Current neurocognitive models of language function have been primarily built from evidence regarding object naming, and their hypothesized white-matter circuit mechanisms tend to be coarse grained.
Methods:
In this cross-sectional, observational study, we used novel correlational tractography to assess the white-matter circuit mechanism behind verb retrieval, measured through action picture-naming performance in adults with chronic aphasia.
Results:
The analysis identified tracts implicated in current neurocognitive dual-stream models of language function, including the left inferior fronto-occipital fasciculus, inferior longitudinal fasciculus, and arcuate fasciculus. However, the majority of tracts associated with verb retrieval were not ones included in dual-stream models of language function. Instead, they were projection pathways that connect frontal and parietal cortices to subcortical regions associated with motor functions, including the left corticothalamic pathway, frontopontine tract, parietopontine tract, corticostriatal pathway, and corticospinal tract.
Conclusions:
These results highlight that corticosubcortical projection pathways implicated in motor functions may be importantly related to language function. This finding is consistent with grounded accounts of cognition and may furthermore inform neurocognitive models.
Impact statement
This study suggests that in addition to traditional dual-stream language fiber tracts, the integrity of projection pathways that connect frontal and parietal cortices to subcortical motor regions may be critically associated with verb-retrieval impairments in adults with aphasia. This finding challenges neurological models of language function.
Get full access to this article
View all access options for this article.
References
1.
AkininaY, DragoyO, IvanovaMV, et al.2019. Grey and white matter substrates of action naming. Neuropsychologia, 131:249–265.
2.
BakTH. 2013. The neuroscience of action semantics in neurodegenerative brain diseases. Curr Opin Neurol, 26:671–677.
3.
BarsalouLW. 2008. Grounded cognition. Annu Rev Psychol, 59:617–645.
4.
BelloL, GambiniA, CastellanoA, et al.2008. Motor and language DTI Fiber Tracking combined with intraoperative subcortical mapping for surgical removal of gliomas. Neuroimage, 39:369–382.
5.
BubbEJ, Metzler-BaddeleyC, AggletonJP. 2018. The cingulum bundle: anatomy, function, and dysfunction. Neurosci Biobehav Rev, 92:104–127.
6.
CaramazzaA, HillisAE. 1991. Lexical organization of nouns and verbs in the brain. Nature, 349:788–790.
7.
ChoS-H, KimDG, KimD-S, et al.2007. Motor outcome according to the integrity of the corticospinal tract determined by diffusion tensor tractography in the early stage of corona radiata infarct. Neurosci Lett, 426:123–127.
8.
DamasioAR. 1989. The brain binds entities and events by multiregional activation from convergence zones. Neural Comput, 1:123–132.
9.
de ChampfleurNM, MaldonadoIL, Moritz-GasserS, et al.2013. Middle longitudinal fasciculus delineation within language pathways: a diffusion tensor imaging study in human. Eur J Radiol, 82:151–157.
10.
DellGS, SchwartzMF, NozariN, et al.2013. Voxel-based lesion-parameter mapping: identifying the neural correlates of a computational model of word production. Cognition, 128:380–396.
11.
DeLongMR, WichmannT. 2007. Circuits and circuit disorders of the basal Ganglia. Arch Neurol, 64:20–24.
12.
DuffauH, GatignolP, Moritz-GasserS, et al.2009. Is the left uncinate fasciculus essential for language? A cerebral stimulation study. J Neurol, 256:382–389.
13.
DuffauH, Moritz-GasserS, MandonnetE. 2014. A re-examination of neural basis of language processing: proposal of a dynamic hodotopical model from data provided by brain stimulation mapping during picture naming. Brain Lang, 131:1–10.
14.
EdmondsLA. 2016. A review of verb network strengthening treatment: theory, methods, results, and clinical implications. Top Lang Disord, 36:123–135.
15.
Fernández-MirandaJC, WangY, PathakS, et al.2015. Asymmetry, connectivity, and segmentation of the arcuate fascicle in the human brain. Brain Struct Funct, 220:1665–1680.
16.
