Elsevier

NeuroImage

Volume 58, Issue 2, 15 September 2011, Pages 362-380
NeuroImage

Probabilistic fibre tract analysis of cytoarchitectonically defined human inferior parietal lobule areas reveals similarities to macaques

https://doi.org/10.1016/j.neuroimage.2011.06.027Get rights and content

Abstract

The human inferior parietal lobule (IPL) is a multimodal brain region, subdivided in several cytoarchitectonic areas which are involved in neural networks related to spatial attention, language, and higher motor processing. Tracer studies in macaques revealed differential connectivity patterns of IPL areas as the respective structural basis. Evidence for comparable differential fibre tracts of human IPL is lacking. Here, anatomical connectivity of five cytoarchitectonic human IPL areas to 64 cortical targets was investigated using probabilistic tractography. Connection likelihood was assessed by evaluating the number of traces between seed and target against the distribution of traces from that seed to voxels in the same distance as the target. The main fibre tract pattern shifted gradually from rostral to caudal IPL: Rostral areas were predominantly connected to somatosensory and superior parietal areas while caudal areas more strongly connected with auditory, anterior temporal and higher visual cortices. All IPL areas were strongly connected with inferior frontal, insular and posterior temporal areas. These results showed striking similarities with connectivity patterns in macaques, providing further evidence for possible homologies between these two species. This shift in fibre tract pattern supports a differential functional involvement of rostral (higher motor functions) and caudal IPL (spatial attention), with probable overlapping language involvement. The differential functional involvement of IPL areas was further supported by hemispheric asymmetries of connection patterns which showed left–right differences especially with regard to connections to sensorimotor, inferior frontal and temporal areas.

Highlights

► Human inferior parietal connections to 64 targets using probabilistic tractography. ► Implementation of analysis algorithm for quantitative evaluation of connections. ► Accounting for seed size and distance between seed and target areas. ► Gradual shift of connection patterns from rostral to caudal IPL. ► Left–right asymmetry of connections for different functional systems.

Introduction

The human inferior parietal lobule (IPL) is a heterogeneous, multimodal brain region as demonstrated by functional neuroimaging and lesion mapping studies. Thus, different parts of human IPL seem to be involved in different functional brain networks, where they interact with different other cortical regions within frontal, occipital, and temporal lobe.

Rostral IPL areas bilaterally seem to be involved in higher motor functions, potentially including parts of a human mirror neuron system (Rizzolatti and Craighero, 2004, Iacoboni, 2005, Keysers and Gazzola, 2009, Caspers et al., 2010). The caudal IPL, in contrast, was shown to feature hemisphere-specific functionality. The right IPL is recruited during spatial and non-spatial attention and motor preparation tasks and conceptualised as part of the “ventral attention network” (Fink et al., 2001, Corbetta and Shulman, 2002, Corbetta et al., 2008, Jakobs et al., 2009). Contrastingly, its left counter-part is thought to form Geschwind's area in the language network, being mainly involved in semantic and phonological processing (Geschwind, 1970, Price, 2000, Gernsbacher and Kaschak, 2003, Vigneau et al., 2006).

In macaque monkeys, electrophysiological recordings have shown evidence of a comparable functional segregation of the IPL as in humans (apart from language processing). Rostral IPL areas in this species have been shown to contain mirror neurons and participate in sensorimotor processing, whereas caudal areas are mainly involved in functions such as spatial attention, auditory-sensory integration, and visuo-motor coordination, e.g., grasping (Hyvärinen, 1982, Pandya and Seltzer, 1982, Seltzer and Pandya, 1984, Rozzi et al., 2006).

In both species, this functional heterogeneity is reflected on a cytoarchitectonic level. In humans, a recent study delineated seven cytoarchitectonically distinct areas within the IPL (Caspers et al., 2006, Caspers et al., 2008). Five of these cover the lateral surface of the IPL in a rostro-caudal sequence (Fig. 1A). The remaining two are located in the Sylvian fissure. Comparably, the macaque IPL has been reported to consist of six main areas (Pandya and Seltzer, 1982, Gregoriou et al., 2006). Of these, four are located on the lateral surface in a rostro-caudal sequence (Fig. 1B), the other two in the Sylvian fissure.

