Top

Published in:

01-07-2017 | Original Article

Neuronal electrical ongoing activity as a signature of cortical areas

Authors: Carlo Cottone, Camillo Porcaro, Andrea Cancelli, Elzbieta Olejarczyk, Carlo Salustri, Franca Tecchio

Published in: Brain Structure and Function | Issue 5/2017

Abstract

Brodmann’s pioneering work resulted in the classification of cortical areas based on their cytoarchitecture and topology. Here, we aim at documenting that diverse cortical areas also display different neuronal electric activities. We investigated this notion in the hand-controlling sections of the primary somatosensory (S1) and motor (M1) areas, in both hemispheres. We identified S1 and M1 in 20 healthy volunteers by applying functional source separation (FSS) to their recorded electroencephalograms (EEG). Our results show that S1 and M1 can be clearly differentiated by their neuroelectric activities in both hemispheres and independently of the subject’s state (i.e., at rest or performing movements or receiving external stimulations). In particular, S1 displayed higher relative power than M1 in the alpha and low beta frequency ranges (8–25 Hz, p < .003), whereas the opposite occurred in the high gamma band (52–90 Hz, p = .006). In addition, S1’s activity had a smaller Higuchi’s fractal dimensions (HFD) than M1’s (p < .00001) in all subjects, permitting a reliable classification of the two areas. Moreover, HFD of M1’s activity resulted correlated with the hand’s fine motor control, as expressed by the 9-hole peg test scores. The present work is a first step toward the identification and classification of brain cortical areas based on neuronal dynamics rather than on cytoarchitectural features. We deem this step to be an improvement of our knowledge of the brain’s structural–functional unity.

Ahmadi K, Ahmadlou M, Rezazade M, Azad-Marzabadi E, Sajedi F (2013) Brain activity of women is more fractal than men. Neurosci Lett 535:7–11. doi:10.1016/j.neulet.2012.12.043 CrossRefPubMed

Alfonso MR, Miquel TF, Xavier B, Blanca AS (2013) Resting parietal electroencephalogram asymmetries and self-reported attentional control. Clin EEG Neurosci 44:188–192. doi:10.1177/1550059412465871 CrossRefPubMed

Allen EA, Damaraju E, Plis SM, Erhardt EB, Eichele T, Calhoun VD (2014) Tracking whole-brain connectivity dynamics in the resting state Cerebral cortex 24:663–676. doi:10.1093/cercor/bhs352 PubMed

Barbati G et al (2006) Functional source separation from magnetoencephalographic signals. Hum Brain Mapp 27:925–934. doi:10.1002/hbm.20232 CrossRefPubMed

Betti V, Zappasodi F, Rossini PM, Aglioti SM, Tecchio F (2009) Synchronous with your feelings: sensorimotor gamma band and empathy for pain. J Neurosci Off J Soc Neurosci 29:12384–12392. doi:10.1523/JNEUROSCI.2759-09.2009 CrossRef

Bola M, Gall C, Sabel BA (2015) Disturbed temporal dynamics of brain synchronization in vision loss. Cortex J Devoted Study Nerv Syst Behav 67:134–146. doi:10.1016/j.cortex.2015.03.020 CrossRef

Brodmann K (1909) Vergleichende Lokalisationslehre der Großhirnrinde. Verlag von Johann Ambrosius Barth, Leipzig

Buzsaki G (2006) Rhythms of the brain. Oxford University Press, Oxford, New YorkCrossRef

Buzsaki G, Mizuseki K (2014) The log-dynamic brain: how skewed distributions affect network operations. Nat Rev Neurosci 15:264–278. doi:10.1038/nrn3687 CrossRefPubMedPubMedCentral

Cajal RY (1888) Estructura de los centros nerviosos de las aves. Rev Trimest Histol Norm Patol 1:1–10

