Mapping human temporal and parietal neuronal population activity and functional coupling during mathematical cognition

[en] Brain areas within the lateral parietal cortex (LPC) and ventral temporal cortex (VTC) have been shown to code for abstract quantity representations and for symbolic numerical representations, respectively. To explore the fast dynamics of activity within each region and the interaction between them, we used electrocorticography recordings from 16 neurosurgical subjects implanted with grids of electrodes over these two regions and tracked the activity within and between the regions as subjects performed three different numerical tasks. Although our results reconfirm the presence of math-selective hubs within the VTC and LPC, we report here a remarkable heterogeneity of neural responses within each region at both millimeter and millisecond scales. Moreover, we show that the heterogeneity of response profiles within each hub mirrors the distinct patterns of functional coupling between them. Our results support the existence of multiple bidirectional functional loops operating between discrete populations of neurons within the VTC and LPC during the visual processing of numerals and the performance of arithmetic functions. These findings reveal information about the dynamics of numerical processing in the brain and also provide insight into the fine-grained functional architecture and connectivity within the human brain

Disciplines :

Neurosciences & behavior

Author, co-author :

Daitch, Amy

Foster, Brett

Schrouff, Jessica ; Université de Liège > Dép. d'électric., électron. et informat. (Inst.Montefiore) > Systèmes et modélisation

Rangarajan, Vinitha

Kasikci, Itir

Gattas, Sandra

Parvizi, Josef

Language :

English

Title :

Mapping human temporal and parietal neuronal population activity and functional coupling during mathematical cognition

Publication date :

2016

Journal title :

Proceedings of the National Academy of Sciences of the United States of America

ISSN :

0027-8424

eISSN :

1091-6490

Publisher :

National Academy of Sciences, Washington, United States - District of Columbia

Volume :

113

Issue :

Peer reviewed :

Peer Reviewed verified by ORBi

European Projects :

H2020 - 654038 - DecoMP_ECoG - Decoding memory processing from experimental and spontaneous human brain activity using intracranial electrophysiological recordings and machine learning based methods.

Funders :

DG RDT - Commission Européenne. Direction Générale de la Recherche et de l'Innovation
CE - Commission Européenne

Available on ORBi :

since 13 December 2016

Statistics

Number of views

72 (1 by ULiège)

Number of downloads

0 (0 by ULiège)