Tracer studies of axonal connectivity in macaques have provided a potential link between structural heterogeneity and functional diversity of the IPL by revealing a differentiated connectivity pattern of the cortical areas in this region. Rostral areas (PF, PFG) show strong reciprocal connections to (pre-) motor, somatosensory and superior parietal areas. In contrast, caudal areas are mainly connected to higher visual areas within occipital and inferior temporal cortex (Cavada and Goldman-Rakic, 1989a, Cavada and Goldman-Rakic, 1989b, Felleman and Van Essen, 1991, Gregoriou et al., 2006).

In humans, the anatomical connectivity of individual IPL areas is largely unknown, although macroanatomical fibre preparations and studies on disconnection syndromes such as apraxia (Freund, 2003, Culham and Valyear, 2006), spatial neglect (Karnath, 2001, Hillis, 2006, Husain and Nachev, 2007) or aphasia (Dronkers et al., 2004) support the idea of a similar connection pattern for humans as in macaques. Diffusion tensor imaging (DTI) studies in healthy humans were indeed able to show partly different connectivity of different aspects of the IPL. Makris et al. (2005) found a partition of one of the two main fibre pathways connecting the IPL with mainly frontal regions, i.e. the superior longitudinal fascicle (SLF) which they could subdivide into four distinct parts, two of which running into the rostral and caudal aspect of the IPL, respectively. Catani et al. (2005) found a comparable partition for the other main pathway, i.e. the arcuate fascicle. They demonstrated that different parts of the arcuate fascicle reach either the rostral or the caudal aspect of the IPL, comparable to the SLF as reported by Makris et al. (2005). Focusing on a possible subdivision of the parietal cortex by means of connectivity based parcellation, Rushworth et al. (2006) showed that rostral IPL is more likely to connect to ventral premotor cortex whereas caudal IPL was more likely to connect with the parahippocampal gyrus. A recent study by Mars et al. (2011) used connectivity-based parcellation of the IPL, resulting in a comparable subdivision of this region as found by cytoarchitectonic parcellation (Caspers et al., 2006, Caspers et al., 2008). Consecutive resting-state functional connectivity analyses showed how the IPL areas were differentially connected to premotor, prefrontal and parahippocampal areas (Mars et al., 2011). These studies provide first hints that the fibre tract pattern of human IPL is different in its many parts, at least in rostral and caudal IPL.

But it can be assumed that the functional and cytoarchitectonic heterogeneity of the IPL is also reflected by a more differentiated fibre tract pattern than a bipartition. In order to provide a precise identification of areal-specific fibre tract pattern as structural basis for the involvement in different functional networks, we assessed the fibre tracts related to five cytoarchitectonic areas of the lateral IPL using probabilistic tractography based on DTI data.

Section snippets

Data acquisition

We acquired diffusion-weighted data from 40 healthy, right-handed human subjects (20 males, mean age ± SD = 28.65 ± 5.73, range 21–42; 20 females, mean age ± SD = 28.75 ± 6.20, range 21–42) on a 3.0 T Tim-Trio Siemens whole-body scanner (Siemens, Erlangen, Germany) with a maximum gradient strength of 40 mT m 1, using a 12-channel phased-array head coil for signal reception. Subjects had no history of neurological or psychiatric disease, or head injury. All subjects gave informed, written consent to

Fibre tract pattern of IPL areas

The courses of the (hemisphere-specific) fibre tract patterns for the individual IPL seed areas are visualised in Fig. 4. It should be noted that the probabilistic nature of the tractography as well as the inter-individual variability of fibre tract patterns contributes to substantial uncertainty of these group-averaged tracts.

Visual inspection of the tractography patterns indicates that homologous regions on either hemisphere show a largely similar course. The most conspicuous differences in

Discussion

The fibre tract patterns of five cytoarchitectonic areas on the lateral surface of the human inferior parietal lobule were assessed by means of probabilistic tractography. Connection likelihood was analysed by evaluating the number of traces reaching a particular target against those reaching other voxels in the same distance from the seed. Random-effects inference then delineated connections that were consistently (across subjects) expressed with higher than expected densities. Across IPL

Acknowledgments

This Human Brain Project/Neuroinformatics Research was funded by the National Institute of Biomedical Imaging and Bioengeneering, the National Institute of Neurological Disorders and Stroke and the National Institute of Mental Health (KZ). Further funding was granted by the Human Brain Project (R01-MH074457-01A1; SBE), the Initiative and Networking Fund of the Helmholtz Association within the Helmholtz Alliance on Systems Biology (Human Brain Model; KZ, SBE), and the Helmholtz Alliance for

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    These authors contributed equally to the present study.

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