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. Author manuscript; available in PMC: 2021 Jun 4.
Published in final edited form as: J Magn Reson Imaging. 2007 Jan 1;25(1):48–54. doi: 10.1002/jmri.20810

Two-Dimensional Population Map of Cortical Connections in the Human Internal Capsule

Mojtaba Zarei 1,*, Heidi Johansen-Berg 1, Mark Jenkinson 1, Olga Ciccarelli 2, Alan J Thompson 2, Paul M Matthews 1
PMCID: PMC7610899  EMSID: EMS124337  PMID: 17152053

Abstract

Purpose

To exploit diffusion imaging tractography to produce a two-dimensional (xy) probabilistic population map of the cortical connections within the human internal capsule (IC).

Materials and Methods

Diffusion tensor imaging (DTI) was carried out on 11 healthy volunteers. We parceled an axial section of the IC according to its connections to the prefrontal, premotor, primary motor, primary somatosensory, posterior parietal, and occipital cortices using our locally developed probabilistic algorithm.

Results

A consistent topographical organization was generated that was consistent with our anatomical knowledge of the IC. In addition, our study shows that in humans the anterior half of the IC is occupied by the prefrontal cortex.

Conclusion

This map may be of clinical use for correlating neurological deficit with hemispheric lesions, particularly those that affect sensorimotor function.

Keywords: human internal capsule, mapping, diffusion tensor imaging, tractography, anatomy

THE MAJORITY OF CONNECTIONS between the cerebral cortex and subcortical structures travel through the internal capsule (IC) (1). The IC is limited laterally by the pallidum and medially by the thalamus (for the posterior limb IC (PLIC)) and head of the caudate nucleus (for the anterior limb IC (ALIC)). Detailed studies of the functional anatomy of the PLIC using deep-brain stimulation localized the corticospinal tract within the posterior half of this segment (2,3). Clinicopathological (4,5) and postmortem investigations (6–8) supported this observation. Tracer studies in nonhuman primates showed that the ALIC is predominantly occupied by connections between the prefrontal (9–11) and temporal (12,13) cortices and other cortical or subcortical structures. The PLIC includes connections of the parietal (14), temporal (12,13), occipital (14,15), and sensorimotor (16,17) cortices.

Recent advances in diffusion-weighted MRI (DWI) have provided investigators a unique opportunity to visualize white matter (WM) pathways in the human brain in vivo (18–20). This method has been used to demonstrate the somatotopic representation of the human motor tracts within the IC of healthy adults (21), and changes in the corticospinal tracts of patients with motor neuron disease (19). In this study we used Bayesian probabilistic diffusion tractography (22) to produce a two-dimensional (2D) map of cortical connections in the xy plane within the IC. We propose that this map may have clinical applications for correlating neurological deficits with structural MRI findings and predicting the recovery of function in stroke patients (23–25).

Materials And Methods

Subjects

In this work we examined 11 right-handed healthy subjects (seven males and four females, 23-57 years old; for a description of the subjects see Ref. 22). Informed written consent was obtained from all subjects and the study was approved by the National Hospital for Neurology and Neurosurgery Joint Research Ethics Committee.

Image Acquisition

DW images were obtained using echo-planar imaging (EPI) on a General Electric 1.5 T Signa Horizon scanner with a standard quadrature head coil and maximum gradient strength of 22 mT m-1. The following parameters were used: slice thickness = 60 × 2.3 mm, field of view (FOV) = 220 × 220 mm2, and matrix = 96 × 96. Images were reconstructed on a 128 × 128 matrix, with a final resolution of 1.7 × 1.7 × 2.3 mm3.

The diffusion weighting was isotropically distributed along 54 directions (δ = 34 msec, Δ = 40 msec, b-value = 1150 s mm-2). Six volumes with no diffusion weighting were also acquired. Cardiac gating was used to minimize artifacts from pulsatile flow of the cerebrospinal fluid (CSF). The total scan time for the DWI protocol was approximately 20 minutes. A high-resolution Tl-weighted (T1W) scan was obtained with a three-dimensional (3D) inversion-recovery prepared spoiled gradient-echo (IR-SPGR) sequence (FOV = 310 X 155; matrix = 256 X 128; in-plane resolution = 1.2 X 1.2 mm2; slice thickness = 156 X 1.2 mm; TI = 450 msec; TR = 2 seconds; TE = 53 msec).

