented. This m ay be regarded as a sm all error,
which did not m eet our criteria for an atypically
oriented pyram idal cell. T he cell in Fig. 4C also
m ade a correction, but m uch of the proxim al portion
53
of the apical dendrite coursed away from the cell
body at an angle of more than 20 Æ
. In a final exam ple
(Fig. 4D ), the apical dendrite coursed along in a
horizontal plane parallel to the pial surface. T hus,
atypical pyram idal cells had a range of orientations,
and the estim ated frequency of such cells will depend
on the criteria used to identify them .
O f 1977 identified pyram idal neurons, 12 (0.61%)
were classified as inverted, in that the apical dendrite
curved from the som a at an angle below the
horizontal plane. T he great m ajority of inverted
pyramidal cells was located in cortical layer V I (Table
1). T hus, 1 of 1004 identified pyram idal cells was
classified as inverted in layer III (0.10% ), 1 of 527
pyramidal cells was inverted in layer V (0.19%), and
10 of 446 identified pyramidal cells were inverted in
layer V I (2.24%). T hus, it appears that for the
F I G U R E 4. Photomicrograph illustrating atypically oriented pyramidal cells. (A) In the cell denoted by the arrow, the long
axis of the cell body and apical dendrite deviates 45 Æfrom radial. (B) A ``regular’’ pyramidal cell (arrow). The cell body
started at an angle slightly off radial, but the apical dendrite corrected its course to radial. (C) A ``regular’’ pyramidal cell
in which the apical dendrite curved to make a correction, but much of the proximal portion of the apical dendrite coursed
away from the cell body at an angle of more than 20 Ê. (D) An exam ple of a horizontal pyramidal cell (arrow) in which the
apical dendrite traveled in the plane parallel to the pial surface. Scale bars: 50 m m .
54
Hui-X in et al.
TA B L E 1. Laminar distribution of inverted pyramidal cells in sensorimotor cortex
M otor cortex
Layer III
Layer V
Layer VI
Total
Som atosensory cortex
Sensorimotor cortex
TP
IP
IP/TP
TP
IP
IP/TP
TP
IP
IP/TP
576
332
264
1172
1
1
8
10
0.17%
0.30%
2.94%
0.85%
427
194
172
793
0
0
2
2
0%
0%
1.15%
0.25%
1003
526
436
1965
1
1
10
12
0.10%
0.19%
2.24%
0.61%
Abbreviations: IP, inverted pyramidal cells; TP, typical pyramidal cells.
subpopulations of SMI-32 positive pyram idal cells,
less than one percent are inverted.
Additional counts were m ade through the sensorim otor area in order to estim ate the percentage of
atypically oriented pyram idal cell, w hich included all
pyramidal cells w ith apical dendrites that deviated
m ore than 20 Æfrom the vertical, including inverted
pyramidal cells. Am ong a total of 704 identified
pyramidal cells, 18 (2.56% ) were classified as atypical (Table 2). O f these, 2 of 396 cells were classified
as atypical in layer III (0.51% ), 4 of 166 in layer V
(2.41%), and 12 of 142 in layer VI (8.45% ).
horizontal pyram idal cells with apical dendrites that
are oriented directly perpendicular to the plane of
the section (i.e., directly toward or away from the
observer) would probably not be identified as pyram idal cells. Atypical pyram idal cells m ay thus be as
m uch as twice as com m on as indicated by the
frequency of recognizable atypical cells.
To our knowledge, this is the first imm unocytochem ical study of atypical pyram idal cells, and the
first report of such cells in chim panzees. O ur
observations illustrate the value of the SM I-32
antibody as a tool for studying pyram idal cell
m orphology, which results from its relatively com plete, G olgi-like staining of the pyram idal cell bodies
and dendrites. SM I-32 labels m any, but not all,
pyramidal cells; it leaves unlabeled m ainly sm aller
pyramidal and nonpyram idal cells. Presum ably, the
latter cells are unstained because they express little
neurofilam ent protein, or express neurofilam ent
proteins that lack the epitope recognized by SM I-32
m onoclonal antibody (see Cam pbell and M orrison,
1989). In any case, the labeling favors large pyram idal neurons, especially those that have long projections (C am pbell and M orrison, 1989).
Previous observations of inverted and atypically
oriented pyram idal cells were based alm ost exclusively on G olgi im pregnation techniques (an exception being de Lim a et al., 1990). Like SM I-32
im m unocytochem istry, the Golgi technique also
labels a subset of cells, although perhaps a random
subset with respect to the neuronal type and size. Even
with the Golgi technique, there have been few
system atic studies of the frequency of atypical
Discussion
We used the SMI-32 antibody to label a subset of
pyramidal cells in the sensorim otor cortex of two
chim panzees. M ost pyram idal cells had radially
oriented apical dendrites extending towards the pial
surface, but neurons w ith apical dendrites of other
orientations were occasionally obser ved as well.
