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The Journal of Neuroscience, 2001, 21:RC163:1-5
RAPID COMMUNICATION
The Pyramidal Cell in Cognition: A Comparative Study in Human and
Monkey
Guy N.
Elston1, 2,
Ruth
Benavides-Piccione2, and
Javier
DeFelipe2
1 Vision, Touch, and Hearing Research Center,
Department of Physiology and Pharmacology, The University of
Queensland, Queensland, 4072, Australia, and 2 Instituto
Cajal, Consejo Superior de Investigaciones Científicas,
28002, Madrid, Spain
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ABSTRACT |
Here we present evidence that the pyramidal cell phenotype varies
markedly in the cortex of different anthropoid species. Regional and
species differences in the size of, number of bifurcations in, and
spine density of the basal dendritic arbors cannot be explained by
brain size. Instead, pyramidal cell morphology appears to accord with
the specialized cortical function these cells perform. Cells in
the prefrontal cortex of humans are more branched and more spinous than
those in the temporal and occipital lobes. Moreover, cells in the
prefrontal cortex of humans are more branched and more spinous than
those in the prefrontal cortex of macaque and marmoset monkeys. These
results suggest that highly spinous, compartmentalized, pyramidal cells
(and the circuits they form) are required to perform complex cortical
functions such as comprehension, perception, and planning.
Key words:
cortex; dendrite; spine; primate; macaque; marmoset; prefrontal; temporal; occipital
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INTRODUCTION |
Despite
Ramon y Cajal's original observations of variation in the morphology
of pyramidal cells in different species (Ramon y Cajal, 1894 ), the
isocortex was and still is considered by many to be uniform in
structure and composed of a repeated basic circuit (Szentagothai, 1975;
Creutzfeldt, 1977; Rockel et al., 1980; Eccles, 1984; Douglas et al.,
1989; Mountcastle, 1995). The application of new methods of analyses
(Elston, 2001) has revealed a remarkable degree of variation in
pyramidal cell morphology between different visual areas (Elston and
Rosa, 1997, 1998, 2000; Elston et al., 1999a,b; see also Lund et
al., 1993). In addition, cells in the macaque prefrontal cortex (PFC)
are considerably more branched and more spinous than those in the
occipital, parietal, and temporal lobes (Elston, 2000). The highly
modified phenotype found in the PFC has been interpreted as being
essential in determining the integration of diverse inputs (Elston,
2000) reportedly necessary for executive cortical function
(Goldman-Rakic, 1999). However, it remains to be determined whether
human's ability to perform complex cognitive functions is solely
attributable to the increase in the number of cortical cells and areas
or whether the human PFC pyramidal cell differs from that of other
species. To evaluate the possibility that the pyramidal cell in the PFC
of humans may differ from that in other primates, we injected cells in
corresponding cortical regions of the New World marmoset monkey
(Callithrix jacchus), the Old World macaque monkey
(Macaca fascicularis), and human. We found marked
differences in the pyramidal cell phenotype between sensory,
sensory-association, and executive cortex in humans. Moreover, we found
clear differences in the pyramidal cell phenotype in corresponding
brain regions between monkeys and humans.
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MATERIALS AND METHODS |
Cell morphology was studied in primate species characterized by
brains of markedly different size and degree of gyrencephalization (Fig. 1a-c). The cortical
areas studied included the second visual area (V2), the ventromedial
region of the inferior temporal cortex (Brodmann's area 21 of humans,
TEa of macaques, and ITr of marmosets), and the anterior
frontal lobe (Brodmann's area 10). Cortical areas were identified
based on previously published electrophysiological, connectional,
myeloarchitectonic, and cytoarchitectonic studies (Brodmann, 1907,
1909; Walker, 1940; Seltzer and Pandya, 1978; Preuss and Goldman-Rakic,
1991; Sereno et al., 1995; Rosa et al., 1997; Elston et al., 1999b).
Human tissue was obtained 2 hr postmortem from the left hemisphere of a
48-year-old normal male and immersed in 4% paraformaldehyde for 24 hr.
Macaque prefrontal cortex was derived from the left hemisphere of a
10-year-old male, whereas occipital and temporal cortex were taken from
the left hemispheres of 18-month-old males (AM1 and DM4, respectively)
(Elston and Rosa, 1998; Elston et al., 1999a). Marmoset PFC was taken
from an 18-month-old male (M908), the temporal lobe was taken from the
left hemisphere of 24- to 28-month-old males (BS10 and ML7), and the
occipital cortex was taken from the left hemispheres of 24- to
27-month-old males (BS10 and CJ715) (Elston et al., 1999b). Monkeys
were overdosed by lethal injection of sodium pentobarbitone and were
perfused intracardially with 4% paraformaldehyde.
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Figure 1.
