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Investigator

Dietmar Plenz, Ph.D.

Section on Critical Brain Dynamics

Porter Neuroscience Research Center
Building 35 Room 3A-1000
35 Convent Drive
Bethesda MD 20892-3726
Office: (301) 402-2249
Lab: (301) 402-2249
Fax: (301) 480-7480
plenzd@mail.nih.gov

Dr. Plenz is Chief of the Section on Critical Brain Dynamics in the Intramural Research Program at the NIMH. He attended college at the Universities of Mainz and Tuebingen, Germany. Under the supervision of Prof. Valentino Braitenberg and Ad Aertsen, he received his Ph.D. in 1993 at the Max-Planck Institute of Biological Cybernetics/University Tuebingen, where he pioneered the development of in vitro cortex networks to study the emergence of neuronal population dynamics. During his 3 year postdoctoral fellowship with Stephen T. Kitai at the University of Tennessee, Memphis, he developed advanced cortex-forebrain neuronal cultures that allowed him to identify the mechanisms underlying distinct activity patterns that characterize normal and abnormal population dynamics in cortex and basal ganglia. Dr. Plenz joined the NIMH as an Investigator in 1999 and was promoted to Senior Investigator with tenure in 2006. His laboratory combines multi-electrode array recordings, 2-photon imaging in vitro and in vivo with neuronal modeling to study the self-organization of neural networks. In 2003, his laboratory identified neuronal avalanches, a previously unknown organization of neuronal activity in the brain. 



Complex systems, when poised at the transition between order and disorder, exhibit scale-free, power law dynamics. These critical systems are highly adaptive and flexibly process and store information, which for decades prompted the conjecture that the brain might operate at criticality. Our discovery of neuronal avalanches in superficial layers of cortex in 2003 provides solid experimental evidence that indeed the brain might be critical. The spatio-temporal, synchronized activity patterns of avalanches form a scale-free organization that spontaneously emerges in cortex. To date, our lab has described neuronal avalanches in vitro in slice cultures and acute slices and in vivo in rat, macaque monkeys, and normal human subjects using a variety of techniques ranging from high-density microelectrode array recordings to 2-photon imaging to magnetoencephalography (MEG).   Avalanches are established at the time of superficial cortex layer differentiation, require balanced fast excitation and inhibition, and are regulated via an inverted-U profile of NMDA/dopamine-D1 interaction, well known from cognitive task paradigms, e.g. working memory. Their internal organization forms a small-world topology that combines local diversity with efficient global communication. Neuronal synchronization in the form of avalanches naturally incorporates gamma-oscillations and cascades, e.g. synfire chains. Cortical networks that display neuronal avalanches optimize their internal information transfer and maximize the range of inputs that can be processed. Since our early description in 2003, avalanche analysis has become an established approach to study brain organization such as in humans using fMRI, MEG, EEG and ECoG. 

Embedded in the scale-invariant avalanche dynamics, is a threshold-dependent mechanism that allows a local neuronal group, once it reaches a minimal size, to replicate its activity at multiple sites. We named such replication a coherence potential and it can be identified by the identical waveforms found almost simultaneously in the local field potential at many sites. This threshold dependent replication is similar to the emergence of gliders in cellular automata with computational power. Coherence potentials form small-world networks with integrated weight distribution as found in other brain, gene, and communication networks.

Overall, our results demonstrate that neuronal avalanches and coherence potentials are signatures of critical network dynamics at which the cortex gains universal properties found at criticality.






Neuronal avalanches in awake monkeys


Neuronal avalanches in awake monkeys

Ongoing activity in the awake monkey is characterized by spontaneous, apparently irregular fluctuations in spatiotemporal synchronization. In a recent PNAS paper (http://www.pnas.org/content/early/2009/08/25/0904089106.full.pdf+html), using data recorded in Miguel Nicolelis's lab (Duke), we show that these fluctuations are precisely organized in space, time, and local neuronal activity levels (in collaboration with Dante Chialvo, North-Western). In fact, the fluctuations represent neuronal avalanches, which are spatio-temporal clusters of synchronized activity that follow a power law in size distributions as expected for systems in the critical state.

Importantly, the avalanches form a fractal organization, that is smaller avalanches are embedded in larger avalanches, which themselves are again linked to even larger avalanches. The image depicts three avalanche rasters that originate from the same cortical area of the monkey (primary motor) cortex for increasingly longer periods of time and increasing minimal threshold levels in the activity detection. Each raster has the hallmark organization of neuronal avalanches.

