Figures and data in Neural dynamics of semantic categorization in semantic variant of primary progressive aphasia

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5 figures, 3 tables and 1 additional file

Figures

Figure 1

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Experimental paradigm, behavioral performance, and cortical atrophy.

(A) Cartoon representation of the experimental setting. Colored drawings were presented for 2 s, with an inter-stimuli interval jittered between 1.7 and 2.1 s. Subjects responded with a button press with their dominant hand. (B) Behavioral performance during the semantic categorization tasks in controls and semantic variant primary progressive aphasia (svPPA) patients, across the two stimuli conditions (living vs. nonliving items). There were no statistically significant effects of diagnosis, category, nor their interaction neither in percentage accuracy (healthy controls [HC]: living: 97.1 ± 6.6, nonliving: 96.8 ± 6.6; svPPA: living: 91.5 ± 6.2, nonliving: 95.9 ± 8.1) nor in reaction times (HC: living: 826.3 ± 112.5, nonliving: 856.9 ± 104.4; svPPA: living: 869.8 ± 179.8, nonliving: 911.1 ± 194.45). (C) Voxel-based morphometry (VBM)-derived atrophy pattern showing significantly reduced gray matter volumes in svPPA patients’ anterior temporal lobes, views from top to bottom: lateral, medial, ventral (thresholded at p<0.05 with family-wise error [FWE] correction, cluster threshold of 100 voxels).

Figure 2

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Stimulus-locked (0 ms = stimulus onset) within-group analyses of task-related changes in oscillatory power.

(a) Rendering of the results in the high-gamma band for both controls (healthy controls [HC], upper row) and patients (semantic variant primary progressive aphasia [svPPA], lower row). Cold color = more desynchronization (vs. baseline). Warm color = more synchronization (vs. baseline). (**c-e**) Same as in (a) but for the low-gamma, beta, alpha, and theta band, respectively. Within-group analyses were performed, with no additional smoothing, on normalized reconstructions using statistical nonparametric mapping (SnPM one-sample, two-tailed t-test against baseline).

Figure 3

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Stimulus-locked (0 ms = stimulus onset) between-group analyses of changes in oscillatory power.

Rendering of the results in the high-gamma (a), low-gamma (b), beta (c), alpha (d), and theta (e) bands. Purple color = more synchronization in semantic variant primary progressive aphasia (svPPA) (vs. healthy controls [HC]). Brown color = less synchronization in svPPA (vs. HC). Table 2 summarizes the temporal windows, peaks of local maxima, and t-values of all clusters isolated by the direct comparison of the two cohorts. Between-group analyses were performed, with no additional smoothing, on normalized reconstructions using statistical nonparametric mapping (SnPM two-sample, two-tailed t-test).

Figure 4

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Results of the region of interest post hoc analysis.

Three regions-of-interest (ROIs) of 20 mm radius were centered on the occipital pole (OCC, Montreal Neurological Institute [MNI]: −10, –94, −16), left ventral occipito-temporal cortex (VOT, MNI: −50, –52, −20), and left ATL (MNI: −30, –6, −40). Pink color represents healthy controls data, light blue svPPA patients. Shaded areas indicate the standard deviation around the group average (i.e., solid line).

Figure 5

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Results of the post hoc regions of interest analysis of power changes.

Full time-frequency plot of power changes in two representative voxels centered in the peak of activation (as per group results, Montreal Neurological Institute [MNI]: −34.8, –93.9, 2.7) and on the occipital pole (OCC, MNI: −10, –94, −16).

Tables

Table 1

Demographics and neuropsychological profiles.

Healthy controls and semantic variant of primary progressive aphasia (svPPA) patients, native English speakers, were matched for age, gender, and education. Scores shown are mean (standard deviation). * Indicates values significantly different from controls (p<0.05). MMSE = Mini-Mental State Exam; CDR = Clinical Dementia Rating; PPVT = Picture Vocabulary Test; WAB = Western Aphasia Battery; VOSP = Visual Object and Space Perception Battery.