Scale images of the human
(a), macaque (b), and
marmoset (c) brains showing the relative
differences in size and gyrencephalization between species. Note the
difference in the size of the cortical lobes. The frontal lobe in
humans comprises a greater proportion of the entire cortex than in
macaque or marmoset monkeys.
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Sections (250 µm) cut tangential to the cortical surface with the aid
of a vibratome were prelabeled with 4,6-diamidino-2-phenylindole (D9542; Sigma, St. Louis, MO). By relating the tangential sections to
traditional transverse sections we were able to identify the border
between layers III and IV. In addition, by focusing through the
thickness of the tangential slice, the cytoarchitectural differences between these layers were readily distinguished, enabling the identification and injection of cells at the base of layer III [Elston
and Rosa (1997), their Fig. 3]. Furthermore, in each case neurons were
also injected in other sections in each series, allowing the
identification of all layers (our unpublished results). Cell injection methodology has been described in detail previously (Buhl and
Schlote, 1987; Einstein, 1988; Elston and Rosa, 1997). Briefly, cells
were injected with Lucifer yellow (8% in 0.1 M Tris
buffer, pH 7.4) by continuous current. After injection of neurons, the
sections were first processed with an antibody to Lucifer yellow
[1:400,000 in stock solution: 2% bovine serum albumin (A3425; Sigma),
1% Triton X-100 (30632; BDH Chemicals, Poole, UK), and 5%
sucrose in 0.1 M phosphate buffer] and then with a biotinylated species-specific secondary antibody (1:200 in stock solution; RPN1004; Amersham Pharmacia Biotech, Little Chalfont, UK), followed by a biotin-horseradish peroxidase complex (1:200 in
phosphate buffer; RPN1051; Amersham). 3,3'-diaminobenzidine (D8001;
Sigma) was used as the chromogen.
The branching pattern of cells was determined by counting the number of
dendritic branches that intersected with concentric circles (centered
on the cell body) with increasing radii (25 µm increments) (Sholl,
1953). Dendritic field areas were determined by calculating the area
contained within a polygon joining the outermost distal tips of the
basal dendrites (Elston and Rosa, 1997). The density of spines on the
dendrites of pyramidal cells was determined by counting the number of
spines per 10 µm increment of 20 horizontally projecting dendrites of
different cells in each cortical area (Valverde, 1967). The total
number of spines found in the "average" pyramidal cell basal
dendritic arbor was calculated by multiplying the average number of
spines of a given portion of dendrite by the average number of branches
for the corresponding region, over the entire dendritic arbor (Elston, 2001).
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RESULTS |
Three hundred and forty-four layer III pyramidal
cells were included for analyses. Various aspects of cell morphology
varied independently, including the branching patterns and spine
densities of the dendrites. From Figure 2a it can be seen
that the maximum number of dendritic branches for any distance from the
cell body differed according to the cortical region and species (Table
1). Statistical analyses revealed that
all within-species between-region comparisons were significantly
different (p < 0.05), as were all within-region
between-species comparisons. Integration of the areas under the curves
revealed a consistent trend: cells in humans were more branched than
those in macaques, which were more branched than those in marmosets,
for any given cortical region. Cells in the frontal lobe of humans had
approximately one-third more dendritic branches than those in macaques
and twice as many as those in marmosets. Moreover, human prefrontal
cells were the most branched of all cells studied. In addition, these
data show a trend for more branched cells with progression from
occipital to temporal and prefrontal cortex in both humans and
macaques. Data for the marmoset, however, do not comply with this
trend. Instead, cells in the prefrontal cortex of the marmoset were
considerably less branched than those in its temporal lobe (ITr).
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Figure 2.
Plots of the number of dendritic branches
(a), areas (b), and
spine densities (c) of the basal dendritic arbors
of layer III pyramidal cells sampled in the occipital
(top), temporal (middle), and prefrontal
(bottom) cortex of humans (black),
macaques (dark gray), and marmosets (light
gray).
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Comparison of branching patterns with the size of the dendritic arbors
(Fig. 2b, Table 1) revealed no consistent correlation between the two variables. Moreover, comparison of the size of cells
revealed that they are not necessarily correlated with brain size. An
ANOVA (F(343) = 218; p < 0.0001) and post hoc Fisher's PLSD tests
(p < 0.05) revealed most comparisons of arbor
size to be significantly different. However, there was no significant difference between the size of cells in the temporal lobe of macaques, the frontal lobe of marmosets, and the occipital lobe of
humans. Nor was there any significant difference in the size of
cells in the frontal lobe of humans and macaques.