T hese unusual orientations ranged from a modest
20 Ædeviation from vertical near the cell body with
subsequent corrections to near vertical, to the m ore
com m on com pletely inverted pyram idal cells.
According to our estim ate, inverted pyram idal cells
were less than 1% of total SM I-32-ir pyram idal cells.
However, the total proportion of atypically oriented
pyramidal cells with unusual orientation (those 20 Æ
or m ore off the vertical; Van der Loos, 1965) was over
2% and constituted over 8% of the pyram idal cells in
layer VI. T he actual num ber of atypically oriented
pyramidal cells is likely to be higher than this since
TA B L E 2. Laminar distribution of atypically oriented pyramidal cells in sensorimotor cortex
M otor cortex
Layer III
Layer V
Layer VI
Total
Som atosensory cortex
Sensorimotor cortex
TP
IP
IP/TP
TP
IP
IP/TP
TP
IP
IP/TP
246
109
89
444
2
2
8
12
0.81%
1.80%
8.25%
2.63%
148
53
41
242
0
2
4
6
0%
3.64%
8.89%
2.42%
394
162
130
686
2
4
12
18
0.51%
2.41%
8.45%
2.56%
Abbreviations same as Table 1.
Inverted pyramidal cells
pyramidal cells. It has been reported that inverted and
atypically oriented pyramidal cells are present in the
cortices of m ice, rats, dogs, cats, m onkeys, and
hum ans (e.g., Van der Loos, 1965; G lobus and
Scheibel, 1967; W illiam s et al., 1975; Parnavelas et al.,
1977; Ferrer et al., 1986; M iller, 1988), that inverted
pyramids are one of the m ost com mon of the
atypically oriented types (Van der Loos, 1965), and
that they are m ore frequent in deeper layers (Van
Brederode and Snyder, 1992; Ferrer et al., 1986a,b,
1987; E instein and Fitzpatrick, 1991) and in abnorm al cortex (W illiam s et al., 1975; Landrieu and
G offinet, 1981; Prieto et al., 1994). Van der Loos
(1965) appears to have made the m ost serious attem pt
to estimate the proportion of atypically oriented
pyramidal neurons, and yet his estim ate of 18% in
rabbit visual cortex (based on 33 atypical out of 183
pyramidal cells) is higher than subsequent estim ates
of 5% in rabbits (G lobus and Scheibel, 1967) and 1%
in rats (Parnavelas et al., 1977). The proportion of
such cells m ay var y across species and cortical areas,
but it seems fair to conclude, based both on previous
reports and on the present study, that atypically
oriented and inverted pyram idal cells are generally
uncom m on, perhaps 1± 3% , although they m ay
constitute a m uch higher proportion of the pyram idal
cells in layer VI, on the order of perhaps 10%.
If these unusual neurons reflect errors in developm ent, it seems fair to ask what the consequences for
neural processing m ight be. A 1± 5% error rate in the
development of norm al dendritic orientation m ay
not have m uch im pact on neural networks. In
addition, given the great plasticity of the developing
brain, and the evidence that m ost of the atypically
oriented neurons have axons that course norm ally
(Einstein and Fitzpatrick, 1991; M iller, 1988; D e
Lim a et al., 1990), many or m ost of the abnorm al
neurons m ay have adopted partially functional roles.
In their intracellular recording of layer V I pyram idal
cells from slices of rat sensorim otor cortex, van
Brederode and Snyder (1992) did not find any
differences between the intrinsic electrical properties
of the regular and irregularly oriented pyram idal
cells. In addition, the possibility rem ains that atypically oriented neurons represent functional subtypes, although they are uncom m on, especially in
layers III and V.
If inverted pyram idal cells represent developm ental errors, as proposed by Van der Loos (1965), then
one m ight expect large-brained and sm all-brained
species to vary in the proportion of errors. The rate of
neuorblast m igrations and the generation of cortical
layers is m uch m ore rapid in brain in rats and m ice
than in m onkeys (see Rakic, 1977), and rapid traffic
along m igratory paths m ight generate m ore disoriented neurons. In contrast, if inverted pyram idal
cells represent a specialized cell class with a specific
functional role, they m ight be m ore frequent in the
large hum an and chim panzee brains, where there
m ay be m ore morphological specialization of neu-
55
rons (Parnavelas et al., 1977; M eyer, 1987). O ur
results, however, suggest that inverted pyram ids are
no more frequent in chimpanzees than in rabbits and
rats. W hether the atypically oriented pyram idal cells
are a developm ental error or a function subtype
rem ains to be determ ined.
Acknowledgm ent
Supported by N IH G rant N S16 446 and by USLN IRC .
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