	Controls	svPPA
Demographic
N	18	18
Age, mean (SD)	70.7 ± 6.5	67.1 ± 6.2
Education, mean (SD)	17.5 ± 1.8	17.9 ± 3.2
Gender, n female	12	9
Handedness, n right	15	15
MMSE (max. 30)	29.0 ± 1.6	24.5 ± 3.8*
CDR score	0.03 ± 0.1	0.7 ± 0.4*
CDR box score	0.3 ± 1.2	4.0 ± 2.6*
Language production
Boston (object) naming test (15)	14.7 ± 0.6	5.4 ± 3.7*
Phonemic (D-letter) fluency	15.7 ± 5.8	9.1 ± 4.3*
Semantic (animal) fluency	23.4 ± 3.9	9.3 ± 4.1*
Language comprehension
PPVT (max. 16)	–	9.4 ± 3.2
WAB auditory word recognition (60)	–	56.5 ± 4.2
WAB sequential command (100)	–	70.7 ± 14.3
Digit span forwards	7.1 ± 1.1	6.4 ± 1.2
Reading
Arizona reading total (max. 36)	35.6 ± 0.5	30.5 ± 3.7*
Regular high-frequency words (9)	9 ± 0.0	8.8 ± 0.4
Regular low-frequency words (9)	8.9 ± 0.2	8.3 ± 1.2
Irregular high-frequency words (9)	8.9 ± 0.3	7.7 ± 0.6
Irregular low-frequency words (9)	8.8 ± 0.4	5.7 ± 2.3
Pseudowords (18)	15.8 ± 2.7	15.2 ± 2.2
Spelling
Arizona spelling total (max. 20)	18.1 ± 1.6	13.1 ± 4.0*
Regular high-frequency words (5)	5 ± 0.0	4.4 ± 0.9
Regular low-frequency words (5)	4.5 ± 0.6	4.1 ± 0.8
Irregular high-frequency words (5)	4.1 ± 0.9	2.1 ± 1.6
Irregular low-frequency words (5)	4.5 ± 0.5	2.6 ± 1.6
Pseudowords (10)	8.8 ± 1.3	8.1 ± 2.6
Famous faces – spontaneous naming (max. 16)	12.4 ± 3.4	2.9 ± 2.4*
Famous faces – face recognition (max 20)	18.4 ± 2.0	12.8 ± 6.5*
Famous faces short triplets, pictures (max. 10)	8.9 ± 1.0	6.6 ± 2.4
Famous faces short triplets, words (max. 10)	9.7 ± 0.6	7.0 ± 2.0
Working memory/executive functions
Digit span backwards	5.4 ± 1.1	4.5 ± 1.6*
Modified trials (total time)	25.3 ± 13.6	41.9 ± 23.1*
Modified trials (# of correct lines)	13.2 ± 3.2	13.2 ± 3.3
Design fluency (# of correct designs)	11.7 ± 3.0	7.1 ± 3.4*
Visuospatial function
Benson figure copy (17)	15.7 ± 0.7	15.3 ± 1.0
VOSP number location (30)	9.3 ± 0.9	9.0 ± 1.5
Visual memory
Benson figure recall (17)	12.1 ± 2.4	7.1 ± 4.9*

Table 2

Local maxima in Montreal Neurological Institute (MNI) coordinates.

Time window, MNI coordinates, p- and t-value of the local maxima of the different magnetoencephalographic (MEG) whole brain contrasts performed. The spatiotemporal distribution of these clusters at four exemplar time points can be appreciated in Figure 3.

