ISSN 0869-6632 (Print)
ISSN 2542-1905 (Online)

For citation:

Chholak P., Tabari F., Pisarchik A. N. Revealing the neural network underlying covert picture-naming paradigm using magnetoencephalography. Izvestiya VUZ. Applied Nonlinear Dynamics, 2022, vol. 30, iss. 1, pp. 76-95. DOI: 10.18500/0869-6632-2022-30-1-76-95

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Language: 
English
Heading: 
Nonlinear Dynamics and Neuroscience
Article type: 
Article
UDC: 
530.182, 612.821.1
DOI: 
10.18500/0869-6632-2022-30-1-76-95

Revealing the neural network underlying covert picture-naming paradigm using magnetoencephalography

Autors: 
Chholak Parth, Universidad Politécnica de Madrid, Centre for Biomedical Technology
Tabari Fatemeh, Universidad Autónoma de Madrid
Pisarchik Alexander Nikolaevich, Universidad Politécnica de Madrid, Centre for Biomedical Technology
Abstract: 

The ability to name trivial everyday objects is a key cognitive function that is tested after head injuries or brain surgeries. Although quite a lot of long-standing knowledge on this topic has accumulated over the past few decades and many theoretical models have been created, the underlying neural substrate and brain functioning are still not fully aligned. As far as we know, there have been no studies on this topic using magnetoencephalography (MEG), which allows recording electrophysiological activity with a high temporal resolution. Therefore, to study the underlying spatio-temporal brain activations during the sensory and semantic processing of object naming, we conducted MEG experiments with 15 subjects grouped into three equal-sized groups with different types of language training and skills. Using boundary element methods for modelling cortical surfaces and dynamic statistical parametric mapping to solve the inverse problem, we reconstructed the cortical source activity from the recorded MEG data. The reconstructed cortical maps showed a homogeneous brain response in all three groups at the sensory processing stage, while the responses between the three groups at the semantic processing stage were different. In addition, average time courses were constructed for key brain regions such as the lateral occipital cortex (LO), fusiform gyrus (FG), Broca’s area (BA), and Wernicke’s area (WA). The obtained results assume unimodal forms for LO and WA time series, and bimodal forms for FG and BA. The only LO curve peak and the first FG peak resided in the time interval for the sensory processing stage, whereas, the only WA peak, the second FG peak and the second BA peak resided in the semantic processing stage. The first BA peak was located at the boundary separating the two stages. In addition to segregating regions involved in sensory and semantic processing, this study confirmed the involvement of FG in object naming (for the first time using MEG) that is at risk of resection during mesial temporal lobe epilepsy interventions. However, the results from this work are preliminary due to the limited sample size, and future research with a larger cohort of subjects are needed to verify/strengthen the findings of this study.

