Cytoarchitectonic parcellation and functional characterization of four new areas in the caudal parahippocampal cortex

Abstract

Brain areas at the parahippocampal gyrus of the temporal-occipital transition region are involved in different functions including processing visual-spatial information and episodic memory. Results of neuroimaging experiments have revealed a differentiated functional parcellation of this region, but its microstructural correlates are less well understood. Here we provide probability maps of four new cytoarchitectonic areas, Ph1, Ph2, Ph3 and CoS1 at the parahippocampal gyrus and collateral sulcus. Areas have been identified based on an observer-independent mapping of serial, cell-body stained histological sections of ten human postmortem brains. They have been registered to two standard reference spaces, and superimposed to capture intersubject variability. The comparison of the maps with functional imaging data illustrates the different involvement of the new areas in a variety of functions. Maps are available as part of Julich-Brain atlas and can be used as anatomical references for future studies to better understand relationships between structure and function of the caudal parahippocampal cortex.

Keywords: Collateral sulcus; Cytoarchitecture; Human brain mapping; Julich-Brain; Parahippocampal gyrus; Parahippocampal place area.

Fig. 1

Historical cytoarchitectonic map of von Economo and Koskinas (1925), basal view. The region of interest is marked in red. It includes areas PH and TH. The collateral sulcus is marked in blue, the rhinal sulcus is marked in green

Fig. 2

Observer-independent identification of cytoarchitectonic borders. a Postmortem brain number 4 (Table 1). The sectioning plane is marked in red. b Coronal section stained for cell bodies with ROI (black rectangle). This ROI was digitized and subsequently transformed into a GLI image. c Inverted GLI image. d Equidistant traverses were calculated and GLI profiles were extracted along these traverses. e Mahalanobis distances as a function on the position of the profile along the cortical ribbon (example for a block size of 20 profiles); significant maximum at profile 55. f Projection of the identified border between areas Ph1 and Ph3 to the original image

Fig. 3

Caudal-to-rostral extent of areas Ph1, Ph2, Ph3 and CoS1 in 14 serial histological sections of postmortem brain number 1. Distance between most caudal and most rostral sections: 33 mm. Adjacent areas V2 (BA18; Amunts et al. 2000), FG1 (Caspers et al. 2013), FG3 and FG4 (Lorenz et al. 2017) are indicated. Collateral sulcus, calcarine sulcus, fusiform gyrus (FG) and parahippocampal gyrus (PG) are also labelled. The red lines in the lateral and ventral view of the postmortem brain in the upper left mark the approximate region from which the section series originates

Fig. 4

Examples of cytoarchitectonic borders between a Ph1 and FG3, b Ph2 and FG3, c Ph3 and V2 as well as d CoS1 and FG3. The histologic images were contrast enhanced for better visualization

Fig. 5

Cytoarchitecture of areas Ph1, Ph2, Ph3 and CoS1. The coloured lines indicate mean GLI profiles. Ph1 was characterized by distinct layers IIIc and VI with predominantly medium-sized pyramidal cells and a clearly visible layer IV. Ph2 was characterized by a layer III with small pyramidal cells and low cell density within all sublayers, a thin and blurred IV and a V with a high density of medium-sized pyramidal cells without a distinct border to VI. Ph3 especially differed from Ph1 by a higher cell density of IV, a layer V with small pyramidal cells and its obvious horizontal stripes due to the high density of IV and VI and the light V in-between them. CoS1 had a thin and light layer IV as well as a slim layer V with a low density of small pyramidal cells. The histologic images were contrast enhanced for better visualization

Fig. 6

Cluster analysis of the four new parahippocampal areas and adjacent fusiform areas (FG1, FG2, FG3 and FG4). The dendrogram shows a grouping of FG1 and FG2 on one branch, and Ph1, Ph2, Ph3, CoS1 as well as FG3 and FG4 on the second branch. Ph3 is rather separated from the other three parahippocampal areas on grounds of more cytoarchitectonic dissimilarities. FG1 and FG2 are structurally similar to each other and differ from the other six areas (y-axis: cytoarchitectonic areas, x-axis: Euclidean distance)

Fig. 7

Probability maps of the areas Ph1, Ph2, Ph3 and CoS1 registered to the MNI single subject reference template Colin27. The probabilities are colour-coded. The coordinates are written in white underneath (left/right). A coronal section is shown enlarged displaying the location of the collateral sulcus (CoS), the calcarine sulcus (CaS) as well as the parahippocampal gyrus (PG)

Fig. 8

MPM of the four parahippocampal areas registered to the MNI single subject reference template Colin27; inflated view without the cerebellum. Available through https://www.fz-juelich.de/inm/inm-1/julich-brain. Red lines mark the collateral sulcus

Fig. 9

Comparison of cytoarchitectonic maps with positions of functional imaging studies of Aguirre et al. (1996) (yellow), Epstein et al. (1999) (white), Hales et al. (2009) (turquoise), Henke et al. (1999) (grey), Janzen et al. (2007) (green), Kirwan and Stark (2004) (blue), Maguire et al. (1998) (pink), Kveraga et al. (2011) (orange) and Sommer et al. (2005) (red) with surface reconstructions of the MPM of the four new areas in the MNI152 reference space. The dots indicate the coordinates of different activations. The light blue area represents the most probable position of the PPA as described by Weiner et al. (2018). Ph1 is marked in green, Ph2 in yellow, Ph3 in red and CoS1 in blue. Coordinates of the named studies are written in Table 4