More statistics

Scopus citations^®

Scopus citations^®
without self-citations

OpenCitations

OpenAlex citations

Bibliography

Lipton JS, Spelke ES (2003) Origins of number sense. Large-number discrimination in human infants. Psychol Sci 14(5):396-401.
Boysen ST, Berntson GG (1989) Numerical competence in a chimpanzee (Pan troglodytes). J Comp Psychol 103(1):23-31.
Brannon EM, Terrace HS (1998) Ordering of the numerosities 1 to 9 by monkeys. Science 282(5389):746-749.
Nieder A (2012) Supramodal numerosity selectivity of neurons in primate prefrontal and posterior parietal cortices. Proc Natl Acad Sci USA 109(29):11860-11865.
Brannon EM, Wusthoff CJ, Gallistel CR, Gibbon J (2001) Numerical subtraction in the pigeon: Evidence for a linear subjective number scale. Psychol Sci 12(3):238-243.
Ansari D (2008) Effects of development and enculturation on number representation in the brain. Nat Rev Neurosci 9(4):278-291.
Dehaene S (2011) The Number Sense: How the Mind Creates Mathematics (Oxford Univ Press, New York), 2nd Ed.
Hannagan T, Amedi A, Cohen L, Dehaene-Lambertz G, Dehaene S (2015) Origins of the specialization for letters and numbers in ventral occipitotemporal cortex. Trends Cogn Sci 19(7):374-382.
Cipolotti L, Butterworth B, Denes G (1991) A specific deficit for numbers in a case of dense acalculia. Brain 114(Pt 6):2619-2637.
Cohen L, Dehaene S (1995) [Reading numbers in pure alexia: Effects of the task and hemispheric specialization]. Rev Neurol (Paris) 151(8-9):480-485.
Dagenbach D, McCloskey M (1992) The organization of arithmetic facts in memory: Evidence from a brain-damaged patient. Brain Cogn 20(2):345-366.
Dehaene S, Cohen L (1991) Two mental calculation systems: A case study of severe acalculia with preserved approximation. Neuropsychologia 29(11):1045-1054.
McCloskey M, Caramazza A, Basili A (1985) Cognitive mechanisms in number processing and calculation: Evidence from dyscalculia. Brain Cogn 4(2):171-196.
Takayama Y, Sugishita M, Akiguchi I, Kimura J (1994) Isolated acalculia due to left parietal lesion. Arch Neurol 51(3):286-291.
Dehaene S (1992) Varieties of numerical abilities. Cognition 44(1-2):1-42.
Dehaene S, Cohen L (1995) Towards an anatomical and functional model of number processing. Math Cogn 1:83-120.
Arsalidou M, Taylor MJ (2011) Is 2+2=4? Meta-analyses of brain areas needed for numbers and calculations. Neuroimage 54(3):2382-2393.
Cantlon JF, Brannon EM, Carter EJ, Pelphrey KA (2006) Functional imaging of numerical processing in adults and 4-y-old children. PLoS Biol 4(5):e125.
Chochon F, Cohen L, van de Moortele PF, Dehaene S (1999) Differential contributions of the left and right inferior parietal lobules to number processing. J Cogn Neurosci 11(6):617-630.
Dastjerdi M, Ozker M, Foster BL, Rangarajan V, Parvizi J (2013) Numerical processing in the human parietal cortex during experimental and natural conditions. Nat Commun 4:2528.
Eger E, Sterzer P, Russ MO, Giraud AL, Kleinschmidt A (2003) A supramodal number representation in human intraparietal cortex. Neuron 37(4):719-725.
Nieder A, Dehaene S (2009) Representation of number in the brain. Annu Rev Neurosci 32:185-208.
Piazza M, Eger E (2016) Neural foundations and functional specificity of number representations. Neuropsychologia 83:257-273.
Piazza M, Izard V, Pinel P, Le Bihan D, Dehaene S (2004) Tuning curves for approximate numerosity in the human intraparietal sulcus. Neuron 44(3):547-555.
Walsh V (2003) A theory of magnitude: Common cortical metrics of time, space and quantity. Trends Cogn Sci 7(11):483-488.
Butterworth B, Varma S, Laurillard D (2011) Dyscalculia: From brain to education. Science 332(6033):1049-1053.
Moeller K, Willmes K, Klein E (2015) A review on functional and structural brain connectivity in numerical cognition. Front Hum Neurosci 9:227.
Matejko AA, Ansari D (2015) Drawing connections between white matter and numerical and mathematical cognition: A literature review. Neurosci Biobehav Rev 48: 35-52.