Key words: 
magnetoencephalography
picture naming
object recognition
cognitive neuroscience
visual perception
Acknowledgments: 
This study was supported by the Portuguese Foundation for Science and Technology and the Portuguese Ministry of Science, Technology and Higher Education (UID/PSI/01662/2019), through the national funds (PIDDAC). The data analysis was supported by the Russian Science Foundation, grant No. 19-12-00050. The authors acknowledge Dr. Adriana Sampaio and Elena Garayzabal Heinze for their role in administering the experiments, fruitful suggestions, and financial support. We would also like to thank Eduardo Lopez-Caneda and Alberto J. Gonzalez-Villar for their help and support in data collection. Lastly, we thank the participating children and their parents along with the King’s College La Moraleja, Hastings School Madrid and C.E.I.P. Principe de Asturias who helped with the data collection and their invaluable input and support.
Reference: 
  1. Quillian M. Semantic memory. In: Minsky M, editor. Semantic Information Processing. Cambridge, MA: MIT Press; 1968. P. 216–270.
  2. Tulving E. Episodic and semantic memory. In: Tulving E, Donaldson W, editors. Organization of Memory. New York: Academic Press; 1972. P. 381–403.
  3. Warrington EK. The selective impairment of semantic memory. Q. J. Exp. Psychol. 1975;27(4):635– 657. DOI: 10.1080/14640747508400525.
  4. Nestor PJ, Fryer TD, Hodges JR. Declarative memory impairments in Alzheimer’s disease and semantic dementia. NeuroImage. 2006;30(3):1010–1020. DOI: 10.1016/j.neuroimage.2005.10.008.
  5. Burnstine TH, Lesser RP, Hart J, Uematsu S, Zinreich SJ, Krauss GL, Fisher RS, Vining EPG, Gordon B. Characterization of the basal temporal language area in patients with left temporal lobe epilepsy. Neurology. 1990;40(6):966–970. DOI: 10.1212/WNL.40.6.966.
  6. Luders H, Lesser RP, Hahn J, Dinner DS, Morris HH, Wyllie E, Godoy J. Basal temporal language area. Brain. 1991;114(2):743–754. DOI: 10.1093/brain/114.2.743.
  7. Damasio H, Grabowski TJ, Tranel D, Hichwa RD, Damasio AR. A neural basis for lexical retrieval. Nature. 1996;380(6574):499–505. DOI: 10.1038/380499a0.
  8. Noppeney U, Price CJ. A PET study of stimulus- and task-induced semantic processing. NeuroImage. 2002;15(4):927–935. DOI: 10.1006/nimg.2001.1015.
  9. Bright P, Moss H, Tyler LK. Unitary vs multiple semantics: PET studies of word and picture processing. Brain Lang. 2004;89(3):417–432. DOI: 10.1016/j.bandl.2004.01.010.
  10. Sharp DJ, Scott SK, Wise RJS. Retrieving meaning after temporal lobe infarction: The role of the basal language area. Ann. Neurol. 2004;56(6):836–846. DOI: 10.1002/ana.20294.
  11. Spitsyna G, Warren JE, Scott SK, Turkheimer FE, Wise RJS. Converging language streams in the human temporal lobe. J. Neurosci. 2006;26(28):7328–7336. DOI: 10.1523/JNEUROSCI.0559-06.2006.
  12. Marinkovic K, Dhond RP, Dale AM, Glessner M, Carr V, Halgren E. Spatiotemporal dynamics of modality-specific and supramodal word processing. Neuron. 2003;38(3):487–497. DOI: 10.1016/S0896-6273(03)00197-1.
  13. Nobre AC, Allison T, McCarthy G. Word recognition in the human inferior temporal lobe. Nature. 1994;372(6503):260–263. DOI: 10.1038/372260a0.
  14. Liu H, Agam Y, Madsen JR, Kreiman G. Timing, timing, timing: Fast decoding of object information from intracranial field potentials in human visual cortex. Neuron. 2009;62(2): 281–290. DOI: 10.1016/j.neuron.2009.02.025.
  15. Mesulam MM. From sensation to cognition. Brain. 1998;121(6):1013–1052. DOI: 10.1093/brain/121.6.1013.
  16. Thompson-Schill SL. Neuroimaging studies of semantic memory: inferring «how» from «where». Neuropsychologia. 2003;41(3):280–292. DOI: 10.1016/S0028-3932(02)00161-6.
  17. Catani M, Ffytche DH. The rises and falls of disconnection syndromes. Brain. 2005;128(10): 2224–2239. DOI: 10.1093/brain/awh622.
  18. Martin A. The representation of object concepts in the brain. Annu. Rev. Psychol. 2007;58:25–45. DOI: 10.1146/annurev.psych.57.102904.190143.
  19. Forseth KJ, Kadipasaoglu CM, Conner CR, Hickok G, Knight RT, Tandon N. A lexical semantic hub for heteromodal naming in middle fusiform gyrus. Brain. 2018;141(7):2112–2126. DOI: 10.1093/brain/awy120.
