Parcellation of human temporal polar cortex: a combined analysis of multiple cytoarchitectonic, chemoarchitectonic, and pathological markers - PubMed (original) (raw)

Parcellation of human temporal polar cortex: a combined analysis of multiple cytoarchitectonic, chemoarchitectonic, and pathological markers

Song-Lin Ding et al. J Comp Neurol. 2009.

Abstract

Although the human temporal polar cortex (TPC), anterior to the limen insulae, is heavily involved in high-order brain functions and many neurological diseases, few studies on the parcellation and extent of the human TPC are available that have used modern neuroanatomical techniques. The present study investigated the TPC with combined analysis of several different cellular, neurochemical, and pathological markers and found that this area is not homogenous, as at least six different areas extend into the TPC, with another area being unique to the polar region. Specifically, perirhinal area 35 extends into the posterior TPC, whereas areas 36 and TE extend more anteriorly. Dorsolaterally, an area located anterior to the typical area TA or parabelt auditory cortex is distinguishable from area TA and is defined as area TAr (rostral). The polysensory cortical area located primarily in the dorsal bank of the superior temporal sulcus, separate from area TA, extends for some distance into the TPC and is defined as the TAp (polysensory). Anterior to the limen insulae and the temporal pyriform cortex, a cortical area, characterized by its olfactory fibers in layer Ia and lack of layer IV, was defined as the temporal insular cortex and named as area TI after Beck (J. Psychol. Neurol. 1934;41:129-264). Finally, a dysgranular TPC region that capped the tip with some extension into the dorsal aspect of the TPC is defined as temporopolar area TG. Therefore, the human TPC actually includes areas TAr and TI, anterior parts of areas 35, 36, TE, and TAp, and the unique temporopolar area TG.

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Figures

Fig. 1

Macrophotographs of human temporal lobes showing different aspects of the human TPC. The anatomical landmarks and the major subdivisions (anterior areas 35, 36, TE, TAp and areas TAr, TI, and TG) and their relationship in the TPC are shown. A-C: Dorsal (A), mediodorsal (B) and medioventral (C) aspects of the same temporal lobe from case 1. Solid line 7A in B indicates the imaging plane of the level A (A1-A4) in Fig.7. D: Dorsal view of the TPC in another case (case 4) showing how the limen insulae (LI) connects the temporal (TI) and frontal (FI) parts of the agranular insular cortex. Note in this case the shallow rhinal sulcus (rs) extends between the pyriform cortex (Pir) and area TI. E: Anterior view of the TPC from case 6. The dashed lines 2A, 2B and 2C indicate the planes of the coronal sections cut from the same brain block and showed in Fig. 2A, B and C, respectively. F: Lateral view of the TPC from another case. The solid lines 2D and 2E indicate the planes of the horizontal sections shown in Fig.2D and 2E, respectively. The dashed line 2F in panel F indicates the sagittal plane shown in Fig.2F. For abbreviations see the list for this figure and for the following figures). Scale bar: 1cm (for A-F).

Fig.2

Coronal (A-C), horizontal (D and E) and sagittal (F) sections through the TPC of a normal aging case (case 6) showing the different patterns of PV immunoreactivity across TPC regions. Note that only one temporal polar sulcus (ps) was observed in the case shown in A-C. The inset shows a posterior section as a comparison for the TPC regions. The orientation of the coronal sections in A-C and in the inset is indicated by the compass in C (d: dorsal; m: medial); that of the horizontal sections in D and E is shown by the compass in E (m; medial; p: posterior); and of the sagittal section in F (d: dorsal; P: posterior). The short solid lines along the cortical surface mark the borders of different cortical areas (the same marks are used in the following figures). The approximate locations of the sections A-C and D-F are indicated in Fig.1E and F. Scale bar: 6 mm (for A-F).

Fig. 3

Typical features of area 35 as revealed by Thioflavin-S staining. A and B: lower (A) and higher (B) power views of the unique layer IIIu in area 35 in a severe AD case (case 12). Note the vertical columns in area 35a. The marks * (in A and the inset) and # (in A and B) point to the corresponding regions. Note in layer IIIu many large pyramidal cells were stained. The imaging location of section A was shown in the inset of Fig.4 by the dashed line 3A. C: A section from a normal aging case (case 7) and double-stained with NeuN (black) and Thioflavin-S (white) shows how layer IIIu and the vertical large-celled columns stained with Thioflavin-S stand out in area 35 against other neurons stained with NeuN. Note the clear alternating large- (white) and small- (black) celled columns in area 35a in this double-stained section. Roman numbers indicate different cortical layers (the same marks are used in the following figures). Scale bars in A-C: 200μm.

Fig.4

Three adjacent horizontal sections from a normal aging case (case 8) and stained for NeuN (A), NFT (thioflavin-S, B) and PV (C) show the typical staining patterns found in anterior area 35. The orientation of section C is shown in the Inset. A and B are higher power views of area 35 from adjacent sections, as indicated in C. Note in C that the anterior and posterior area 35 are positioned anterior and posterior to the EC, respectively. D. A high power view of NFT-containing neurons in the marked region of B (the arrow D in B and the arrow in D point to the corresponding location). The dashed line 3A in the inset indicates the imaging coronal plane where section A in Fig.3A was taken. Scale bars: A and B, 800μm; C and inset, 1cm; D, 200μm.

