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Pyramidal neurons of granular prefrontal cortex of the galagoComplexity in evolution of the psychic cell in primates.

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THE ANATOMICAL RECORD PART A 285A:610 – 618 (2005)
Pyramidal Neurons of Granular
Prefrontal Cortex of the Galago:
Complexity in Evolution of the
Psychic Cell in Primates
GUY N. ELSTON,1* ALEJANDRA ELSTON,1 VIVIEN CASAGRANDE,2 AND
JON H. KAAS3
1
Vision, Touch and Hearing Research Centre, School of Biomedical Sciences &
Queensland Brain Institute, University of Queensland, Queensland, Australia
2
Department of Cell and Developmental Biology, Vanderbilt University,
Nashville, Tennessee
3
Department of Psychology, Vanderbilt University, Nashville, Tennessee
ABSTRACT
Typically, cognitive abilities of humans have been attributed to their
greatly expanded cortical mantle, granular prefrontal cortex (gPFC) in
particular. Recently we have demonstrated systematic differences in microstructure of gPFC in different species. Specifically, pyramidal cells in adult
human gPFC are considerably more spinous than those in the gPFC of the
macaque monkey, which are more spinous than those in the gPFC of
marmoset and owl monkeys. As most cortical dendritic spines receive at
least one excitatory input, pyramidal cells in these different species putatively receive different numbers of inputs. These differences in the gPFC
pyramidal cell phenotype may be of fundamental importance in determining the functional characteristics of prefrontal circuitry and hence the
cognitive styles of the different species. However, it remains unknown as to
why the gPFC pyramidal cell phenotype differs between species. Differences could be attributed to, among other things, brain size, relative size of
gPFC, or the lineage to which the species belong. Here we investigated
pyramidal cells in the dorsolateral gPFC of the prosimian galago to extend
the basis for comparison. We found these cells to be less spinous than those
in human, macaque, and marmoset. © 2005 Wiley-Liss, Inc.
Key words: striate; extrastriate; cortex; dendrite; spine; Lucifer
yellow
Pyramidal cells in the cerebral cortex vary in size,
branching pattern, spine density, and the total number
of dendritic spines (Lund et al., 1993; Elston and Rosa,
1997, 1998, 2000; Elston et al., 1999a, 1999b; Elston,
2000, 2003a; Jacobs et al., 2001). These structural differences are thought to influence sampling geometry,
compartmentalization of processing, cooperativity between inputs, and the total number of excitatory inputs
integrated within their arbors (for reviews, see Jacobs
and Scheibel, 2002; Elston, 2003b, 2003c). In addition,
marked differences have been reported in the patterns
of axon projections of pyramidal cells in different cortical areas and species (Bugbee and Goldman-Rakic,
1983; Preuss and Goldman-Rakic, 1991; Lund et al.,
1993).
©
2005 WILEY-LISS, INC.
In a series of studies, we have attempted to correlate the
relationship between pyramidal cell structure, patterns of
Grant sponsor: the J.S. McDonnell Foundation; Grant sponsor:
the Australian National Health and Medical Research Council.
*Correspondence to: Guy N. Elston, Vision, Touch and Hearing
Research Centre, School of Biomedical Sciences, University of
Queensland, Queensland, 4072, Australia. Fax: 61-7-33654522.
E-mail: [email protected]
Received 3 August 2004; Accepted 5 January 2005
DOI 10.1002/ar.a.20198
Published online 23 May 2005 in Wiley InterScience
(www.interscience.wiley.com).
PYRAMIDAL CELLS IN GALAGO PFC
Fig. 1. A: Photomicrograph of a sagittal section of the galago brain
illustrating, in particular, cytoarchitecture in the frontal and parietal lobes.
Higher-power micrographs highlight differences in the cytoarchitecture
between (B) granular prefrontal cortex, (C) premotor cortex, and (D) the
primary motor area.
connectivity, and function. These studies were focused
primarily in visual cortex, where a great deal is known
about the response properties of neurons and visual function. These studies revealed systematic differences in pyramidal cell structure in visual cortical areas, which parallel systematic differences in their function (for reviews,
see Elston, 2003b, 2003c). For example, there is a consistent trend for pyramidal cells of progressively more complex structure with anterior progression through occipitotemporal cortical areas, which parallel differences in their
functional complexity and discharge properties. Systematic differences in pyramidal cell structure in somatosensory, motor, and limbic cortex also parallel functional specializations of neurons contained within (Elston and
Rockland, 2002; Elston et al., 2005a).