  20. Grill-Spector K, Kourtzi Z, Kanwisher N. The lateral occipital complex and its role in object recognition. Vis. Res. 2001;41(10–11):1409–1422. DOI: 10.1016/S0042-6989(01)00073-6.
  21. Indefrey P, Levelt WJM. The spatial and temporal signatures of word production components. Cognition. 2004;92(1–2):101–144. DOI: 10.1016/j.cognition.2002.06.001.
  22. Ungerleider LG, Mishkin M. Two cortical visual systems. In: Ingle DJ, Goodale MA, Mansfield RJW, editors. Analysis of Visual Behavior. Cambridge: MIT Press; 1982. P. 549–586.
  23. Felleman DJ, Van Essen DC. Distributed hierarchical processing in the primate cerebral cortex. Cereb. Cortex. 1991;1(1):1–47. DOI: 10.1093/cercor/1.1.1-a.
  24. Thompson-Shill SL, D’Esposito M, Aguirre GK, Farah MJ. Role of left inferior prefrontal cortex in retrieval of semantic knowledge: A reevaluation. Proc. Natl. Acad. Sci. U.S.A. 1997;94(26): 14792–14797. DOI: 10.1073/pnas.94.26.14792.
  25. Wagner AD, Pare-Blagoev EJ, Clark J, Poldrack RA. Recovering meaning: Left prefrontal cortex guides controlled semantic retrieval. Neuron. 2001;31(2):329–338. DOI: 10.1016/S0896-6273(01)00359-2.
  26. Hickok G, Poeppel D. The cortical organization of speech processing. Nat. Rev. Neurosci. 2007;8(5):393–402. DOI: 10.1038/nrn2113.
  27. Poldrack RA, Wagner AD, Prull MW, Desmond JE, Glover GH, Gabrieli JDE. Functional specialization for semantic and phonological processing in the left inferior prefrontal cortex. NeuroImage. 1999;10(1):15–35. DOI: 10.1006/nimg.1999.0441.
  28. Badre D, Poldrack RA, Pare-Blagoev EJ, Insler RZ, Wagner AD. Dissociable controlled retrieval and generalized selection mechanisms in ventrolateral prefrontal cortex. Neuron. 2005;47(6):907– 918. DOI: 10.1016/j.neuron.2005.07.023.
  29. Bastos AM, Vezoli J, Bosman CA, Schoffelen JM, Oostenveld R, Dowdall JR, De Weerd P, Kennedy H, Fries P. Visual areas exert feedforward and feedback influences through distinct frequency channels. Neuron. 2015;85(2):390–401. DOI: 10.1016/j.neuron.2014.12.018.
  30. Michalareas G, Vezoli J, van Pelt S, Schoffelen JM, Kennedy H, Fries P. Alpha-beta and gamma rhythms subserve feedback and feedforward influences among human visual cortical areas. Neuron. 2016;89(2):384–397. DOI: 10.1016/j.neuron.2015.12.018.
  31. Lazar RM, Mohr JP. Revisiting the contributions of Paul Broca to the study of aphasia. Neuropsychol. Rev. 2011;21(3):236–239. DOI: 10.1007/s11065-011-9176-8.
  32. Trupe LA, Varma DD, Gomez Y, Race D, Leigh R, Hillis AE, Gottesman RF. Chronic apraxia of speech and Broca’s area. Stroke. 2013;44(3):740–744. DOI: 10.1161/STROKEAHA.112.678508.
  33. Flinker A, Korzeniewska A, Shestyuk AY, Franaszczuk PJ, Dronkers NF, Knight RT, Crone NE. Redefining the role of Broca’s area in speech. Proc. Natl. Acad. Sci. U.S.A. 2015;112(9): 2871–2875. DOI: 10.1073/pnas.1414491112.
  34. Chao LL, Martin A. Representation of manipulable man-made objects in the dorsal stream. NeuroImage. 2000;12(4):478–484. DOI: 10.1006/nimg.2000.0635.
  35. Binder JR, Desai RH. The neurobiology of semantic memory. Trends Cogn. Sci. 2011;15(11): 527–536. DOI: 10.1016/j.tics.2011.10.001.
  36. Conner CR, Chen G, Pieters TA, Tandon N. Category specific spatial dissociations of parallel processes underlying visual naming. Cereb. Cortex. 2014;24(10):2741–2750. DOI: 10.1093/cercor/bht130.
  37. Binney RJ, Embleton KV, Jefferies E, Parker GJ, Lambon Ralph MA. The ventral and inferolateral aspects of the anterior temporal lobe are crucial in semantic memory: Evidence from a novel direct comparison of distortion-corrected fMRI, rTMS, and semantic dementia. Cereb. Cortex. 2010;20(11):2728–2738. DOI: 10.1093/cercor/bhq019.
  38. Mion M, Patterson K, Acosta-Cabronero J, Pengas G, Izquierdo-Garcia D, Hong YT, Fryer TD, Williams GB, Hodges JR, Nestor PJ. What the left and right anterior fusiform gyri tell us about semantic memory. Brain. 2010;133(11):3256–3268. DOI: 10.1093/brain/awq272.
  39. Noppeney U, Phillips J, Price C. The neural areas that control the retrieval and selection of semantics. Neuropsychologia. 2004;42(9):1269–1280. DOI: 10.1016/j.neuropsychologia.2003.12.014.