	Time window	Local maxima
t-test svPPA vs. HC	ms	MNI [x,y,z]	p-value	t-value
Theta band [3–7 Hz]
Left lingual gyrus	0–212	−10.0 –100.0 −10.0	0.005	3.7	More ERD in svPPA
Left lingual gyrus	412–612	−8.5 –100.0 −8.1	0.005	3.1	More ERD in svPPA
Right medial and superior frontal gyrus	187–387	18.6 61.4 –14.7	0.001	−3.92	Less ERS in svPPA
Alpha band [8–12 Hz]
Right precentral gyrus	212–612	45.0 –15.0 40.0	0.001	3.4	More ERD in svPPA
Left middle temporal gyrus	287–362	−59.8 –41.6 −1.0	0.005	2.8	More ERD in svPPA
Bilateral medial and orbital frontal gyrus	462–612	−6.2 34.3 –24.9	0.001	5.1	More ERS in svPPA
Beta band [12–30 Hz]
Left cingulate cortex	0–62	−6.2–30.3 43.3	0.005	2.9	More ERS in svPPA
Right medial frontal gyrus	137–262	7.8 56.8 11.7	0.001	3.6	More ERS in svPPA
Left middle temporal gyrus	237–362	−65.0 –20.0 −5.0	0.001	−3.4	Less ERD in svPPA
Left superior frontal gyrus	587–612	−21.8 46.7 45.7	0.005	−3.1	Less ERD in svPPA
Low-gamma band [30–55 Hz]
Left lingual gyrus	62–612	−10.1–98.4 −8.9	0.001	4.2	More ERS in svPPA
Left inferior occipital gyrus	362–612	−34.8 –93.9 2.7	0.001	4.1	More ERS in svPPA
Right lingual gyrus	212–437	18.2 –89.1 8.3	0.005	3.4	More ERS in svPPA
Right medial frontal gyrus	212–412	9.3 63.0 2.2	0.001	3.7	Less ERD in svPPA
Left superior frontal gyrus	262–462	−3.8 62.8 14.0	0.005	3.6	Less ERD in svPPA
High-gamma band [63–117 Hz]
Left superior frontal gyrus	62–137	−36.5 26.6 48.8	0.001	3.4	More ERS in svPPA
Left superior temporal gyrus	62–287	−48.2 –22.3 13.3	0.005	3	More ERS in svPPA
Left parahippocampal gyrus	212–312	−15.5 –27.1 −6.5	0.001	3.3	More ERS in svPPA
Right medial frontal gyrus	287–337	13.2 70.7 0.6	0.005	3.2	More ERS in svPPA
Left superior frontal gyrus	287–612	−22 68.4 14	0.001	3.6	More ERS in svPPA
Right superior frontal gyrus	462–612	43.9 54.7 17.2	0.001	3.9	More ERS in svPPA

Table 3

Psycholinguistic characteristics of the stimuli.

Stimuli consisted of 70 colored drawings illustrating living items (n = 36) or nonliving items (n = 34). Length, imaginability, concreteness, and familiarity (norm) were extracted from the Medical Research Council (MRC) Psycholinguistic Database searching for the most common label for each item. Similarly, frequency was extracted from the Corpus of Contemporary American English (COCA). Category agreement, category prototypicality, and familiarity (quest.) were assessed with a behavioral study on separate age-matched healthy controls. As a proxy for visual complexity, we used Shannon entropy as computed with Scikit-Image. Values shown are mean (standard deviation). * Indicate values significantly different between the two categories (two-tailed t-test, p<0.05).

	Living items	Nonliving items
N	36	34
Examples	Fish, flower	Scissors, train
Frequency (log)	3.69 (0.54)	3.96 (0.65)
Length (# of letters)	5.29 (1.58)	5.61 (1.84)
Imageability	613.19 (19.62)	596.43 (28.08)	*
Familiarity (norm)	498.26 (69.32)	547.96 (45.82)	*
Familiarity (quest.)	6.15 (0.32)	6.67 (0.21)	*
Concreteness	608.27 (16.26)	599.10 (25.94)
Category agreement	96.86 (4.07)	99.18 (1.20)	*
Category prototypicality	6.24 (0.52)	6.47 (0.32)	*
Visual complexity	3.04 (0.84)	3.13 (0.96)