Image Analysis

Image analysis was carried out with the use of tools from the FMRIB Software Library (FSL, http://www.fm-rib.ox.ac.uk/fsl). BET was used for brain extraction of T1- and T2W images. FLIRT was used to derive affine transformation matrices between DW, T1W, and standard (MNI) space. Two levels (z = 1 and 7 in MNI space) were selected to better test the reproducibility of the IC map topography. The lower level was chosen to lie just below the level of the adjacent deep gray matter (GM) structure (thalamus and striatum) and thus reduce the impact of partial-volume contributions from them. We reduced the effects of eddy currents and head motion by registering all DW images to a non-DW references image using affine registration. Analysis of the DW images was carried out with the use of tools from the FMRIB Diffusion Toolkit. Probabilistic modeling of diffusion parameters and tractography were carried out using previously described methods (26). Tractography was run from seed voxels within the IC, and the probability of a connection between these seeds and specific cortical target masks was recorded.

Definition of Seed and Target Masks

Seed masks of the IC in both hemispheres for each subject were drawn manually on an axial image at two levels (z = 1 and 7) from fractional anisotropy (FA) maps derived from the DWI data set and registered in standard space. The lateral and medial borders of the IC masks were defined using an FA threshold of 0.3. The FA (mean ± standard error (SE)) of structures adjacent to the IC was 0.12 ± 0.01 for basal ganglia, 0.24 ± 0.01 for thalamus, and 0.64 ± 0.02 for WM. We limited the IC masks posteriorly to a hypothetical line between the most posterior borders of thalamus and putamen, and anteriorly to a line between the most anterior borders of the putamen and head of the caudate nucleus. The volume of the IC masks was 448 ± 13 mm3 for the right hemisphere and 432 ± 16 mm3 for the left hemisphere.

Cortical target masks for each individual subject were defined for the prefrontal, premotor (including supplementary motor cortex), primary motor (M1), primary somatosensory (S1), posterior parietal, temporal, and occipital cortices. The anatomical criteria for identifying these areas were described previously (22). Connections from IC voxels to lateral aspects of sensorimotor cortex (representing the head, face, tongue, and adjacent structures) are difficult to identify because tracts connected to these parts crosses the superior longitudinal fasciculus (SLF). Current tractography algorithms are typically unable to trace past such crossing fiber regions efficiently (26) because of the ambiguity of a single fiber direction representation. As an approximation, we assumed that the paths of fibers of the IC entering the SLF would be linear across its width. While this assumption is unlikely to be an accurate representation for individual axons (they may take a more curvilinear curve), at the level of resolution of the tracts used here the approximation was considered reasonable (see below). After interpolation across the SLF mask was performed, tractography was continued from the newly defined seed region to the cortical target. To define the 3D mask of the SLF, we ran our probabilistic tractography algorithm on a 2D mask drawn on coronal sections (y = -46) of the FA map through the sensorimotor cortex for each individual. The volume corresponding to the SLF was defined as that with strongest anteroposterior anisotropy. To ensure that this method did not adversely affect our map, we also mapped motor tracts related to foot, hand, and facial muscle regions on M1, and found a somatotopic organization of these areas within the IC (27) that is consistent with our current understanding of anatomy.

Connectivity-Based Segmentation of the IC

Individual Subject Analysis

For each subject, probabilistic tractography was run from seed voxels within the IC, as discussed above, and the probability of connection between these seeds and specific cortical target masks was recorded. We carried out “hard” segmentation of the IC for individual subjects by classifying each IC voxel according to the unique cortical target mask with which it had the highest probability of connection. In an additional representation, we separately defined clusters of voxels that connected to each cortical target mask by thresholding at 10% of the maximum connectivity value to that target mask.

Group Analysis

We constructed an inclusive group IC mask by adding all individual-subject IC masks together. This group IC mask was thresholded to include only those voxels in the IC that were shared among at least 70% of the subjects. Two-dimensional affine registration was then used to linearly align each slice of each individual subject’s IC mask with the corresponding slices in the group mask (28). We then applied the resulting transformation matrices to individual clusters of IC voxels connected to each cortical region to align these clusters with the group IC mask space. For hard segmentation at the group level, we labeled each voxel within the group IC map by the target mask to which that voxel was most strongly connected in the greatest number of the individuals.