  40. Binder JR. The Wernicke area: Modern evidence and a reinterpretation. Neurology. 2015;85(24): 2170–2175. DOI: 10.1212/WNL.0000000000002219.
  41. Drane DL, Loring DW, Voets NL, Price M, Ojemann JG, Willie JT, Saindane AM, Phatak V, Ivanisevic M, Millis S, Helmers SL, Miller JM, Meador KJ, Gross RE. Better object recognition and naming outcome with MRI-guided stereotactic laser amygdalohippocampotomy for temporal lobe epilepsy. Epilepsia. 2015;56(1):101–113. DOI: 10.1111/epi.12860.
  42. Hoppe C, Witt JA, Helmstaedter C, Gasser T, Vatter H, Elger CE. Laser interstitial thermotherapy (LiTT) in epilepsy surgery. Seizure. 2017;48:45–52. DOI: 10.1016/j.seizure.2017.04.002.
  43. Oldfield RC. The assessment and analysis of handedness: The Edinburgh inventory. Neuropsychologia. 1971;9(1):97–113. DOI: 10.1016/0028-3932(71)90067-4.
  44. Genesee F. Second language learning through immersion: A review of U.S. programs. Rev. Educ. Res. 1985;55(4):541–561. DOI: 10.2307/1170246.
  45. Gramfort A, Luessi M, Larson E, Engemann DA, Strohmeier D, Brodbeck C, Parkkonen L, Hamalainen MS. MNE software for processing MEG and EEG data. NeuroImage. 2014;86: 446–460. DOI: 10.1016/j.neuroimage.2013.10.027.
  46. Peirce JW. PsychoPy–Psychophysics software in Python. J. Neurosci. Methods. 2007;162(1–2): 8–13. DOI: 10.1016/j.jneumeth.2006.11.017.
  47. Niso G, Gorgolewski KJ, Bock E, Brooks TL, Flandin G, Gramfort A, Henson RN, Jas M, Litvak V, Moreau JT, Oostenveld R, Schoffelen JM, Tadel F, Wexler J, Baillet S. MEG-BIDS, the brain imaging data structure extended to magnetoencephalography. Sci. Data. 2018;5(1):180110. DOI: 10.1038/sdata.2018.110.
  48. Fischl B. FreeSurfer. NeuroImage. 2012;62(2):774–781. DOI: 10.1016/j.neuroimage.2012.01.021.
  49. Dale AM, Liu AK, Fischl BR, Buckner RL, Belliveau JW, Lewine JD, Halgren E. Dynamic statistical parametric mapping: Combining fMRI and MEG for high-resolution imaging of cortical activity. Neuron. 2000;26(1):55–67. DOI: 10.1016/S0896-6273(00)81138-1.
  50. Grill-Spector K, Kushnir T, Hendler T, Edelman S, Itzchak Y, Malach R. A sequence of objectprocessing stages revealed by fMRI in the human occipital lobe. Hum. Brain Mapp. 1998;6(4): 316–328. DOI: 10.1002/(SICI)1097-0193(1998)6:4<316::AID-HBM9>3.0.CO;2-6.
  51. Grill-Spector K, Kushnir T, Edelman S, Itzchak Y, Malach R. Cue-invariant activation in objectrelated areas of the human occipital lobe. Neuron. 1998;21(1):191–202. DOI: 10.1016/S0896-6273(00)80526-7.
  52. Murtha S, Chertkow H, Beauregard M, Evans A. The neural substrate of picture naming. J. Cogn. Neurosci. 1999;11(4):399–423. DOI: 10.1162/089892999563508.
  53. Kourtzi Z, Kanwisher N. Cortical regions involved in perceiving object shape. J. Neurosci. 2000;20(9):3310–3318. DOI: 10.1523/JNEUROSCI.20-09-03310.2000.
  54. Doniger GM, Foxe JJ, Murray MM, Higgins BA, Snodgrass JG, Schroeder CE, Javitt DC. Activation timecourse of ventral visual stream object-recognition areas: High density electrical mapping of perceptual closure processes. J. Cogn. Neurosci. 2000;12(4):615–621. DOI: 10.1162/089892900562372.
  55. Allison T, Ginter H, McCarthy G, Nobre AC, Puce A, Luby M, Spencer DD. Face recognition in human extrastriate cortex. J. Neurophysiol. 1994;71(2):821–825. DOI: 10.1152/jn.1994.71.2.821.
  56. Allison T, Puce A, Spencer DD, McCarthy G. Electrophysiological studies of human face perception. I: Potentials generated in occipitotemporal cortex by face and non-face stimuli. Cereb. Cortex. 1999;9(5):415–430. DOI: 10.1093/cercor/9.5.415.
  57. McCarthy G, Puce A, Belger A, Allison T. Electrophysiological studies of human face perception. II: Response properties of face-specific potentials generated in occipitotemporal cortex. Cereb. Cortex. 1999;9(5):431–444. DOI: 10.1093/cercor/9.5.431.
  58. Puce A, Allison T, McCarthy G. Electrophysiological studies of human face perception. III: Effects of top-down processing on face-specific potentials. Cereb. Cortex. 1999;9(5):445–458. DOI: 10.1093/cercor/9.5.445.
Received: 
10.07.2021
Accepted: 
01.08.2021
Published: 
31.01.2022
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