Fig. 5

Sequential AT8/NeuN double-labeled sections from the anterior (A) and posterior (B) part of the TPC from a normal case (case 2) show that heavy AT8+ immunostaining was only observed in layer Ia (the dark bands) of pyriform cortex (Pir) and area TI (B) but not in other regions. The dark AT8+ band in layer Ia (in B, H and J) of the pyriform cortex (Pir) and area TI (TI) is composed of AT8+ thorn-shaped astrocytes. High power views of layer Ia in area TI are shown in Fig. 10F and G. Cytoarchitectonic features of the TPC areas TG (C), 35b (D), 36 (E), TE (F), TAr (G), Pir (H), 35a (I), TI (J), and TAp (K) were clearly revealed by NeuN immunostaining in this normal case. The locations of C-K are shown in A and B by the black bars with corresponding letters. Section L shows the dense olfactory fibers in layer Ia of area TI. For detailed explanations, see text. Scale bars: 6 mm (A and B); 200μm (C-L).

Fig. 5

Fig.6

Low power views of the staining pattern revealed by three different markers at three anteroposterior levels (A-C) of the anterior temporal lobe from a normal case (case 3). At each level, adjacent coronal sections are shown for NeuN, PV and CB labeling. Higher power views of the CB staining in areas Eo, 35a, 36 and TE are shown in D, E, F and G, respectively. Note that the staining intensity in CB+ pyramidal cells (arrows) is generally lower than that in CB+ non-pyramidal cells (arrowheads; D-G). The locations of these areas are marked by black bars with corresponding letters. For detailed explanations, see text and table 2. Scale bars: 10mm (A-C); 200μm (D-G).

Fig.7

Low power views of the staining pattern revealed by four different markers at six anteroposterior levels (A-F) of the anterior temporal lobe from a normal aging case (case 9). At each level, adjacent coronal sections are shown for NeuN, PV, AT8 and WFA staining. Higher power views of the PV staining in areas 35a, 35b, 36, TG, TEv, TEd, TAp and TAr are shown in panels A, B, C, D, E, F, G and H of Fig.8, respectively. The locations of these areas are marked by black bars 8A-8H in C2 and D2. In addition, higher power views of the AT8 staining in areas 35b, 36, TG, TE and TI were shown in A, B, C, D and E of Fig.10, respectively. The locations of these areas are marked by black bars A-E in C3 and D3. Finally, higher power views of the locations indicated by black bars 13A-E in B1, A1, C1 (for NeuN) are shown in Fig.13A-E, respectively. Scale bar: 6 mm.

Fig.8

Higher power views of PV immunostaining patterns in different layers of areas 35a (A), 35b (B), 36 (C), TG (D), TEv (E), TEd (F), TAp (G) and TAr (H) from the case shown in Fig.7. The locations of these images are indicated in sections C2 and D2 of Fig.7. Note the differences in density and staining intensity of PV+ neurons and neuropil across different areas. Scale bar: 200μm (A-H).

Fig.9

Two adjacent sections from the anterior TPC immunostained with NeuN (A) and SMI-32 (B) antibodies in a normal case (case 5) show typical cytoarchitectonic and SMI-32+ staining patterns at different locations in the TPC. Higher power views of SMI-32+ labeling in areas 35b, 36, TE, TAr and TG in section B are shown in C, D, E, F and G, respectively. Scale bars: 6 mm (A and B); 300μm (C-G).

Fig.10

A-E: Higher power views of AT8 staining patterns in different layers of areas 35b (A), 36 (B), TG (C), TE (D) and TI (E) from the case shown in Fig.7. The locations of these images are indicated in sections C3 and D3 of Fig.7. Note the apparent difference in density of AT8+ neurons and neuropil across different areas. F and G: An AT8 and NeuN double-stained section from area TI from the case shown in Fig. 5 shows densely packed AT8+ astrocytes in layer Ia (brown color) but not in other layers. Thus, layer II only contains NeuN immunostained neurons (blue color). H and I: Low power views of the two AChE stained sections at levels C and D of Fig.7 (from the same case) show the general AChE staining patterns found in TPC areas. Higher power views of the AChE staining in the EC (Eo) and areas TI, 35, TG, 36 and TE (locations indicated by the black bars) are shown in Fig. 11A-F, respectively. Scale bars: 200μm (A-F); 50μm (G); 6mm (H and I).

Fig.11

Higher power views of AChE staining patterns in different layers of the Eo (A) and areas TI (B), 35 (C), TG (D), 36 (E) and TE (F) from the locations shown in Fig. 10H and I. Note that relatively darker AChE staining was seen in layers V and VI than in layers II and III of all areas except area 35 where relatively darker labeling was observed in layers II and III than in layers V and VI. Scale bar: 200μm.

Fig.12

Higher power views of typical WFA staining patterns found in different layers of the Eo (A) and areas TI (B), 35 (C), TG (D), 36 (E) and TE (F) from the locations shown in Fig. 7C4, D4. Note the different density and staining intensity of WFA labeling in different areas. Scale bar: 200μm.

Fig.13

Higher power views of NeuN staining in areas Eo (A and B), PACo (C), TEv (D), and TEd (E) from the same case as shown in Fig.7. The locations of these images are shown in sections B1, A1 and C1 of Fig. 7 by black bars 13A-13E, respectively. The cell islands in layer II of the Eo in A and B are circled while the patches in layer III of area PEA in C are indicated by arrows. In addition, NeuN labeled neurons in layers IV, V and VI of area 36 are shown in F at high magnification while CB immunoreactive cells and neuropil in both superficial and deep layers of area 36 is shown in G. Note in G that layers IV –VI have many fewer CB labeled neurons than layers II-III and that arrows and arrowheads point to pyramidal and nonpyramidal neurons respectively. Scale bars: 200μm (A-E, G); 100μm (F).

Fig.14

Summary of the locations of different TPC areas and their relationships on the lateral (A), dorsal (B) and medial (C) aspects of the human temporal lobe.

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Parcellation of human temporal polar cortex: a combined analysis of multiple cytoarchitectonic, chemoarchitectonic, and pathological markers - PubMed (original) (raw)