Jolles D, et al. (2016) Parietal hyper-connectivity, aberrant brain organization, and circuit-based biomarkers in children with mathematical disabilities. Dev Sci 19(4): 613-631.
Iuculano T, Cohen Kadosh R (2014) Preliminary evidence for performance enhancement following parietal lobe stimulation in developmental dyscalculia. Front Hum Neurosci 8:38.
Salillas E, Semenza C, Basso D, Vecchi T, Siegal M (2012) Single pulse TMS induced disruption to right and left parietal cortex on addition and multiplication. Neuroimage 59(4):3159-3165.
Andres M, Pelgrims B, Michaux N, Olivier E, Pesenti M (2011) Role of distinct parietal areas in arithmetic: An fMRI-guided TMS study. Neuroimage 54(4):3048-3056.
Allison T, Puce A, Spencer DD, McCarthy G (1999) Electrophysiological studies of human face perception. I: Potentials generated in occipitotemporal cortex by face and non-face stimuli. Cereb Cortex 9(5):415-430.
Park J, Hebrank A, Polk TA, Park DC (2012) Neural dissociation of number from letter recognition and its relationship to parietal numerical processing. J Cogn Neurosci 24(1):39-50.
Pinel P, Dehaene S, Rivière D, LeBihan D (2001) Modulation of parietal activation by semantic distance in a number comparison task. Neuroimage 14(5):1013-1026.
Price GR, Ansari D (2011) Symbol processing in the left angular gyrus: Evidence from passive perception of digits. Neuroimage 57(3):1205-1211.
Shum J, et al. (2013) A brain area for visual numerals. J Neurosci 33(16):6709-6715.
Abboud S, Maidenbaum S, Dehaene S, Amedi A (2015) A number-form area in the blind. Nat Commun 6:6026.
Grotheer M, Herrmann KH, Kovács G (2016) Neuroimaging evidence of a bilateral representation for visually presented numbers. J Neurosci 36(1):88-97.
Hermes D, et al. (October 26, 2015) Electrophysiological responses in the ventral temporal cortex during reading of numerals and calculation. Cereb Cortex, 10.1093/ cercor/bhv250.
Schrouff J, Mourão-Miranda J, Phillips C, Parvizi J (2016) Decoding intracranial EEG data with multiple kernel learning method. J Neurosci Methods 261:19-28.
Manning JR, Jacobs J, Fried I, Kahana MJ (2009) Broadband shifts in local field potential power spectra are correlated with single-neuron spiking in humans. J Neurosci 29(43):13613-13620.
Ray S, Maunsell JH (2011) Different origins of gamma rhythm and high-gamma activity in macaque visual cortex. PLoS Biol 9(4):e1000610.
Logothetis NK, Pauls J, Augath M, Trinath T, Oeltermann A (2001) Neurophysiological investigation of the basis of the fMRI signal. Nature 412(6843):150-157.
Flinker A, Chang EF, Barbaro NM, Berger MS, Knight RT (2011) Sub-centimeter language organization in the human temporal lobe. Brain Lang 117(3):103-109.
Parvizi J, et al. (2012) Electrical stimulation of human fusiform face-selective regions distorts face perception. J Neurosci 32(43):14915-14920.
Foster BL, Rangarajan V, Shirer WR, Parvizi J (2015) Intrinsic and task-dependent coupling of neuronal population activity in human parietal cortex. Neuron 86(2): 578-590.
Lewis CM, Bosman CA, Womelsdorf T, Fries P (2016) Stimulus-induced visual cortical networks are recapitulated by spontaneous local and interareal synchronization. Proc Natl Acad Sci USA 113(5):E606-E615.
Luczak A, Barthó P, Harris KD (2009) Spontaneous events outline the realm of possible sensory responses in neocortical populations. Neuron 62(3):413-425.
Kenet T, Bibitchkov D, Tsodyks M, Grinvald A, Arieli A (2003) Spontaneously emerging cortical representations of visual attributes. Nature 425(6961):954-956.
Arieli A, Sterkin A, Grinvald A, Aertsen A (1996) Dynamics of ongoing activity: Explanation of the large variability in evoked cortical responses. Science 273(5283): 1868-1871.
Tsodyks M, Kenet T, Grinvald A, Arieli A (1999) Linking spontaneous activity of single cortical neurons and the underlying functional architecture. Science 286(5446): 1943-1946.
Keller CJ, et al. (2013) Neurophysiological investigation of spontaneous correlated and anticorrelated fluctuations of the BOLD signal. J Neurosci 33(15):6333-6342.
