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Categorization is the mental operation by which the brain classifies objects and events. It is classically assessed using semantic and non-semantic matching or sorting tasks. These tasks show a high variability in performance across healthy controls and the cerebral bases supporting this variability remain unknown. In this study we performed a voxel-based morphometry study to explore the relationships between semantic and shape categorization tasks and brain morphometric differences in 50 controls. We found significant correlation between categorization performance and the volume of the gray matter in the right anterior middle and inferior temporal gyri. Semantic categorization tasks were associated with more rostral temporal regions than shape categorization tasks. A significant relationship was also shown between white matter volume in the right temporal lobe and performance in the semantic tasks. Tractography revealed that this white matter region involved several projection and association fibers, including the arcuate fasciculus, inferior fronto-occipital fasciculus, uncinate fasciculus, and inferior longitudinal fasciculus. These results suggest that categorization abilities are supported by the anterior portion of the right temporal lobe and its interaction with other areas.
• Anterior temporal lobe morphometry correlates with categorization performances
• Semantic is associated with a more rostral temporal region than shape categorization
• Semantic categorization performances are associated with right temporal connections.
Categorization is the mental operation by which the brain classifies objects and events. The ability to categorize information has an impact in virtually all domains of cognition and behavior, from learning (children learn new concepts by categorizing items that look similar or have similar properties) to survival (to recognize an animal as dangerous, primates need to categorize it as similar to a previously encountered dangerous animal).
The evaluation of categorization abilities relies on various tests, including semantic and visual categorization tests. Semantic categorization abilities are usually assessed by matching tests based on taxonomic or thematic categorization, such as the Pyramid and Palm Tree Test (PPT test) (
Functional neuroimaging studies in healthy subjects, as well as electrophysiological studies in primates, have shown the involvement of various brain regions in categorization tasks. For instance, the ventrolateral prefrontal cortex (PFC) (
Regarding brain structure, the exact shape of every human brain is unique, resulting in inter-individual anatomical variability (
Fifty right-handed native French speakers (25 females; age 22–71 years, mean = 47 ± 14.3 years) participated in the study. A large age range was chosen to represent the diversity of the general population. All participants were healthy adults with no history of neurological or psychiatric disorders and no abnormalities were revealed on their structural MRI. Participants had an average of 15.4 ± 3.0 years of education (range, 10–26). They had no cognitive impairment as assessed with the Mini Mental State Examination (
We used a short version of the categorization paradigm described in a previous functional imaging study (
Stimuli consisted of triads of black-and-white drawings of real-life objects that were displayed on a computer screen. One drawing at the top of the screen was framed; the two other drawings were located at the bottom left and right sides of the screen (
Samples of stimuli. The framed drawing was compared with the two bottom ones according to four possible instructions:
The 160 stimuli were divided into four sets of 40 stimuli each. Each set was assigned to one of the four following tasks: the
Stimulus presentation was programmed on a PC using meyeParadigm 1.17 software
Accuracy and response times (RTs) were measured and statistical analyses were conducted using SPSS software
All participants underwent the same high-resolution T1-weighted structural MRI scans acquired on a Siemens 3 Tesla VERIO TIM system equipped with a 32-channel head coil. An axial 3D MPRAGE dataset covering the whole head was acquired for each participant as follows: 176 slices, voxel resolution = 1 mm × 1 mm × 1 mm, TE = 2.98 ms, TR = 2300 ms, flip angle = 9°.
3D T1-weighted sequences were processed and analyzed with SPM8 (Wellcome Department of Imaging Neuroscience, London, United Kingdom) running on Matlab (Mathworks Inc., United States).
To investigate the relationship between VBM regional gray matter (GM) structural variability and different aspects of categorization, we ran multiple regression analyses in SPM8 between GM volume and behavioral scores. RTs for accurate responses were used for the analyses because of a ceiling effect in accuracy. First, the averaged scores in the Category dimension (
To investigate the relationship between VBM regional white matter (WM) density and different aspects of categorization, we ran multiple regression analyses in SPM8 between WM volume and behavioral scores. We used the same models and covariates as for the GM VBM analyses. Data were also normalized and corrected for individual total WM volume by entering their values as covariates in the linear model. For each regression analysis, we investigated significant results at
The functions of brain regions depend on their connectivity with other brain regions. Therefore, anatomical connectivity of the VBM results was investigated in a connectivity study using diffusion images. We explored the connections terminating in and emerging from the brain regions identified in the WM VBM in 44 out of the 50 participants (22 females; age 22–71 years, mean = 46.5 ± 14.5 years).
