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. 2008 Jul;100(1):129-39.
doi: 10.1152/jn.00077.2008. Epub 2008 Apr 2.

Distinct cortical anatomy linked to subregions of the medial temporal lobe revealed by intrinsic functional connectivity

Itamar Kahn  1 , Jessica R Andrews-Hanna, Justin L Vincent, Abraham Z Snyder, Randy L Buckner
Affiliations

Distinct cortical anatomy linked to subregions of the medial temporal lobe revealed by intrinsic functional connectivity

Itamar Kahn et al. J Neurophysiol. 2008 Jul.

Abstract

The hippocampus and adjacent cortical structures in the medial temporal lobe (MTL) contribute to memory through interactions with distributed brain areas. Studies of monkey and rodent anatomy suggest that parallel pathways converge on distinct subregions of the MTL. To explore the cortical areas linked to subregions of the MTL in humans, we examined cortico-cortical and hippocampal-cortical correlations using high-resolution, functional connectivity analysis in 100 individuals. MTL seed regions extended along the anterior to posterior axis and included hippocampus and adjacent structures. Results revealed two separate brain pathways that correlated with distinct subregions within the MTL. The body of the hippocampus and posterior parahippocampal cortex correlated with lateral parietal cortex, regions along the posterior midline including posterior cingulate and retrosplenial cortex, and ventral medial prefrontal cortex. By contrast, anterior hippocampus and the perirhinal/entorhinal cortices correlated with distinct regions in the lateral temporal cortex extending into the temporal pole. The present results are largely consistent with known connectivity in the monkey and provide a novel task-independent dissociation of the parallel pathways supporting the MTL memory system in humans. The cortical pathways include regions that have undergone considerable areal expansion in humans, providing insight into how the MTL memory system has evolved to support a diverse array of cognitive domains.