To estimate how many excitatory inputs may be sampled by individual
cells, we determined the number and distribution of spines within the
dendritic arbors of cells in the occipital, temporal, and prefrontal
cortex. Over 47,000 individual spines were reconstructed from 180 dendrites of different cells. In all three cortical regions studied,
spine density was highest in humans, followed by macaques, and then
marmosets (Fig. 2c, Table 1). A two-way repeated-measures ANOVA of the entire data set revealed spine densities to be
significantly different between cortical regions and/or species
(F(3258) = 188; p < 0.0001). Post hoc two-way repeated-measures ANOVAs revealed that, with the exception of cells in the human temporal and prefrontal cortex, all within-species regional comparisons were significantly different (p < 0.001). Within-region
between-species comparisons revealed significant differences
(p < 0.001), except for cells in the occipital
cortex of humans and macaques and cells in the temporal cortex of
humans and macaques. By combining the data on branching patterns and
spine density, we were able to estimate the number of spines in the
basal dendritic arbor of the average cell in each area. These
calculations revealed that cells in the PFC of humans and macaques
(15,138 and 8766, respectively) were considerably more spinous than
those in the temporal lobe (12,700 and 7260, respectively) (Fig. 3). In
marmosets, however, cells in the frontal lobe (3983) were considerably
less spinous than those in the temporal lobe (5176). In all three
species, cells in the temporal lobe were more spinous than those in the
occipital lobe (human, 2417; macaque, 1139; marmoset, 1240).
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DISCUSSION |
The present study shows that pyramidal cell morphology varies
markedly between cortical regions in different anthropoid genera. These
data extend previous findings of systematic differences in the
pyramidal cell phenotype in the monkey cortex and reveal interareal
differences in pyramidal cell morphology in the human cortex. In
conjunction, the results provide substantial evidence for the thesis
that pyramidal cells, and the circuits they form, are specialized for
their functional requirements.
Methodological considerations
Data in the present study were, in the case of monkeys, sampled
from different animals of varying developmental ages. As both dendritic
processes and spines atrophy with aging (Scheibel et al., 1975; Lund et
al., 1977; Huttenlocher, 1979; Bourgeois and Goldman-Rakic, 1993;
Anderson and Rutledge, 1996; Jacobs et al., 1997), some interareal
variation in the pyramidal cell phenotype reported here may be
attributable to sampling error. However, in the macaque monkey, the
most complex spinous cells were observed in the PFC of the oldest
animal, which would have been subject to the greatest spine loss and
dendritic regression. In the marmoset monkey, data from the PFC was
sampled from a slightly younger animal than those from which occipital
and temporal lobe data were sampled. Thus, it may be argued that
prefrontal cells had not yet reached their peak, whereas those in the
occipital and temporal cortex had done so (i.e., peak spine density in
the PFC may occur at a later developmental age than in the occipital
and temporal cortex). Although we are unaware of any published data on
the age at which the peak spine density is reached in the marmoset occipital, temporal, and prefrontal cortex, peak spine density in both
the occipital cortex and prefrontal cortex of humans and macaques is
reached by ~1.5 years of age (Huttenlocher, 1979; Bourgeois et al.,
1994; Anderson and Rutledge, 1996). As the marmoset prefrontal data
were sampled from an animal that was 18 months of age, it is likely
that peak spine density had already been reached.
Phenotypic variation and cell function
Various aspects of cell structure are reportedly critical in
determining the subcellular, cellular, and systems function of neurons.
Differences in the size and number of branches in the dendritic arbors
of cortical pyramidal neurons affect the total number of spines
contained within, reflecting putative differences in the number of
excitatory inputs received by individual cells (Elston and Rosa, 1997,
1998; Elston et al., 1999a,b; Elston, 2000). Varying spine densities
reported on the basal dendrites may also affect electrical and
biochemical compartmentalization, cooperativity between inputs, and
shunting inhibition (Koch et al., 1982; Shepherd et al., 1985; Rall and
Segev, 1987; Shepherd and Brayton, 1987; Koch and Zador, 1993; Mainen,
1999). In addition, differences in the total length of, number of
branches in, and diameters of the dendrites determine the cable
properties (Rall, 1959), the degree of nonlinear compartmentalization
(Rall, 1964; Koch et al., 1982), and the propagation of potentials
(Stuart and Häusser, 1994; Spruston et al., 1995; Markram et al.,
1997; Vetter et al., 2001) within the arbor (for review, see Rall et al., 1992; Stuart et al., 1997; Koch, 1999; Mel, 1999; Spruston et al., 1999; Häusser et al., 2000). Modeling studies have also shown that a greater potential for electrical compartmentalization in
highly branched dendritic arbors may result in a significant increase
in the capacity for learning and memory of a neuron by increasing the
representational power of the cell (Poirazi and Mel, 2001). Thus, it
appears likely that regional differences in pyramidal cell morphology
contribute to area-specific aspects of cellular and systems function
such as discharge properties and contrasting synaptic plasticity
(Fuster and Alexander, 1971; Kubota and Niki, 1971; Fuster and Jervey,
1981; Ashford and Fuster, 1985; Miyashita and Chang, 1988; Funahashi et
al., 1989; Murayama et al., 1997). As a logical extension, species
differences in pyramidal cell morphology (for corresponding brain
regions) are likely to contribute to species-specific differences in
cortical function. In particular, cells in the human PFC potentially
compartmentalize a greater number of inputs within their dendritic
arbors than those in the PFC of the macaque, and those in the PFC of
macaque compartmentalize more than those in the PFC of the marmoset.