FiezJA, TranelD. 1997. Standardized stimuli and procedures for investigating the retrieval of lexical and conceptual knowledge for actions. Memory Cogn, 25:543–569.
17.
FolsteinMF, FolsteinSE, McHughPR. 1975. “Mini-mental state”: a practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res, 12:189–198.
18.
GerfoEL, OliveriM, TorrieroS, et al.2008. The influence of rTMS over prefrontal and motor areas in a morphological task: grammatical vs. semantic effects. Neuropsychologia, 46:764–770.
19.
GlasserMF, RillingJK. 2008. DTI tractography of the human brain's language pathways. Cerebral Cortex, 18:2471–2482.
20.
GoodglassH. 1993. Understanding aphasia. New York, NY: Academic Press. p. 297.
21.
HamerPCDW, Moritz-GasserS, GatignolP, et al.2011. Is the human left middle longitudinal fascicle essential for language? A brain electrostimulation study. Hum Brain Mapp, 32:962–973.
22.
HanZ, MaY, GongG, et al.2013. White matter structural connectivity underlying semantic processing: evidence from brain damaged patients. Brain, 136:2952–2965.
23.
HaukO, JohnsrudeI, PulvermüllerF. 2004. Somatotopic representation of action words in human motor and premotor cortex. Neuron, 41:301–307.
24.
HickokG, PoeppelD. 2007. The cortical organization of speech processing. Nat Rev Neurosci, 8:393–402.
25.
HulaWD, PanesarS, GravierM, et al.2020. Structural white matter connectometry of word production in aphasia. Brain, 143:2532–2544.
26.
JankowskiMM, RonnqvistKC, TsanovM, et al.2013. The anterior thalamus provides a subcortical circuit supporting memory and spatial navigation. Front Syst Neurosci, 7:45.
27.
KemmererD, RudraufD, ManzelK, et al.2012. Behavioral patterns and lesion sites associated with impaired processing of lexical and conceptual knowledge of actions. Cortex, 48:826–848.
28.
KinoshitaM, de ChampfleurNM, DeverdunJ, et al.2015. Role of fronto-striatal tract and frontal aslant tract in movement and speech: an axonal mapping study. Brain Struct Funct, 220:3399–3412.
29.
Kronfeld-DueniasV, AmirO, Ezrati-VinacourR, et al.2016. The frontal aslant tract underlies speech fluency in persistent developmental stuttering. Brain Struct Funct, 221:365–381.
LiuzziG, FreundliebN, RidderV, et al.2010. The involvement of the left motor cortex in learning of a novel action word lexicon. Curr Biol, 20:1745–1751.
32.
LoversoF, PrescottT, SelingerM. 1987. Cueing verbs: a treatment strategy for aphasic adults (CVT). J Rehabil Res Dev, 25:47–60.
33.
MartinA. 2016. GRAPES-Grounding representations in action, perception, and emotion systems: How object properties and categories are represented in the human brain. Psychon Bull Rev, 23:979–990.
34.
MätzigS, DruksJ, MastersonJ, et al.2009. Noun and verb differences in picture naming: past studies and new evidence. Cortex, 45:738–758.
35.
McNeilMR, PrattSR. 2001. Defining aphasia: some theoretical and clinical implications of operating from a formal definition. Aphasiology, 15:901–911.
36.
MiceliG, SilveriMC, NocentiniU, et al.1988. Patterns of dissociation in comprehension and production of nouns and verbs. Aphasiology, 2:351–358.
37.
MorrisLS, KunduP, DowellN, et al.2016. Fronto-striatal organization: defining functional and microstructural substrates of behavioural flexibility. Cortex, 74:118–133.
38.
ParlatiniV, RaduaJ, Dell'AcquaF, et al.2017. Functional segregation and integration within fronto-parietal networks. Neuroimage, 146:367–375.
39.
PulvermüllerF. 2005. Brain mechanisms linking language and action. Nat Rev Neurosci, 6:576–582.
40.
PulvermüllerF. 2018. Neural reuse of action perception circuits for language, concepts and communication. Progr Neurobiol, 160:1–44.
41.