In the present investigation, we extend our studies of
pyramidal cell structure in prefrontal cortex. Presently
available data reveal that pyramidal cells in adult human
granular prefrontal cortex (gPFC) are considerably more
branched and more spinous than those in gPFC of the
macaque monkey, which are more branched and more
spinous than those in gPFC of marmoset and owl monkeys. These data suggest that pyramidal cells in human
receive more excitatory inputs than those in the macaque
monkey and compartmentalize these inputs to a greater
degree. Thus, the functional capacity of the individual
cells is likely to be greater in human than in macaque-
611
Fig. 2. Photomicrograph of the lateral aspect of the brain of the
human, macaque monkey, marmoset monkey, owl monkey, and galago.
The extent of granular prefrontal cortex is represented by stipple. Scale
bar ⫽ 2 cm for human and 1 cm for all other species.
,greater in macaque than owl monkey, and so on (cf
Poirazi and Mel, 2001). These data led us to question how
specialization in pyramidal cell structure observed in extant species may have evolved. Presently available data in
humans, macaques, marmosets, and owl monkeys suggest
at least two possibilities. Differences in the gPFC pyramidal cell phenotype could vary between different primate
lineages; for example, highly complex pyramidal cell
structure may be restricted to simians or anthropoids.
Alternatively, the structural complexity of gPFC pyramidal cells may reflect the extent of gPFC expansion, irrespective of lineage.
In a bid to test these two possibilities, we studied pyramidal cell structure in the galago, a prosimian primate
with a well-developed gPFC (Fig. 1). The lorisiform prosimians, which include the galago, have been separated
from the simian lineage for over 50 million years (Martin,
1990). Importantly, the galago has a smaller granular
prefrontal cortex than that in the marmoset (Fig. 2)
(Preuss and Goldman-Rakic, 1991). Consequently, if pyramidal cells in the gPFC of the galago are less branched
and less spinous than those in the marmoset, the complexity of the gPFC pyramidal cell phenotype is likely to reflect
the relative expansion of gPFC. Alternatively, if pyramidal cells in the gPFC of the galago are more branched and
more spinous than those in the marmoset, other features
are likely to influence the cell phenotype.
MATERIALS AND METHODS
Galagos used in the present study (G1 and G2, 3.5 and
4 year old males, respectively) were the same as those
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ELSTON ET AL.
Fig. 3. Schematic of the galago brain and various cortical areas that
have been identified by cyto- and myelarchitectonic, connectional, and
mapping experiments. Note the motor areas that have been identified in
the frontal lobe, including the primary (M1), supplementary (SMA), premotor dorsal (PMD), premotor ventral (PMV) areas. Anterior to the arcuate sulcus lies the granular prefrontal cortex, which includes the region
of cortex extending from the frontal eye field (FEF) to the frontal pole.
Neurons were injected in gPFC in both cases; however, the exact
location in which neurons were injected varied slightly between galago 1
(G1) and galago 2 (G2). Modified from Kaas (2003).
used in a previous study (Elston et al., 2005b). Briefly,
animals were overdosed with sodium pentobarbitone and
perfused with 0.95% saline in PB (0.1 M phosphate buffer,
pH 7.2), followed by 4% paraformaldehyde in PB. Cortices
were flat-mounted and left in the 4% paraformaldehyde in
PB for 12 hr at 4°C. Blocks including the entire frontal
lobe were cut tangentially to the cortical surface and were
sectioned (250 ␮m) with the aid of a Vibratome. The region
corresponding to dorsolateral granular prefrontal cortex,
anterior and medial to the frontal eye field (Wu et al.,
2000; Wu and Kaas, 2003), was selected for study (Fig. 3).