We constructed a probabilistic group map of cortical connections in the IC by binarizing clusters of IC voxels connecting to each cortical mask for each subject (using a threshold connectivity probability value of 10%) and summing these binarized clusters across subjects. IC voxel values in the resulting group maps for each cortical target area therefore reflect the number of subjects who showed dominant connections between IC voxels and the cortical target of interest. These group probability maps were thresholded to include only voxels in which >30% of the population showed connections for each cortical target area.

Results

Cortical connections were successfully traced within the IC at two different axial levels (z = 1 and 7) in all subjects.

Topographic Organization of the IC

Diffusion tractography is blind to the direction of the tracts; it simply defines probability of presence of tracts, be it afferent or efferent. We found a topographic organization of tracts within the IC related to the anteroposterior part of their cortical connections (Fig. 1). Connections of the prefrontal cortex were located within the ALIC and the anterior part of the PLIC. Premotor cortical connections were located in the anterior part of the PLIC. Immediately posterior to the premotor region were M1 tracts, followed by S1 tracts. Posterior to S1 were predominantly posterior parietal cortical connections. Pathways of the temporal cortex were diffuse but mostly aggregated along the posterolateral part of the PLIC and to a lesser degree in the medial border of the ALIC. Occipital cortical connections were found in the most posterior part of the PLIC in the lower IC mask (z = 1) and to a lesser degree in the anteromedial aspect of the ALIC in the upper IC mask (z = 7).

Figure 1.

Figure 1

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Group probability maps for each cortical region show a remarkable reproducibility of location of cortical connections within the IC across individuals. Prefrontal cortical connections occupied half of the entire volume of the IC. Sensorimotor tracts are in the posterior half of the PLIC. All cortical tracts are seen in both the lower (z = 1) and upper (z = 7) IC masks. Voxels are thresholded at 10% connection probability. Abbreviations: PFC = prefrontal, M1 = primary motor, S1 = primary somatosensory, PPC = posterior parietal, PMC = premotor, Occ = occipital, Tmp=temporal.

The probabilistic group map demonstrates that there were considerable overlaps between adjacent cortical tracts (Fig. 2). This was particularly apparent between the premotor cortex and M1, and between M1 and S1 tracts. Hard segmentation maps for individual subjects demonstrated high consistency among subjects (Fig. 3).

Figure 2.

Figure 2

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a: Hard segmentation map for the population, showing a topographical organization of cortical tracts in the IC that is very similar to the organization seen in the cerebral cortex. b: A group probability map that was thresholded to include voxels that were present in >30% of the group illustrates the overlap between connection regions, particularly the premotor cortex and M1, and M1 and S1. Abbreviations as in Fig. 1.

Figure 3.

Figure 3

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Hard segmentation maps for each individual studied, showing a remarkable reproducibility and consistency across subjects. They also demonstrate the consistency of topography of voxels at both axial levels. Voxels are thresholded at 10% connection probability. Abbreviations as in Fig. 1.

Variability

The location of cortical connections within the IC showed remarkable reproducibility. This was assessed by statistical analysis of coordinates of peak connection probability values for each cortical region (Table 1). However, the volumes and mean connection probabilities of cortical tracts and their apparent volumes within hard segmentation were variable.

Table 1. Variability of Coordinates of Maximum Value Voxels for Each Cortical Tract in Talairach Space.

Right hemisphere Left hemisphere
X ± SEM Y ± SEM X ± SEM Y ± SEM
Prefrontal 19.0 ± 0.8 −2.1 ± 3.3 −16.1 ± 1.4 0.4 ± 3.4
Premotor 21.4 ± 0.7 −12.7 ± 0.9 −20.6 ± 0.6 −14.2 ± 0.8
M1 23.8 ± 0.5 −17.3 ± 0.4 −21.0 ± 0.6 −18.4 ± 0.7
S1 25.2 ± 0.8 −18.6 ± 0.5 −21.9 ± 0.9 −20.5 ± 0.5
Postparietal 26.1 ± 0.7 −21.1 ± 0.6 −20.9 ± 0.6 −23.2 ± 0.8
Temporal 20.2 ± 2.8 −10.1 ± 3.7 −20.7 ± 2.5 −10.0 ± 4.5
Occipital 27.5 ± 1.9 −23.4 ± 0.8 −26.2 ± 0.8 −24.0 ± 1.2
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Tract Continuity