Crone NE, Miglioretti DL, Gordon B, Lesser RP (1998a) Functional mapping of human sensorimotor cortex with electrocorticographic spectral analysis. II. Event-related synchronization in the gamma band. Brain J Neurol 121(Pt 12):2301–2315CrossRef

Crone NE, Miglioretti DL, Gordon B, Sieracki JM, Wilson MT, Uematsu S, Lesser RP (1998b) Functional mapping of human sensorimotor cortex with electrocorticographic spectral analysis. I. Alpha and beta event-related desynchronization. Brain J Neurol 121(Pt 12):2271–2299CrossRef

Faisal AA, Selen LP, Wolpert DM (2008) Noise in the nervous system. Nat Rev Neurosci 9:292–303. doi:10.1038/nrn2258 CrossRefPubMedPubMedCentral

Glasser MF, Goyal MS, Preuss TM, Raichle ME, Van Essen DC (2014) Trends and properties of human cerebral cortex: correlations with cortical myelin content. Neuroimage 93(Pt 2):165–175. doi:10.1016/j.neuroimage.2013.03.060 CrossRefPubMed

Golgi C (1873) Sulla struttura della sostanza grigia del cervello. Gazzetta Medica Italiana. Lombardia 33:244–246

Grassberger P, Procaccia I (1983) Measuring the strangeness of strange attractors. Phys D 9:20CrossRef

Graziadio S, Basu A, Tomasevic L, Zappasodi F, Tecchio F, Eyre JA (2010) Developmental tuning and decay in senescence of oscillations linking the corticospinal system. J Neurosci Off J Soc Neurosci 30:3663–3674. doi:10.1523/JNEUROSCI.5621-09.2010 CrossRef

Handwerker DA, Roopchansingh V, Gonzalez-Castillo J, Bandettini PA (2012) Periodic changes in fMRI connectivity. Neuroimage 63:1712–1719. doi:10.1016/j.neuroimage.2012.06.078 CrossRefPubMedPubMedCentral

He BJ (2011) Scale-free properties of the functional magnetic resonance imaging signal during rest and task. J Neurosci Off J Soc Neurosci 31:13786–13795. doi:10.1523/JNEUROSCI.2111-11.2011 CrossRef

He BJ, Zempel JM, Snyder AZ, Raichle ME (2010) The temporal structures and functional significance of scale-free brain activity. Neuron 66:353–369. doi:10.1016/j.neuron.2010.04.020 CrossRefPubMedPubMedCentral

Higuchi T (1988) Approach to an irregular time series on the basis of the fractal theory. Physica D 31:6CrossRef

Mathiowetz V, Volland G, Kashman N, Weber K (1985) Adult norms for the Box and Block Test of manual dexterity. Am J Occup Ther 39:386–391CrossRefPubMed

Moreno-Dominguez D, Anwander A, Knosche TR (2014) A hierarchical method for whole-brain connectivity-based parcellation. Hum Brain Mapp 35:5000–5025. doi:10.1002/hbm.22528 CrossRefPubMed

Moutard C, Dehaene S, Malach R (2015) Spontaneous fluctuations and non-linear ignitions: two dynamic faces of cortical recurrent loops. Neuron 88:194–206. doi:10.1016/j.neuron.2015.09.018 CrossRefPubMed

Nelson SM, McDermott KB, Wig GS, Schlaggar BL, Petersen SE (2013) The critical roles of localization and physiology for understanding parietal contributions to memory retrieval. Neuroscientist 19:578–591. doi:10.1177/1073858413492389 CrossRefPubMed

Niedermeyer E, da Silva FH (2005) Electroencephalography: basic principles, clinical applications, and related fields. Lippincott Williams & Wilkins, Philadelphia, USA

Ohara S et al (2000) Movement-related change of electrocorticographic activity in human supplementary motor area proper. Brain J Neurol 123(Pt 6):1203–1215CrossRef

Oxford Grice K, Vogel KA, Le V, Mitchell A, Muniz S, Vollmer MA (2003) Adult norms for a commercially available Nine Hole Peg Test for finger dexterity. Am J Occup Ther 57:570–573CrossRefPubMed

