1 Vision, Touch and Hearing Research Centre, Department of Physiology and Pharmacology, School of Biomedical Sciences, The University of Queensland, Queensland 4072, Australia and 2 Instituto Cajal (CSIC), Avda Dr Arce, 37, 28002, Madrid, Spain
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Abstract |
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Key Words: association cognition dendritic spine emotion intracellular injection Lucifer Yellow Sholl
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Introduction |
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The results of recent studies of pyramidal cell structure provide evidence for the latter hypothesis: there is marked variation in the structure of pyramidal cells, the most ubiquitous neuron in cortex, between different cortical areas (Lund et al., 1993; Elston et al., 1999a
, b
; Jacobs et al., 2001
). In macaque, marmoset and owl monkeys there is a progressive increase in the complexity of pyramidal cell structure through the primary visual area (V1), the second visual area (V2), and inferotemporal (IT) cortex (Elston and Rosa, 1998
; Elston et al., 1999a
,b
; Elston, 2003b
). Likewise, pyramidal cells in visual areas of the parietal lobe have more complex structure than those in V1 or V2 (Elston and Rosa, 1997
; Elston et al., 1999b
). There is also a progressive increase in the complexity of pyramidal cell structure through somatosensory areas 3b, 5 and 7 (Elston and Rockland, 2002
). Granular prefrontal cortex (gPFC) in higher primates, which has undergone dramatic expansion (Brodmann, 1913
; for a translation, see Elston and Garey, 2004
), is composed of highly branched and spinous pyramidal cells: macaque prefrontal pyramidal cells have, on average, over 16 times more dendritic spines than those in its V1 and those in human prefrontal cortex have 23 times more spines than those in macaque V1 (Elston, 2000
; Elston et al., 2001
). As each dendritic spine receives at least one excitatory input (for reviews, see Harris, 1999
; Elston and DeFelipe, 2002
), regional differences in the number of spines in the dendritic arbours of neurons suggest that they integrate different numbers of inputs. It has been argued that regional specializations in pyramidal cell structure reflect fundamental differences in patterns in cortical circuitry, which shape its functional abilities (for reviews, see Elston, 2002
, 2003a
; Jacobs and Scheibel, 2002
). Here we focus on pyramidal cell structure in anterior and posterior cingulate areas of the macaque monkey in a bid to gather more information regarding the underlying trends that result in specialization of the pyramidal cell phenotype and how they relate to cortical function.
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Materials and Methods |
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Tissue was taken from the caudal region of the cingulate gyrus (corresponding to Brodmann's area 23), the rostral portion of the cingulate gyrus (corresponding to Brodmann's area 24), the rostral third of the ventral bank of the superior temporal sulcus (IT; cytoarchitectural area TEa of Seltzer and Pandya, 1978; TEad(s) of Yukie, 1997
; PIT of Felleman and Van Essen, 1991
) and the occipital operculum (V1 or area 17 of Brodmann) of the left hemisphere (Fig. 1). Blocks were prepared as flattened specimens by unfolding the tissue, removing the white matter and postfixing between glass slides. Sections (250 µm, tangential to the cortical surface) were cut with the aid of a vibratome and prelabelled with the fluorescent dye 4,6 diamidino-2-phenylindole (DAPI; Sigma D9542). Individual cell bodies can be visualized in DAPI labelled tissue with the aid of UV excitation. Differences in neuronal packing density and cell type can be identified in DAPI-labelled sections in much the same way as in preparations labelled for Nissl-substance or thionin (see Fig. 3 of Elston and Rosa, 1997
). Distinction was easily made in granular cortex between the cell dense layer IV and adjacent supra- and infragranular layers by (i) calculating the depth of the series of 250 µm tangential sections (from cortical surface to white matter) and comparing with that in adjacent tissue cut in the transverse plane and (ii) studying the morphology of injected neurons (spiny stellate cells are restricted to layer IV and are rarely present in supra- and infragranular layers). [Here we use the terminology of Hassler (1966)
in preference to that of Brodmann (1909
; translated by Garey, 1994
) for reasons outlined in Elston and Rosa (1997)
and Casagrande and Kaas (1994)
.] In the case of posterior dysgranular cingulate cortex, we calculated from our own preparations, and previous studies (e.g. Figure 3 of Nimchinsky et al., 1996
), that the base of layer III is located approximately half way between the cortical surface and the white matter, corresponding to our third successive 250 µm tangential section.