Individual neurons were visualized under fluorescence excitation by first prelabeling the sections with 10⫺5 mol/L
4,6-diamidino-2-phenylindole (D9542; Sigma) in PB. Cells
were injected [8% Lucifer Yellow (L-0259; Sigma) in 0.1 M
Tris buffer; pH 7.4] at the base of layer III. Because of the
presence of a distinct granular layer (e.g., Fig. 1B) in the
PFC of the galago [by definition prefrontal cortex is granular (Brodmann, 1913)], it was relatively easy to identify
layer III and inject cells at the base of layer III. Three
criteria are used to determine that cells are injected at the
base of layer III. In the first instance, the unprocessed
serial tangential sections cut from the flat-mounted blocks
are placed on a black background and their color com-
pared: supragranular sections are much whiter than the
granular and infragranular sections. Second, the density
of cell bodies clearly differs between supragranular, granular, and infragranular sections when visualized under
UV excitation (e.g., see Fig. 3 of Elston and Rosa, 1997),
allowing distinction between these layers. Third, by injecting cells in successive sections, it is easy to distinguish
and identify the section that contains the granular layer
by cell type. In addition, the base of layer III is relatively
easily detected while injecting as the transition between
layers III and IV can be detected visually while injecting.
Following cell injection, the tissue was processed with
an antibody to Lucifer Yellow (LY) for 5 days at a concentration of 1:400,000 in stock solution [2% bovine serum
albumin (Sigma A3425), 1% Triton X-100 (BDH 30632),
5% sucrose in 0.1 mol/l phosphate buffer]. Anti-LY was
detected by a species-specific biotinylated secondary antibody (Amersham RPN 1004; 1:200 in stock solution for 2
hr), followed by a biotin-horseradish peroxidase complex
(Amersham RPN1051; 1:200 in 0.1 mol/l phosphate
buffer). Labeling was revealed using 3,3⬘-diaminobenzidine (DAB; Sigma D 8001; 1:200 in 0.1 mol/l phosphate
buffer) as the chromogen (for details of cell, filling, immunohistochemical processing, confirmation of the laminar
lacoation of injected neurons, and methods of quantification, see Elston and Rosa, 1997, 1998).
Cells were reconstructed from the 250 ␮m thick slices.
Neurons that had an unambiguous apical dendrite were
located at the base of layer III and had the complete basal
dendritic arbor contained within the section were drawn
with the aid of a camera lucida attachment coupled to a
Zeiss Axioplan microscope. A polygon joining the outermost distal tips of the basal dendrites was drawn over
each cell and the area contained within was determined
with the aid of NIH Image (Elston and Rosa, 1997). Complexity of the dendritic branching structure was quantified by Sholl analysis (Sholl, 1953). Spine density was
determined as a function of distance from the cell body to
the distal tips of the dendrites for complete reconstructions of 10 randomly selected horizontally projecting basal
dendrites of different pyramidal cells (e.g., Eayrs and
Goodhead, 1959; Valverde, 1967; Elston, 2001). Correction
factors used in Golgi studies when quantifying spines
(e.g., Feldman and Peters, 1979) were not used in the
present study as the DAB reaction product allows the
visualization of spines that issue from the underside of
dendrites. No distinction was made between the different
types of spines: stubby, mushroom, and thin spines were
all included in the counts. The tangential dimension of
somata was determined using standard features of NIH
Image. The total number of spines located in the basal
dendritic arbor of the average pyramidal cell was calculated by multiplying the average number of dendritic
branches per Sholl annul by the average spine density for
the corresponding annul and summing over all successive
annuls included in the dendritic arbor (see Elston, 2001).
RESULTS
Ninety-six neurons were injected at the base of layer III
in dorsolateral prefrontal cortex (59 in B1 and 37 in G2),
47 of which were included for analyses according to selection criteria outlined in the Materials and Methods section
(20 in G1 and 27 in G2). We made no attempt to determine
which prefrontal areas these cells were sampled from, but
it was likely that a large portion of them were sampled
PYRAMIDAL CELLS IN GALAGO PFC
613
Fig. 4. Photomicrographs of the basal dendritic arbors pyramidal cells injected with Lucifer Yellow at the
base of layer III in the dorsolateral granular prefrontal cortex that were processed for a light-stable DAB
reaction product. Scale bar ⫽ 50 ␮m.
anterior to the frontal eye field (FEF; Fig. 4). Data for
these cells was compared with those of the primary (V1),
second (V2), dorsolateral (DL), and inferotemporal (IT)
visual areas sampled in the same hemisphere of these
animals (Elston et al., 2005b).