Pascual-Marqui RD (2002) Standardized low-resolution brain electromagnetic tomography (sLORETA): technical details. Methods Find Exp Clin Pharmacol 24(Suppl D):5–12

Pittaccio S et al (2011) Primary sensory and motor cortex activities during voluntary and passive ankle mobilization by the SHADE orthosis. Hum Brain Mapp 32:60–70. doi:10.1002/hbm.20998 CrossRefPubMed

Porcaro C, Tecchio F (2014) Semi-blind functional source separation algorithm from non-invasive electrophysiology to neuroimaging. In: Wang G (ed) Blind source separation: signals and communication technology. Springer-Verlag, Berlin, Heidelberg

Porcaro C, Barbati G, Zappasodi F, Rossini PM, Tecchio F (2008) Hand sensory-motor cortical network assessed by functional source separation. Hum Brain Mapp 29:70–81. doi:10.1002/hbm.20367 CrossRefPubMed

Porcaro C et al (2009) Hand somatosensory subcortical and cortical sources assessed by functional source separation: an EEG study. Hum Brain Mapp 30:660–674. doi:10.1002/hbm.20533 CrossRefPubMed

Porcaro C et al (2013) Multiple frequency functional connectivity in the hand somatosensory network: an EEG study. Clin Neurophysiol Off J Int Fed Clin Neurophysiol 124:1216–1224. doi:10.1016/j.clinph.2012.12.004 CrossRef

Power JD et al (2011) Functional network organization of the human brain. Neuron 72:665–678. doi:10.1016/j.neuron.2011.09.006 CrossRefPubMedPubMedCentral

Ramon C, Holmes MD (2014) Spatiotemporal phase clusters and phase synchronization patterns derived from high density EEG and ECoG recordings. Curr Opin Neurobiol 31C:127–132. doi:10.1016/j.conb.2014.10.001

Roberts JA, Iyer KK, Finnigan S, Vanhatalo S, Breakspear M (2014) Scale-free bursting in human cortex following hypoxia at birth. J Neurosci Off J Soc Neurosci 34:6557–6572. doi:10.1523/JNEUROSCI.4701-13.2014 CrossRef

Siegel M, Donner TH, Engel AK (2012) Spectral fingerprints of large-scale neuronal interactions. Nat Rev Neurosci 13:121–134. doi:10.1038/nrn3137 PubMed

Smith SM et al (2012) Temporally independent functional modes of spontaneous brain activity. Proc Natl Acad Sci USA 109:3131–3136. doi:10.1073/pnas.1121329109 CrossRefPubMedPubMedCentral

Smits FM, Porcaro C, Cottone C, Cancelli A, Rossini PM, Tecchio F (2016) Electroencephalographic fractal dimension in healthy ageing and Alzheimer’s disease. PloS One 11:e0149587. doi:10.1371/journal.pone.0149587 CrossRefPubMedPubMedCentral

Tadel F, Baillet S, Mosher JC et al (2011) Brainstorm: a user-friendly application for MEG/EEG analysis. Comput lntell Neurosci 2011:13

Tecchio F et al (2007a) Somatosensory dynamic gamma-band synchrony: a neural code of sensorimotor dexterity. Neuroimage 35:185–193. doi:10.1016/j.neuroimage.2006.12.002 CrossRefPubMed

Tecchio F, Porcaro C, Barbati G, Zappasodi F (2007b) Functional source separation and hand cortical representation for a brain-computer interface feature extraction. J Physiol 580:703–721. doi:10.1113/jphysiol.2007.129163 CrossRefPubMedPubMedCentral

Tecchio F, Zappasodi F, Porcaro C, Barbati G, Assenza G, Salustri C, Rossini PM (2008) High-gamma band activity of primary hand cortical areas: a sensorimotor feedback efficiency index. Neuroimage 40:256–264. doi:10.1016/j.neuroimage.2007.11.038 CrossRefPubMed