Leopold DA, Logothetis NK (2003) Spatial patterns of spontaneous local field activity in the monkey visual cortex. Rev Neurosci 14(1-2):195-205.
Nir Y, et al. (2008) Interhemispheric correlations of slow spontaneous neuronal fluctuations revealed in human sensory cortex. Nat Neurosci 11(9):1100-1108.
He BJ, Snyder AZ, Zempel JM, Smyth MD, Raichle ME (2008) Electrophysiological correlates of the brain's intrinsic large-scale functional architecture. Proc Natl Acad Sci USA 105(41):16039-16044.
Hipp JF, Hawellek DJ, Corbetta M, Siegel M, Engel AK (2012) Large-scale cortical correlation structure of spontaneous oscillatory activity. Nat Neurosci 15(6):884-890.
Varela F, Lachaux JP, Rodriguez E, Martinerie J (2001) The brainweb: Phase synchronization and large-scale integration. Nat Rev Neurosci 2(4):229-239.
Fries P (2005) A mechanism for cognitive dynamics: Neuronal communication through neuronal coherence. Trends Cogn Sci 9(10):474-480.
Buzsaki G (2011) Rhythms of the Brain (Oxford Univ Press, New York) 1st Ed.
Canolty RT, et al. (2006) High gamma power is phase-locked to theta oscillations in human neocortex. Science 313(5793):1626-1628.
Miller KJ, et al. (2010) Dynamic modulation of local population activity by rhythm phase in human occipital cortex during a visual search task. Front Hum Neurosci 4:197.
Voytek B, et al. (2015) Oscillatory dynamics coordinating human frontal networks in support of goal maintenance. Nat Neurosci 18(9):1318-1324.
Watrous AJ, Deuker L, Fell J, Axmacher N (2015) Phase-amplitude coupling supports phase coding in human ECoG. eLife 4:07886, erratum in eLife (2015) 4:12810.
Foster BL, Parvizi J (2012) Resting oscillations and cross-frequency coupling in the human posteromedial cortex. Neuroimage 60(1):384-391.
Voytek B, et al. (2010) Shifts in gamma phase-amplitude coupling frequency from theta to alpha over posterior cortex during visual tasks. Front Hum Neurosci 4:191.
van der Meij R, Kahana M, Maris E (2012) Phase-amplitude coupling in human electrocorticography is spatially distributed and phase diverse. J Neurosci 32(1):111-123.
Maris E, van Vugt M, Kahana M (2011) Spatially distributed patterns of oscillatory coupling between high-frequency amplitudes and low-frequency phases in human iEEG. Neuroimage 54(2):836-850.
Corbetta M, Shulman GL (2002) Control of goal-directed and stimulus-driven attention in the brain. Nat Rev Neurosci 3(3):201-215.
Dosenbach NU, et al. (2007) Distinct brain networks for adaptive and stable task control in humans. Proc Natl Acad Sci USA 104(26):11073-11078.
Harvey BM, Klein BP, Petridou N, Dumoulin SO (2013) Topographic representation of numerosity in the human parietal cortex. Science 341(6150):1123-1126.
Eger E, Pinel P, Dehaene S, Kleinschmidt A (2015) Spatially invariant coding of numerical information in functionally defined subregions of human parietal cortex. Cereb Cortex 25(5):1319-1329.
Nieder A, Miller EK (2004) A parieto-frontal network for visual numerical information in the monkey. Proc Natl Acad Sci USA 101(19):7457-7462.
Roitman JD, Brannon EM, Platt ML (2007) Monotonic coding of numerosity in macaque lateral intraparietal area. PLoS Biol 5(8):e208.
Saalmann YB, Kastner S (2011) Cognitive and perceptual functions of the visual thalamus. Neuron 71(2):209-223.
Zikopoulos B, Barbas H (2007) Circuits formultisensory integration and attentional modulation through the prefrontal cortex and the thalamic reticular nucleus in primates. Rev Neurosci 18(6):417-438.
Steriade M, McCormick DA, Sejnowski TJ (1993) Thalamocortical oscillations in the sleeping and aroused brain. Science 262(5134):679-685.
Hermes D, Miller KJ, Noordmans HJ, Vansteensel MJ, Ramsey NF (2010) Automated electrocorticographic electrode localization on individually rendered brain surfaces. J Neurosci Methods 185(2):293-298.
Schrouff J, et al. (2013) PRoNTo: Pattern recognition for neuroimaging toolbox. Neuroinformatics 11(3):319-337.