Basal Dendritic Arbor Size
In galago 1, the average size of the basal dendritic
arbors of layer III pyramidal cells was 91.3 ⫾ 4.97 ⫻ 103
␮m2 (mean ⫾ standard error) and that in galago 2 was
118 ⫾ 4.32 ⫻ 103 ␮m2 (Fig. 5). In both animals, the arbors
of layer III pyramidal cells in gPFC were larger than those
of cells in V1, V2, and DL. One-way analyses of variance
revealed these differences to be significant in both G1
(F(4,85) ⫽ 17.8; P ⬍ 0.001) and G2 (F(3,71) ⫽ 78.8; P ⬍
0.001).
Complexity of Basal Dendritic Arbors
Cells in PFC had a peak dendritic complexity of 27.1 ⫾
3.49 (mean ⫾ SEM) in G1 and 27.9 ⫾ 3.67 in G2 (Fig. 5).
Repeated-measures ANOVAs revealed the branching patterns of cells to be significantly different between cortical
areas in G1 (intercept, F(1,81) ⫽ 700, P ⬍ 0.001; cortical
area, F(4,81) ⫽ 32.8, P ⬍ 0.001) and G2 (intercept, F(1, 68) ⫽
1351, P ⬍ 0.001; cortical area, F(3,68) ⫽ 53.2, P ⬍ 0.001).
The number of branches in the basal dendritic arbors of
neurons in PFC was higher than that in V1, V2, and DL
but lower than that in IT (Fig. 5).
Spine Densities of Basal Dendrites
The peak average spine density in G1 was 15.7 ⫾ 3.02
(mean ⫾ SD) at a distance of 101–110 ␮m from the cell
body. That in G2 was 16.0 ⫾ 2.79 at the same distance
from the cell body (Fig. 5). Repeated-measures ANOVAs
revealed a significant difference in the distribution of
spines along the dendrites of pyramidal cells in G1 (intercept, F(1,32) ⫽ 707.8, P ⬍ 0.001; cortical area, F(4,32) ⫽
57.3, P ⬍ 0.001) and G2 (intercept, F(1,36) ⫽ 1.62 ⫻ 103,
P ⬍ 0.001; cortical area, F(3,36) ⫽ 112.3, P ⬍ 0.001).
Posthoc analysis revealed that spine density was higher in
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ELSTON ET AL.
Fig. 5
PYRAMIDAL CELLS IN GALAGO PFC
615
Fig. 6. Estimates of the total number of spines in the basal dendritic
arbor of the average pyramidal cell in granular prefrontal cortex in the
young mature adult galago, marmoset monkey, macaque monkey, and
human. Note that there is a trend for a systematic increase in the total
number of spines in the basal dendritic arbor of pyramidal cells with
increasing size of gPFC. Individual values obtained from G1 and G2 are
illustrated as individual columns headed galago (left and right column,
respectively). Relative interindividual differences in the pyramidal cell
phenotype in gPFC of the galago may be attributable to differences in
the age of the animals (3.5 vs. 4 years old), the differing gender of the
animals, or reflect natural variation or differences in the region from
where cells were sampled. Data from Aotus (Elston, 2003a) are not
compared here because of the marked difference in the age of the
animal from which those data were sampled.