Uhlhaas PJ, Singer W (2012) Neuronal dynamics and neuropsychiatric disorders: toward a translational paradigm for dysfunctional large-scale networks. Neuron 75:963–980. doi:10.1016/j.neuron.2012.09.004 CrossRefPubMed

Van Essen DC (2013) Cartography and connectomes. Neuron 80:775–790. doi:10.1016/j.neuron.2013.10.027 CrossRefPubMed

Van Essen DC, Glasser MF (2014) In vivo architectonics: a cortico-centric perspective. Neuroimage 93(Pt 2):157–164. doi:10.1016/j.neuroimage.2013.04.095 CrossRefPubMed

von Economo C, Koskinas GN (2008) Atlas of cytoarchitectonics of the adult human cerebral cortex. Karger, Basel

Wang J et al (2009) Parcellation-dependent small-world brain functional networks: a resting-state fMRI study. Hum Brain Mapp 30:1511–1523. doi:10.1002/hbm.20623 CrossRefPubMed

Wang Z, Chen LM, Negyessy L, Friedman RM, Mishra A, Gore JC, Roe AW (2013) The relationship of anatomical and functional connectivity to resting-state connectivity in primate somatosensory cortex. Neuron 78:1116–1126. doi:10.1016/j.neuron.2013.04.023 CrossRefPubMedPubMedCentral

Wig GS, Laumann TO, Petersen SE (2014) An approach for parcellating human cortical areas using resting-state correlations. NeuroImage 93(Pt 2):276–291. doi:10.1016/j.neuroimage.2013.07.035 CrossRefPubMed

Wolpert DM, Diedrichsen J, Flanagan JR (2011) Principles of sensorimotor learning. Nat Rev Neurosci 12:739–751. doi:10.1038/nrn3112 PubMed

Zappasodi F, Olejarczyk E, Marzetti L, Assenza G, Pizzella V, Tecchio F (2014) Fractal dimension of EEG activity senses neuronal impairment in acute stroke. PloS One 9:e100199. doi:10.1371/journal.pone.0100199 CrossRefPubMedPubMedCentral

Zappasodi F, Marzetti L, Olejarczyk E, Tecchio F, Pizzella V (2015) Age-related changes in electroencephalographic signal complexity. PloS One 10:e0141995. doi:10.1371/journal.pone.0141995 CrossRefPubMedPubMedCentral

Zilles K, Amunts K (2012) Architecture of the cerebral cortex. In: Paxinos G, Mai JK (eds) The human nervous system, Elsevier Academic Press, San Diego, CA pp 836–895CrossRef

Title: Neuronal electrical ongoing activity as a signature of cortical areas
Authors: Carlo Cottone
Camillo Porcaro
Andrea Cancelli
Elzbieta Olejarczyk
Carlo Salustri
Franca Tecchio
Publication date: 01-07-2017
Publisher: Springer Berlin Heidelberg
Published in: Brain Structure and Function / Issue 5/2017
Print ISSN: 1863-2653
Electronic ISSN: 1863-2661
DOI: https://doi.org/10.1007/s00429-016-1328-4

At a glance: The STEP trials

Springer Medicine

Neuronal electrical ongoing activity as a signature of cortical areas

Abstract

At a glance: The STEP trials

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 5/2017

Commonly preserved and species-specific gyral folding patterns across primate brains

Human astrocytes: structure and functions in the healthy brain

NR2A- and NR2B-NMDA receptors and drebrin within postsynaptic spines of the hippocampus correlate with hunger-evoked exercise

Interaction of nucleus reuniens and entorhinal cortex projections in hippocampal field CA1 of the rat

Using a novel PV-Cre rat model to characterize pallidonigral cells and their terminations

Acute restraint stress decreases c-fos immunoreactivity in hilar mossy cells of the adult dentate gyrus