We identified clusters of voxels within the IC that were connected with the cortical regions using an IC seed mask at z = 7 for comparison with results generated using a seed mask at z = 1. With the exception of the occipital cortex, pathways that connected with all cortical targets were identified in the IC masks at both levels, consistent with the continuity of these tracts within the IC. Almost invariably, voxels with the highest connection probability in the lower mask were slightly more posteriorly located than in the upper mask. Occipital tracts were identified mostly in the lower IC mask.

We also tested directly whether potential partial-volume effects of adjacent GM structures (thalamus, striatum, and caudate) influence the apparent connectivity patterns within the IC. To do this, we re-ran the tractography algorithm on five subjects with these GM structures excluded from the tractography. We found no significant changes in the resulting IC connectivity patterns (data not shown).

Quantification of Cortical Connections in the Human IC

We calculated the ratio of the volume of the connected voxels in the mask to the volume of the target mask (mask-to-target volume ratio) for each cortical area. The IC-to-cortex volume ratio provides a simple measure of the relative representation of a cortical region in the IC. The sensorimotor tracts (M1, S1, and premotor cortices) had higher ratios than other cortical tracts in both hemispheres (Fig. 4). Interestingly, these ratios were significantly higher in the left hemisphere (M1: t = –3.4, P = 0.007;S1: t = –3.0, P = 0.013; premotor: t = –2.8, P = 0.017) than the right (Fig. 4).

Figure 4.

Figure 4

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The IC tract-to-cortex volume ratio for the cortical connections in the IC shows that sensorimotor tracts make up the largest relative volume in the IC. This suggests that the sensorimotor connections have denser fiber tracts than other cortical tracts. In addition, this ratio is higher in the left hemisphere, which may suggest a correlation with the cerebral dominance. A repeated-measures analysis of variance (ANOVA) showed significant main effects of hemisphere (F = 18.3, P = 0.002) and cortical target (F = 43.6, P < 0.001), and a significant interaction between hemisphere and cortical target (F = 5.9, P < 0.001). On average, the seed to target volume percentile was greater for the left hemisphere, and this effect was significant by paired t-tests in the primary motor (t = -3.4, P = 0.007), premotor (t = -2.8, P = 0.017), and primary somatosensory (t = -3.0, P = 0.013) cortices. Abbreviations as in Fig. 1.

Discussion

We found a clear and reproducible topographical organization of cortical tracts within the IC using MRI diffusion tractography. Our results confirm previous reports (18,21,29) that cortical connections can be mapped non-invasively and reproducibly in the human IC. However, none of these reports produced a comprehensive probabilistic map of cortical connections of the human IC. For example, the latest study identified sensorimotor connections only (21). Clearly, more accurate mapping can be achieved with the use of intracerebral electrical stimulation (2), but this method is highly invasive and therefore is not feasible for daily clinical use.

In this study we tried to map all of the cortical connections that pass through the IC (given the limitations of diffusion tensor imaging (DTI); see below). As expected, prefrontal connections were found mainly in the ALIC. The PLIC included connections with premotor, M1, S1, posterior parietal, temporal, and occipital cortices arranged approximately anteroposteriorly. To some extent, this anteroposterior organization reflects previous findings in studies that used DTI in adjacent gray matter structures, including the striatum (30) and thalamus (22). These similarities reflect a combination of genuine similarities in the topographic organization of these structures (echoing the anteroposterior organization of the cortex itself) and some partial-volume effects due to the limited spatial resolution of the imaging technique.