PFC than all other areas sampled in both G1 and G2. By
multiplying the spine density, averaged over 25 ␮m segments of dendrite, by the number of branches recorded
over the corresponding segment, we were able to estimate
the total number of dendritic spines in the basal dendritic
arbor of the average layer III pyramidal neuron. In galago
1, the average cell had 3,219 spines in its basal dendritic
arbor, which in galago 2 had 3,759 spines (Fig. 6).
ramidal cells has been quantified and compared with that
of pyramidal cells in other cortical areas sampled from the
same cortical hemisphere. This comparative approach has
revealed new insights into specialization of the pyramidal
cell phenotype in the granular prefrontal cortex of different primate species. The results of earlier studies suggested that the highly complex phenotype reported in
gPFC of humans and macaque monkeys may be restricted
to higher primates. The present data are consistent with
this theory. By quantifying the differences in pyramidal
cell structure in different species, we are gaining new
insight into the thinking of Ramon y Cajal (1893) when,
based on his comparative data, he concluded that the
pyramidal cell is the “psychic cell.” Our findings suggest
that specializaton of pyramidal cell phenotype may be an
important factor during the evolution of increasingly complex intellect in primates.
How these differences in cortical circuitry may influence
cognitive style, particularly that in primates, remains to
be determined. However, there are multiple converging
lines of evidence to suggest a parallel between pyramidal
cell structure and cognitive ability. For example, decline
in cognitive ability with aging is paralleled by a decrease
in dendritic branching and spine loss (Scheibel et al.,
1975, 1976; de Brabander et al., 1998; Page et al., 2002)
and the relatively impoverished structure of pyramidal
cells in the brains of individuals with Down syndrome and
fragile X parallel cognitive abilities (Marin-Padilla, 1976;
Huttenlocher, 1979; Suetsugu and Mehraein, 1980;
Takashima et al., 1981; Leuba, 1983; Hinton et al., 1991;
Dierssen et al., 2002; for review, see Kaufmann and
Moser, 2000; Dierssen et al., 2003). In addition, pyramidal
cells in experimental animals reared in an enriched environment have more complex structure, and the animals
perform better on behavioral tasks, than animals that
Somal Areas
The average size of the somata of layer III pyramidal
cells in G1 was 202 ⫾ 44 ⫻ 103 ␮m2 (mean ⫾ standard
deviation), and that in G2 was 247 ⫾ 35 ⫻ 103 ␮m2, being
on average larger than those of cells in other areas (Fig. 5).
One-way analyses of variance revealed these differences
to be significant in both G1 (F(4,85) ⫽ 18.02; P ⬍ 0.001) and
G2 (F(3,71) ⫽ 188; P ⬍ 0.001). Posthoc analysis revealed
that cells in PFC had significantly larger somata than
those in V1, V2, DL, and IT.
DISCUSSION
The present study is one of several morphological investigations in which the structure of prefrontal cortical py-
Fig. 5. A: Frequency histograms of the size of the basal dendritic
arbors of layer III pyramidal neurons in the dorsolateral prefrontal cortex
(PFC; black) dorsolateral visual area (DL; blue), second visual area (V2;
green), and the primary visual area (V1; orange). B: Plots of the number
of dendritic intersections of the basal dendrites of pyramidal neurons as
determined by Sholl analysis. C: Plots of the number of dendritic spines
per 10 ␮m segment of dendrite, as a function of distance from the cell
body, in the basal dendritic arbors of layer III pyramidal neurons. D:
Frequency histograms of somal areas of pyramidal neurons. Error
bars ⫽ standard deviations.
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ELSTON ET AL.
Fig. 8. Graph illustrating the size of granular prefrontal cortex relative
to the surface area of the entire cortex of the human, chimpanzee,
gibbon, mandril, baboon, macaque monkey, long-tailed monkey, capuchin monkey, marmoset monkey, black lemur, dwarf lemur, fruit bat,
dog, cat rabbit, hedgehog, armadillo, and opossum (taken from Brodmann, 1913). Regression analysis revealed that exclusion of the human
(long dashed line) and the human and chimpanzee (short dashed line)
result in slopes of lesser gradient than regression analysis of all species
(solid black line), suggesting disproportionate expansion of gPFC in
human and chimpanzee.
Fig. 7. Graphs illustrating differences in the number of dendritic
branches (top) and spines density (bottom) in the basal dendritic trees of
layer III pyramidal cells in granular prefrontal cortex of human (red),
macaque monkey (orange), marmoset monkey (blue), and the galago
(cream). Data taken from Elston et al. (2001) and the present results.
have been reared in a nonenriched environment (e.g.,
Greenough et al., 1973, 1985; Dierssen et al., 2002; for
reviews, see Harris, 1999; Kintsova and Greenough, 1999;
Wooley, 1999; Elston and DeFelipe, 2002).