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Figures

FIG. 1.
FIG. 1.
Major anatomic landmarks in the parietal, temporal, and medial temporal lobes. A: reconstructed cortical representation of a typical participant illustrates the various display formats used in this paper. Views of the lateral and medial aspects of the brain show locations of major anatomical landmarks; a view of the ventral aspect shows the location of the medial temporal lobe section analyzed extensively in this paper (outlined in yellow). B: inflated representation of the cortex is shown to the left of a flattened representation of the medial temporal lobe. C: coronal slices of the group average overlaid with an outline of the cortical gray matter ribbon (white) and labels of cortical subdivisions based on estimates of architectonically defined areas and anatomical landmarks. The labels were derived from a probabilistic atlas that takes into account inter-subject variance of the region ( Desikan et al. 2006; Fischl et al. 2002, 2004). CaS, calcarine sulcus; CoS, collateral sulcus; CS, central sulcus; HF, hippocampal fissure; IPS, intraparietal sulcus; ITS, inferior temporal sulcus; OTS, occipitotemporal sulcus; STS, superior temporal sulcus.
FIG. 2.
FIG. 2.
Signal-to-noise estimates for the present 2 data sets. A: lateral and medial views depict relatively uniform signal-to-noise across the 2 groups. B: flattened representation of the medial temporal lobe demonstrates that signal dropout is predominant between the occipitotemporal and inferior temporal sulci. Formats of the surface representations are illustrated in Fig. 1.
FIG. 3.
FIG. 3.
Seed regions in the medial temporal lobe of the left hemisphere. A: sagittal slices of the group-averaged structural images depict the seed locations (blue dots) along the long axis of the hippocampus and the collateral sulcus. B: a flattened patch of the medial temporal lobe is shown with the 16 seed locations (white dots) depicted. The seeds cover the hippocampus and the medial temporal lobe including the parahippocampal and perirhinal/entorhinal cortices. Coordinates here and elsewhere refer to the atlas coordinate system of the Montreal Neurological Institute (MNI) template (see text).
FIG. 4.
FIG. 4.
Distinct cortical regions are correlated with the perirhinal/entorhinal cortices (PRc/ERc) and parahippocampal cortex (PHc). Correlation maps are illustrated for 2 seed regions along the collateral sulcus. PRc/ERc (MNI coordinates [−26 −20 −30]) and PHc ([−26 −40 −12]) seeds defined as 3-mm spheres are depicted on coronal slices of group-averaged structural image. An outline of the cortical gray matter is depicted on the left. Seed locations are depicted in black on coronal slices and as black stars on the cortical ribbon outline. Correlation maps were obtained after within-subject transformation using Fisher's r-to-z and submitted for a second level analysis using a random effects model (threshold P < 0.001). Two distinct patterns of correlated activity were observed. A: the PRc/ERc correlated with the anterior aspect of the lateral temporal lobe. B: in contrast, the PHc was correlated with lateral and medial parietal and ventral medial prefrontal cortices.
FIG. 5.
FIG. 5.
Distinct cortical regions are correlated with the perirhinal/entorhinal (PRc/ERc) and the body of the hippocampus (bHipp). Correlation maps are illustrated for 2 seed regions in the anterior part of the collateral sulcus (PRc/ERc) and in the hippocampus. A: PRc/ERc (MNI coordinates [−26 −20 −30]) and bHipp (−24 −18 −18) seeds defined as 3-mm spheres are depicted on coronal slices of group average T1-weighted MR images. An outline of the cortical gray matter is depicted below. Seed locations are depicted in black on coronal slices and as black stars on the cortical ribbon outline. Random effects maps (P < 0.001) were obtained after within-subject transformation using Fisher's r-to-z and submitted for a second level analysis. B: 2 distinct patterns of correlated cortical activity were observed. An overlap map for both left and right hemispheres demonstrates that the PRc/ERc was correlated with the anterior lateral temporal lobe (blue), the bHipp was correlated with lateral parietal, posterior cingulate/retrosplenial, as well as medial prefrontal cortices (red). Overlap in correlated activity is shown along the collateral sulcus (yellow). Note the close proximity of the seeds and consistent bilateral activation for both seeds.
FIG. 6.
FIG. 6.
Anterior inferior temporal sulcus (aITS) and inferior parietal lobule (IPL) correlate with distinct subregions of the MTL. Correlated activity relative to seed regions in aITS (MNI coordinates [−50 −2 −32]) and IPL ([−44 −78 38]) are depicted for the 2 independent groups. Data Set 1 was used to define the seeds and Data Set 2 is a fully independent replication of the correlation patterns in MTL. A: the anterior lateral temporal and inferior parietal lobe regions were defined in Data Set 1 based on their preferential correlation with the anatomically defined body and head of the hippocampus (bHipp and hHipp) seed regions, respectively (depicted in black on coronal slices and as black stars on the cortical ribbon outline). The aITS and IPL regions were applied to Data Set 2. Estimated areas based on architectonic and landmark-based subdivisions of the MTL (see text) are depicted on coronal slices of group-averaged T1-weighted MR images, and an outline of the cortical gray matter and seed locations (black stars) are depicted to the left. B: the correlation maps from Data Set 1 are displayed for aITS (left) and IPL (right). The original, anatomically defined MTL seeds are depicted as circles outlined in black and the critical origin seeds in the MTL are depicted as filled circles. C: correlation maps for Data Set 2 are shown, representing an independent replication of the dissociation. Note the close similarity in the patterns of correlation observed between the 2 groups. D: correlation values z(r) are presented for each of the 2 cortical seeds of the 16 MTL regions. These values come from Data Set 2 and thus provide unbiased statistical tests. Seed regions shaded in gray are significantly different between the 2 cortical seeds and demonstrate an anterior-posterior dissociation. Anterior seed regions show significantly greater correlation with aITS (left), whereas posterior seed regions show greater correlation with IPL (right; all Pcorr < 0.05). Correlation values significantly different from 0 are in bold (Pcorr < 0.05).
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