Moreover, cells in the human PFC may integrate a greater diversity of
inputs than those in other species.
On brain size and heterogeneity of the pyramidal
cell phenotype
The present results clearly show that the size of and the number
of branches and spines in the basal dendritic arbors of pyramidal cells
may vary independently of each other. Some of these variables may be
correlated with brain size, but others may not. For example, among the
areas studied here, spine density appears to be correlated with brain
size: spine density was consistently higher in humans compared with
macaques and higher in macaques compared with marmosets for any of the
given brain regions. However, the size of the cells does not
necessarily correlate with brain size: cells in the occipital and
temporal lobe of the marmoset were larger than those in corresponding cortical regions in the macaque. Moreover, pyramidal cells in different
cortical regions and/or species are not merely scaled versions of the
same type but are structurally different (Elston and Jelinek, 2001;
Jelinek and Elston, 2001). In addition, the total number of spines in
the basal dendritic arbor of the average cell in each cortical region
did not correlate with brain size. Whereas cells in the PFC of humans
and macaques were considerably more spinous than those in the temporal
and occipital lobes, those in the PFC of marmosets were less spinous
than those in the temporal cortex (Fig.
3). Marmoset PFC occupies a smaller
fraction of its isocortex compared with the PFC of humans and
macaques, and comprises fewer cortical areas (Gebhard et al.,
1995). In contrast, the marmoset temporal lobe is relatively expansive
and appears to be highly specialized for visual processing (Rosa,
1997). The second visual area is reportedly homologous across species
(Sereno et al., 1995; Rosa et al., 1997), being a phylogenetically old cortical area (Kaas, 1992). Thus, the number of spines in the basal
dendritic arbor of the average pyramidal cell in each area appears to
reflect both the level of processing (sensory, sensory association, or
executive function) and the extent to which a particular region has
become specialized for the particular function.
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Figure 3.
Plot of the estimates of the total number of
spines in the basal dendritic arbor of the "average" pyramidal cell
in the occipital, temporal, and prefrontal cortex of marmosets
(light gray), macaques (dark gray), and
humans (black). These calculations revealed that cells
in the prefrontal cortex of humans and macaques (15,138 and 8766, respectively) are considerably more spinous than those in the temporal
lobe (12,700 and 7260, respectively). In marmosets, however, cells in
the prefrontal cortex (3983) were less spinous than those in the
temporal lobe (5176).
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Conclusions
The present results show that the enlargement of the cortex in
higher primates has not occurred solely through the addition of new
cortical areas of similar circuitry. Instead, the results suggest that
pyramidal cell morphology in marmosets, macaques, and humans is
specialized for their functional requirements in any given cortical
region. In particular, prefrontal pyramidal cells have become more
branched and spinous during the evolution of the PFC in higher
primates, facilitating specialized cortical functions such as
comprehension, perception, and planning. Differences in the branching
structure of prefrontal pyramidal cells, and the number of spines they
contain, are not correlated with brain size, but reflect fundamental
differences in circuitry between species.
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FOOTNOTES |
Received April 12, 2001; revised June 8, 2001; accepted June 11, 2001.
This work was supported by a C. J. Martin Fellowship (G.N.E.), by
a Comunidad Autonoma de Madrid Fellowship (R.B.-P.) (01/07f2/2000), by
Grant 990007 from the Australian National Health and Medical Research
Council, and by Dirección General de Investigación Cientifica y Técnica Grant PM99-0105 from Spain. We thank Prof. Pettigrew and Drs. Rosa and Muñoz for suggestions for improving this manuscript. Marmoset PFC was kindly supplied by Dr. Rosa.
Correspondence should be addressed to Guy Elston, Vision, Touch, and
Hearing Research Center, Department of Physiology and Pharmacology, The
University of Queensland, Queensland, 4072, Australia. E-mail:
G.Elston{at}vthrc.uq.edu.au.
This article is published in
The Journal of Neuroscience, Rapid Communications Section,
which publishes brief, peer-reviewed papers online, not in print. Rapid
Communications are posted online approximately one month earlier than
they would appear if printed. They are listed in the Table of Contents
of the next open issue of JNeurosci. Cite this article as:
JNeurosci, 2001, 21:RC163 (1-5). The
publication date is the date of posting online at
www.jneurosci.org.
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ABSTRACT
INTRODUCTION