While there is a growing body of evidence to suggest a
link between pyramidal cell structure and behavioral abilities, less is known as to how aspects of pyramidal cell
structure, such as the size or branching pattern of their
dendritic arbors, or their spine density, may directly affect
cellular and systems function. Our estimates of the number of spines in the basal dendritic trees of layer III pyramidal cells reveal that those in gPFC of the galago are 7
times more spinous than those in its V1, those in macaque
gPFC are 17 times more spinous than those in galago V1,
and those in human gPFC are on average 30 times more
spinous than those in galago V1 (present results; Elston et
al., 2001), making it highly likely that cells in these different species receive different numbers of asymmetrical
(excitatory) inputs (for reviews, see Elston, 2002, 2003b,
2003c; Jacobs and Scheibel, 2002). In addition, differences
in the number of branches may influence the degree to
which processing of these inputs is compartmentalized
within the dendritic arbors of pyramidal cells in gPFC of
the different species. More spinous cells such as those in
gPFC of human, for example, are more branched than the
less spinous cells in galago gPFC, imparting different
functional capabilities: cells with more dendritic branches
have a greater capacity than cells with fewer dendritic
branches (e.g., Poirazi and Mel, 2001). Differences in the
branching structure also influence the propagation of in-
puts to the soma (Vetter et al., 2001). Furthermore, circuits composed of neurons with complex branching pattern such as those observed in human gPFC, which are
also characterized by high spine density (peak of 32.5 ⫾
1.64 spines per 10 ␮m), have a greater potential for plastic
change than circuits composed of less branched cells such
as those in galago gPFC with lower spine density (16.0 ⫾
2.78) (Stepanyants et al., 2002). Differences in the dendritic structure of pyramidal cells in gPFC of different
primate species, coupled with differences in patterns of
intrinsic connectivity (Bugbee and Goldman-Rakic, 1983;
Preuss and Goldman-Rakic, 1991), may influence the potential for resonant excitation via recurrent collaterals,
which is believed to be important in mnemonic processing
(for reviews, see Yuste and Tank, 1996; Koch, 1997;
Häusser et al., 2000; Magee, 2000; Euler and Denk, 2001;
Segev et al., 2001; Wang, 2001).
Given the variation in the structural complexity of the
mature pyramidal cell phenotype in gPFC of different
species (Fig. 7), and the behavioral implications of these
differences, it was natural to ask why they occur. One
interpretation is that pyramidal cells have become more
spinous during expansion of gPFC (Fig. 8). The present
data are consistent with this interpretation. For example,
gPFC has a surface area of 148 mm2 in marmoset, 1,733
mm2 in macaque, and 39,287 mm2 in man (Brodmann,
1913; for translation, see Elston and Garey, 2004), and
complexity of pyramidal cell structure increases through
these species. These data may be interpreted as evidence
that pyramidal cell structure necessarily becomes more
complex during cortical expansion. However, this is not
the case. The primary visual area has also undergone
considerable expansion in size in primates. That in the
macaque (1,102 mm2) is considerably larger than that in
galago (343 mm2), which is larger than that in the marmoset (198 mm2) (Brodmann, 1913), yet the number of
spines found in the arbors of pyramidal cells in these
species does not follow a similar progression [735, 556,
and 699, respectively; the first number is the average from
PYRAMIDAL CELLS IN GALAGO PFC
animals RM12, RM13, MF1, and MF2 (Elston et al.,
2004a); the second number is the average from animals
G1 and G2 (Elston et al., 2004b); the third number is the
average from animal BS10 (Elston et al., 1999b)]. Thus, it
appears as though circuitry or, more specifically, pyramidal cell structure has evolved differently in V1 and gPFC.
In future studies, it will be worthwhile to study the apical
dendrites of these neurones, as well as pyramidal cells in
other cortical layers (e.g., Elston and Rosa, 2000).
ACKNOWLEDGMENTS
The authors thank Iwona Stepniewska, Laura Trice,
Laura Ferris, and Brendan Zeitsch for technical help.
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