A total of 70 near-axial slices were acquired during the same MRI session as T1 images. We used an acquisition sequence fully optimized for tractography of DWI that provided isotropic (2 mm × 2 mm × 2 mm) resolution and coverage of the whole head. The acquisition was peripherally gated to the cardiac cycle with an echo time (TE) of 85 ms. We used a repetition time (TR) equivalent to 24 RR. At each slice location, six images were acquired with no diffusion gradient applied. Sixty diffusion-weighted images were acquired in which gradient directions were uniformly distributed in space. Diffusion weighting was equal to a
One supplementary image with no diffusion gradient applied but with reversed phase-encode blips was collected. This step provided us with a pair of images with no diffusion gradient applied and distortions going in opposite directions. From these pairs, the susceptibility-induced off-resonance field was estimated using a method similar to that described in
Spherical deconvolution was chosen to estimate multiple orientations in voxels containing different populations of crossing fibers (
Whole-brain tractography was performed by selecting every brain voxel with at least one fiber orientation as a seed voxel. From these voxels and for each fiber, orientation streamlines were propagated using Euler integration with a step size of 1 mm. When entering a region with crossing WM bundles, the algorithm followed the orientation vector of the least curvature (
The significant results of WM VBM analysis were used as regions of interest (ROIs) for tract dissections. We dissected the tracts connecting the observed ROIs associated with
In short, each participant’s convergence speed maps (
Behavioral data. Histograms represent means ± standard errors of the mean. ∗∗∗
The mean error rate was low (mean: 3.2%, all conditions included). Repeated measures two-way ANOVAs revealed no effect of dimension [i.e.,
Repeated measures two-way ANOVA revealed a significant effect of dimension [
Age was significantly positively correlated with RT in all conditions:
Gray matter VBM–whole brain analysis: negative GM correlations with RT in Shape, Category, Same, and Different tasks at
Brain region | Side | BA | MNI coordinate (maxima) | Cluster size | Cluster-level |
||
---|---|---|---|---|---|---|---|
Shape | Middle and inferior temporal gyrus | R | 20/21 | 56 -19 -20 | 4.74 | 679 | 0.044 |
Category | Temporal pole, middle and inferior temporal gyrus | R | 20/21/38 | 57 -2 -27 | 4.97 | 1558 | 0.003 |
Same | Temporal pole, middle and inferior temporal gyrus | R | 20/21 | 57 -13 -20 | 5.00 | 1352 | 0.004 |
Different | Middle and inferior temporal gyrus | R | 20/21 | 57 -16 -21 | 4.41 | 1308 | 0.009 |
Results from the whole-brain GM VBM analysis according to dimension.
Voxel-wise multiple regression analyses of RTs for each task dimension (
At an FWE-corrected threshold, RTs in the
To illustrate this finding, we examined the functional profile of
At an FWE-corrected threshold, RTs in the
At
At an FWE-corrected threshold, RTs in the
White matter (WM) correlations with RT in Category at
Negative correlation | Brain region | Side | MNI coordinate | Cluster size | Cluster-level |
|
---|---|---|---|---|---|---|
Category | Temporal lobe | R | 48 -9 -27 | 4.92 | 689 | 0.023 |
Results from whole-brain WM analysis.
At
The connectome representing fibers connecting the right temporal WM region associated with category performance included projection fibers from the right arcuate fasciculus (AF, long segment), inferior fronto-occipital fasciculus (IFOF), uncinate fasciculus (UF), inferior longitudinal fasciculus (ILF), and commissural fibers encompassing the anterior commissure and corpus callosum (splenium).
In this study we performed a voxel-based morphometry study to explore the relationship between semantic and shape categorization tasks and morphometric differences in the brain. Three findings emerge from our work. Firstly, our results revealed a significant correlation between subjects’ performance in terms of RT in all conditions and dimensions, and the volume of the right anterior middle and inferior temporal gyri encompassing the ATL. Secondly, the semantic (
Interindividual variability in RTs in categorization tasks was related to the GM volume in the right lateral temporal regions. Subjects who were faster to categorize drawings had higher GM volume in the right anterior middle and inferior temporal gyri. To our knowledge, this study is the first to show a correlation between categorization abilities and regional GM volume in healthy participants. This result suggests the role of the lateral part of the right ATL in categorization. Our results are consistent with previous studies that showed a correlation between conceptual processing performances in healthy subjects and resting functional connectivity in the ATL (
Previous functional imaging data inconsistently showed the involvement of the ATL during perceptual or semantic categorization tasks. Some authors showed an activation of the ATL (
Previous functional imaging data showed the involvement of both the right and left lateral and inferior temporal cortices (
We cannot exclude that the right lateralization of the main effects in our study can be due to more structural variability on the right ATL than on the left ATL.
Overall, our results complete previous functional imaging findings by demonstrating the relationship between the ability to categorize and the structure of the anterior temporal cortex.
We showed a rostrocaudal specialization within the temporal lobe: performance in the semantic (
VBM of the WM and connectivity analyses showed a correlation between RTs in semantic categorization (
IFOF, UF, and AF connect the ATL with the frontal lobe. More specifically, the IFOF and UF connect the ATL with medial and lateral orbitofrontal PFC, whereas the AF connects the ATL with the ventrolateral PFC (
We could not exclude that variable processing speed may have influenced our results, because our findings were based on RTs and not accuracy. A previous study performed on 367 healthy subjects found a correlation between processing speed as assessed by the part A of the Trail Making Test (
Additionally, the physiological significance of GM volume correlation remains unclear. For instance, performances negatively correlated with GM volume of the PFC. Correlations between cognition and GM volume, notably in the PFC, do not always respond to the assertion “bigger is better.” Some studies have reported a positive correlation (
Our results showed the role of the right ATL in categorization abilities in healthy subjects. This study suggested a rostrocaudal specialization in the temporolateral cortex according to the nature of the category. Semantic category judgment was associated with more anterior regions than visuoperceptual category judgment. To our knowledge, this is the first study on the cerebral basis of interindividual variability of categorization abilities. The results add to the current knowledge of the cerebral basis of categorization.
BG: conception, organization, execution of the research project, design and execution of statistical analysis, writing of the first draft and revision of the manuscript. MU and MT: design and execution of statistical analysis, review and critique of manuscript. RL: conception of research project, review and critique of manuscript. EV: conception, organization, execution of the research project, design and execution of statistical analysis, revision of the manuscript.
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
This work was supported by the ‘Fondation pour la Recherche Médicale’ (FRM) [grant numbers FDM20150632801 and DEQ20150331725]. Additional support comes from the ‘Agence Nationale de la Recherche,’ [grants numbers ANR-09-RPDOC-004-01 and ANR-13-JSV4-0001-01]. The research leading to these results received funding from the program ‘Investissements d’avenir’ ANR-10-IAIHU-06.
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