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Results |
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Pyramidal Neurons in M. fasicularis
Basal Dendritic Arbour Size
The size of the basal dendritic arbours of pyramidal cells in anterior cingulate were larger (>50%) than those in posterior cingulate (Table 1; Figs 3 and 4). Moreover, cells in both anterior and posterior cingulate were larger than those in IT and V1 (Table 1; Figs 3 and 4). A one way analysis of variance (ANOVA) revealed significant differences (P < 0.001) in the sizes of the basal dendritic arbours of pyramidal cells these four cortical areas in both MF1 [F(3,103) = 115.1] and MF2 [F(3,129) = 117.2]. Post hoc Scheffe tests revealed significant differences (P < 0.05) in the size of the basal dendritic arbors of layer III pyramidal cells between cingulate (anterior and posterior) cortex and both IT and V1 in both cases MF1 and MF2.
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Pyramidal cells in anterior cingulate had more branches in their basal dendritic arbours than those in posterior cingulate (Fig. 5). In addition, pyramidal cells in both anterior and posterior cingulate had more branches than those in IT and V1 (Fig. 5; Table 2). Analysis of variance revealed these differences to be significant [P < 0.001; MF1, intercept F(1,118) = 2558, cortical area F(3,118) = 99.16; MF2, intercept F(1,131) = 2826, cortical area F(3,131) = 98.63]. Post hoc Scheffe tests revealed that, in both MF1 and MF2 monkeys, cells in anterior cingulate were significantly more branched than those in IT. In addition, those in both anterior and posterior cingulate were significantly more branched than those in V1 (P < 0.05).
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In order to determine possible differences in the density and distribution of dendritic spines we drew and tallied >16 000 spines from 20 horizontally projecting basal dendrites of different neurons in each cortical area. From Figure 6 it is clear that the density of spines varied markedly for pyramidal cells in the different areas. Pyramidal cells in anterior cingulate had higher average peak spine density than those in posterior cingulate (Fig. 6; Table 3). The average peak spine density of cells in IT was similar to that in our previous studies (Elston et al., 1999a), being greater than that of cells in cingulate cortex (Fig. 6; Table 3). The average peak spine density of cells in V1 was similar to that reported in our previous studies (Elston and Rosa, 1997
, 1998
), being considerably lower than that in the other cortical areas (Fig. 6; Table 3). A repeated measures ANOVA (cortical area x distance from soma x spine density), revealed a significant difference in the distribution of spines [intercept F(1,76) = 1463, cortical area F(3,76) = 93.3; P < 0.001]. Post hoc Scheffe tests revealed all between area comparisons to be significantly different (P < 0.05), except that between area 24 and IT. By combining data from the Sholl analyses with that of spine densities we were able to determine an estimate for the total number of dendritic spines in the basal dendritic arbour of the average pyramidal neuron in each area (see Elston, 2001
). The average neuron in anterior cingulate had considerably more spines in its basal dendritic arbour than that in posterior cingulate (6825 and 4357 spines, respectively). The average cell in IT had 6170 spines, whereas that in V1 had 855 spines in its basal dendritic arbour.
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Cell bodies were drawn in the plane tangential to the cortical surface, and plotted in Figure 7. In contrast to the size of the basal dendritic arbours, the somata of cells in layer III of anterior cingulate were, on average, smaller than those in posterior cingulate (Table 4). In addition, somata in both regions of the cingulate cortex were larger than those in IT and V1 (Table 4). Statistical analysis of the size of the cell bodies revealed significant differences between anterior and posterior cingulate areas [repeated measures ANOVAs: MF1, F(3,106) = 53.0, MF2, F(3,132) = 128; P < 0.001] and these cells were significantly different to those in IT and V1 (P < 0.05).
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In agreement with our findings in M. fasicularis, we found that the basal dendritic arbours of pyramidal cells in anterior cingulate of M. mulatta were larger than those in posterior cingulate (Fig. 8; Table 1). A MannWhitney U-test revealed the difference to be significant (P < 0.001; kurtosis = 0.39, skew = 0.753). Moreover, we found that pyramidal cells in anterior cingulate of M. mulatta had more dendritic branches than those in posterior cingulate (Fig. 8; Table 3). A repeated measures ANOVA revealed the difference to be significant [P < 0.001; intercept F(1,111) = 2472, cortical area F(1,111) = 29.8; P < 0.05]. As in M. fasicularis, we found that the size of the somata in anterior cingulate of M. mulatta were, on average, smaller than those in posterior cingulate (Fig. 8; Table 4). However, an unpaired t-test revealed no significant difference between the two groups [t(90) = 1.27; P = 0.2075; kurtosis = 0.0397, skew = 0.432].