As expected, sensorimotor tracts were located in the posterior half of the PLIC (1,6,7,21,31). In monkeys these fibers occupy a large portion of the PLIC (17,32) and the premotor tracts extend into the ALIC (16). In humans, however, sensorimotor tracts are localized in the posterior third of the PLIC, and premotor tracts are not found as far anterior in the genu (2,3,31). We believe that the posterior shift of sensorimotor tracts in humans may be a consequence of the prominent development of the prefrontal cortex and its projection through the IC (7). Our study also shows considerable overlap between the premotor and M1 connections, and between the M1 and S1 connections. Because DTI tractography is unable to identify the direction of the fibers, the M1 tracts identified in the IC are not necessarily limited to the corticospinal fibers and probably also contain some afferent sensory fibers. In addition, previous histological studies demonstrated that the sensorimotor tracts include both ascending sensory and descending motor fibers (33). The overlap between M1 and premotor cortex may be related to a more general somatotopic organization of motor control efferents (16,34). The higher mask-to-IC ratio for the somatosensory and motor connections represents a relatively larger bundle of fibers in the IC. By defining the relative laterality of these connections, we may be able to further refine predictions regarding clinical outcomes following lateralized damage.

A better understanding of the anatomy of the IC and associated WM is potentially highly informative for the prediction of clinical outcomes. For example, it will be possible to ask whether damage to sensory or motor fibers predicts a worse prognosis for recovery of function in patients with stroke. The ability to characterize the IC using relatively short examinations may enable maps to be defined on patients on an individual basis (35). For example, in a patient with lacunar infarct in the right IC causing left-hand weakness, the coordinates of the lesion site on MRI would be expected to show high connectivity to the M1 region on our map.

Prefrontal connections occupy the anterior half of the volume of the IC. Previous studies observed localization of the prefrontal connections in the ALIC (10–12); however, our observations highlight the large volume in the IC that is occupied by these tracts—an aspect of the structure that is not well appreciated in most neuroanatomy text-books. This is because of the fact that our anatomical understanding of prefrontal connections originates from studies of these connections in nonhuman primates which have a much smaller prefrontal cortex than humans (12,36). Previous studies showed that the ALIC also contains prefrontotemporal fibers (37). Thalamoprefrontal and prefrontalbasal ganglia connections pass through the ALIC (12,13,38,39). Abundant connections of the prefrontal cortex and basal ganglia also pass through the ALIC (15). Most of these connections are with the caudate nucleus (10,36,40,41).

Posterior parietal connections occupied a proportion of the IC that was relatively small compared to the volume of the parietal cortex. The parietal cortex includes predominantly association cortices that receive connections from other cortical areas that do not necessarily pass through the IC (42,43). However, there is clear evidence that the posterior parietal cortex is connected to thalamic nuclei through the IC (44–47).

Temporal connections were identified in both the ALIC and PLIC. Anatomical studies confirmed that the ALIC contains frontotemporal connections (37,48,49). However, most voxels that were found to be connected to the ALIC in the hard segmentation map of some individuals were in fact the result of partial-volume effects from the head of caudate, which is connected to the temporal cortex. We tested this explanation by producing a probabilistic map of the caudate (unpublished data). True connections of the temporal lobe were identified in the PLIC. These are probably connections with the basal ganglia, thalamus, and occipitoparietal regions. There are also connections between temporal and occipital cortices (50–53) and between temporal and parietal cortices (46,54–56) that pass through the IC.

Occipital connections were found mostly in the lower IC mask at the most posterior part of the PLIC. This contribution may reflect connections between the higher-order visual cortex and the temporal lobe (57). However, connections from the rostral caudate to the occipital lobe do not pass through the IC, since they follow through the optic tracts and radiations. An additional factor contributing to this observation is partial volume effect from voxels related to the visual pathway that are adjacent to the PLIC.

There are a number of general limitations that are inherent to DTI tractography. It is difficult to trace pathways through regions of fiber crossing or complexity. For example, tracing paths from IC to lateral cortical areas is problematic because the fibers cross the superior longitudinal fasciculus. In this study we took a pragmatic approach to this problem by masking out the SLF region and linearly interpolating areas. The development of approaches to characterize fiber complexity (58,59) should make it possible to trace paths through crossing fiber regions, and it would be useful in future studies to confirm the organization we found here with more sophisticated tracing approaches.

In conclusion, DWI tractography can be used as a noninvasive technique to produce a reproducible map of cortical connections in the human IC. This map shows a clear topographic organization of cortical connections within the human IC, and may be useful for clinicoanatomical correlations of cerebral lesions.

Acknowledgments

We are grateful to T.E. Behrens, C.A. Wheeler-King-shott, P.A. Boulby, and G.J. Barker for their comments.

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