RavenJC. 1965. Guide to Using the Coloured Progressive Matrices: Sets A, Ab, B. Boston, MA: William Grieve & Sons.
42.
RoachA, SchwartzMF, MartinN, et al.1996. The Philadelphia naming test: scoring and rationale. Clin Aphasiol, 24:121–134.
43.
RobertsA, NguyenP, OrangeJB, et al.2017. Differential impairments of upper and lower limb movements influence action verb processing in Parkinson disease. Cortex, 97:49–59.
44.
RoelofsA. 2014. A dorsal-pathway account of aphasic language production: The WEAVER++/ARC model. Cortex, 59:33–48.
45.
RojkovaK, VolleE, UrbanskiM, et al.2016. Atlasing the frontal lobe connections and their variability due to age and education: a spherical deconvolution tractography study. Brain Struct Funct, 221:1751–1766.
46.
SaurD, KreherBW, SchnellS, et al.2008. Ventral and dorsal pathways for language. Proc Natl Acad Sci USA, 105:18035–18040.
47.
SierpowskaJ, GabarrósA, Fernandez-CoelloA, et al.2015. Morphological derivation overflow as a result of disruption of the left frontal aslant white matter tract. Brain Lang, 142:54–64.
48.
StefaniakJD, HalaiAD, Lambon RalphMA. 2020. The neural and neurocomputational bases of recovery from post-stroke aphasia. Nat Rev Neurol, 16:43–55.
TranelD, AdolphsR, DamasioH, et al.2001. A neural basis for the retrieval of words for actions. Cogn Neuropsychol, 18:655–674.
51.
VassalF, BoutetC, LemaireJ-J, et al.2014. New insights into the functional significance of the frontal aslant tract: an anatomo–functional study using intraoperative electrical stimulations combined with diffusion tensor imaging-based fiber tracking. Br J Neurosurg, 28:685–687.
52.
ViglioccoG, VinsonDP, DruksJ, et al.2011. Nouns and verbs in the brain: a review of behavioural, electrophysiological, neuropsychological and imaging studies. Neurosci Biobehav Rev, 35:407–426.
53.
WatkinsKE, JenkinsonN. 2016. Chapter 8—The Anatomy of the Basal Ganglia.In: Hickok G, Small SL (eds.) Neurobiology of Language. San Diego: Academic Press. p. 85.
54.
WelniarzQ, DusartI, RozeE. 2017. The corticospinal tract: evolution, development, and human disorders. Dev Neurobiol, 77:810–829.
55.
WurmMF, CaramazzaA. 2019. Distinct roles of temporal and frontoparietal cortex in representing actions across vision and language. Nat Commun, 10:289.
56.
YehF-C, TangP-F, TsengW-YI. 2013. Diffusion MRI connectometry automatically reveals affected fiber pathways in individuals with chronic stroke. Neuroimage Clin, 2:912–921.
57.
YehF-C, BadreD, VerstynenT. 2016. Connectometry: a statistical approach harnessing the analytical potential of the local connectome. Neuroimage, 125:162–171.
58.
YehF-C, PanesarS, BarriosJ, FernandesD, AbhinavK, MeolaA, Fernandez-MirandaJC. 2019. Automatic removal of false connections in diffusion MRI tractography using topology-informed pruning (TIP). Neurotherapeutics, 16:52–58.
59.
ZhuLL, LindenbergR, AlexanderMP, et al.2010. Lesion load of the corticospinal tract predicts motor impairment in chronic stroke. Stroke, 41:910–915.
60.
ZwaanRA, MaddenCJ. Embodied sentence comprehension. In: PecherD, ZwaanRA (eds.) Grounding Cognition: The Role of Perception and Action in Memory, Language, and Thinking. Cambridge, UK: Cambridge University Press. p. 224.
Supplementary Material
Please find the following supplemental material available below.
For Open Access articles published under a Creative Commons License, all supplemental material carries the same license as the article it is associated with.
For non-Open Access articles published, all supplemental material carries a non-exclusive license, and permission requests for re-use of supplemental material or any part of supplemental material shall be sent directly to the copyright owner as specified in the copyright notice associated with the article.