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Discussion |
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A study of the literature reveals little agreement regarding functions performed in anterior and posterior cingulate cortex. Various authors have attributed higher cognitive and emotional functions to the anterior cingulate cortex and vegetative functions to posterior cingulate cortex (Goldman-Rakic, 2000; Passingham, 2000
; Allman et al., 2001
) whereas others have claimed the reverse (e.g. Baleydier and Mauguiere, 1980
). Indeed, there are many differences in opinion regarding the evolution and function of cingulate cortex (for reviews, see Sanides, 1970
; Baleydier and Mauguiere, 1980
; MacLean, 1989
; Allman et al., 2001
). In a recent series of studies in which cortical activity was recorded in awake behaving monkeys by fMRI, Dreher and colleagues revealed that anterior cingulate, unlike posterior cingulate, is often co-activated with granular prefrontal cortex (gPFC) during cognitive tasks (Dreher and Berman, 2002
; Dreher and Grafman, 2003
). Our results show that the size, branching pattern and spine density along the dendrites of the pyramidal cells in anterior cingulate is considerably higher than that in posterior cingulate cortex. Moreover, pyramidal cell structure in anterior cingulate cortex more closely approximates that seen for cells sampled from gPFC of the same hemisphere, than do those in posterior cingulate (unpublished observations).
As reviewed elsewhere, these different aspects of pyramidal cell microanatomy may influence different aspects of cellular, and systems, function (Segev and Rall, 1998; Koch, 1999
; Mel, 1999
; Spruston et al., 1999
; Häusser et al., 2000
; Segev et al., 2001
; Elston, 2002
, 2003a
; Häusser and Mel, 2003
). Briefly, the size of the arbour influences sampling geometry: the relationship between the size of the dendritic arbour and the arborization pattern of axons from which they sample inputs determines the degree of convergence/divergence (Malach, 1994
). The branching structure influences the potential for compartmentalization of processing within the arbours of pyramidal cells, which reportedly endows more branched cells with greater functional capability (Poirazi and Mel, 2000
). The branching structure and spine density influence the total number of putative excitatory inputs sampled by cells. That pyramidal cells in anterior cingulate cortex have more complex structure than those in posterior cingulate cortex but less complex structure than those in granular prefrontal cortex (cf. Elston, 2000
) suggests that patterns of intrinsic connectivity and, hence, the functional capabilities, of circuitry in the anterior cingulate is intermediate between the posterior cingulate and gPFC.
Specialization in Pyramidal Cell Structure in Cingulate Cortex
The present data confirm and extend previous findings of regional variation in pyramidal cell structure in primate cingulate cortex (Nimchinsky et al., 1996, 1997
). Moreover, direct comparison of layer III pyramidal cells sampled in cingulate cortex with those sampled in V1 of the same hemisphere revealed that those in anterior cingulate are, on average, at least eight times more spinous than those in V1. Comparison of the present data with those of previous studies reveals that layer III pyramidal cells in cingulate (both anterior and posterior) are characterized by more complex structure than those in primary somatosensory and auditory areas (cf. Elston and Rockland, 2002
; Elston et al., 2002
). In addition, layer III pyramidal cells in cingulate cortex are more spinous than those in many association areas. For example, they are more branched and more spinous than those in the lateral intraparietal area (LIP), cytoarchitectonic area 7a and the fourth visual area (cf. Elston and Rosa, 1997
, 1998
). However, the relative structural complexity of pyramidal cells in cingulate cortex depends on where in cingulate cortex the cells are located. In future studies it will be interesting to study pyramidal cell structure in that part of cingulate cortex that occupies the medial wall of the frontal lobe (anterior to the commisure, e.g. Brodmann's area 32 or area MF of Preuss and Goldman-Rakic, 1991
) to determine how they compare with those sampled here and those in gPFC.
Address correspondence to Guy Elston, Vision, Touch and Hearing Research Centre, Department of Physiology and Pharmacology, School of Biomedical Sciences, The University of Queensland, Queensland 4072, Australia. Email: g.elston{at}vthrc.uq.edu.au.
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Acknowledgments |
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