Watch a movie of this activity: http://www.youtube.com/watch?v=N6HXsSvYyKE. Follow this link to a feature article in the NewScientist: http://www.newscientist.com/article/mg20327235.100-many-degrees-of-separation-in-dementia-brains.html

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  • 1) Bai, R., Stewart, C. V., Plenz, D., Basser, P. J. (2016)
  • Assessing the sensitivity of diffusion MRI to detect neuronal activity directly
  • PNAS, 113, E1728–E1737
  • 2) Meisel, C., Schulze-Bonhage, A., Freestonec, D., Cook, M. J., Achermann, P., Plenz, D. (2015)
  • Intrinsic excitability measures track antiepileptic drug action and uncover increasing/decreasing excitability over the wake/sleep cycle
  • PNAS, 112, 14694–14699
  • 3) Bellay, T., Klaus, A., Seshadri, S., Plenz, D. (2015)
  • Irregular spiking of pyramidal neurons organizes as scale-invariant neuronal avalanches in the awake state
  • eLife, 4, e07224
  • 4) Shew, W., Plenz, D (2013)
  • The functional benefits of criticality in the cortex
  • The Neuroscientist, 19, 88-100
  • 5) Shriki, O., Alstott, J., Carver, F., Holroyd, T., Henson, R.N.A., Smith, M.L., Coppola, R., Bullmore, E., Plenz, D. (2013)
  • Neuronal avalanches in the resting MEG of the human brain
  • J. Neurosci., 33, 7079-7090
  • 6) Pajevic, S., Plenz, D. (2012)
  • The organization of strong links in complex networks
  • Nat. Phys. doi, 1038, nphys2257
  • 8) Plenz, D., Stewart, C.V., Shew, W., Yang, H., Klaus, A., Bellay, T. (2011)
  • Multi-electrode array recordings of neuronal avalanches in organotypic cultures
  • J. Vis. Exp., 1, pii:2949
  • 9) Yu, S., Yang, H., Nakahara, H., Santos, G.S., Nikolic, D., Plenz, D. (2011)
  • Higher-order interactions characterized in cortical activity
  • J. Neurosci. , 31, 17514-17526
  • 10) Shew, W.L., Yang, H., Yu, S., Roy, R., Plenz, D. (2011)
  • Information capacity and transmission are maximized in balanced cortical networks with neuronal avalanches
  • J. Neurosci, 31(1), 55-63
  • 11) Klaus, A., Yu, S., Plenz, D. (2011)
  • Statistical analyses support power law distributions found in neuronal avalanches
  • PLoS One, 6(5), e19779
  • 12) Plenz, D. (2010)
  • A leak-proof model
  • Nat. Phys., 6, 717-718
  • 13) Shew, W. L., Bellay, T., Plenz, D. (2010)
  • Simultaneous multi-electrode array recording and two-photon calcium imgaging of neural activity.
  • J. Neurosci. Meth., 192, 75-82
  • 14) Santos, G.S., Gireesh, E.D., Plenz, D., Nakahara, H. (2010)
  • Hierarchical interaction structure of neural activities in cortical slice cultures
  • J. Neurosci, 30, 8720-8733
  • 15) Hahn, G., Petermann, T., havenith, M.N., Yu, S., Singer, W., Plenz, D., Nikilolic, D. (2010)
  • Neuronal avalanches in spontaneous activity in vivo.
  • J. Neurophys, 104, 3312-3322
  • 16) Thiagarajan, T. C., Lebedev, M. A., Nicolelis, M. A.and D. Plenz (2010)
  • Coherence potentials: loss-less, all-or-none network events in the cortex
  • PLoS Biol., 8(1), e1000278
  • 17) Shew, W., Yang, H., Petermann, T., Roy, R., and D. Plenz (2009)
  • Neuronal avalanches imply maximum dynamic range in cortical networks at criticality
  • arXive
  • 18) Shew, W., Yang, H., Petermann, T., Roy, R., and D. Plenz (2009)
  • Neuronal avalanches imply maximum dynamic range in cortical networks at criticality
  • J. Neurosci., 29(49), 15595-600
  • 19) Petermann, T., Thiagarajan, T.C., Lebedev, M., Nicolelis, M., Chialvo, R.C. and D. Plenz (2009)
  • Ongoing cortical activity in awake monkeys composed of neuronal avalanches
  • Proc. Natl. Acad. Sci. U. S. A., 106(37), 15921-6
  • 20) Pajevic, S. and D. Plenz (2008)
  • Efficient network reconstruction from dynamical cascades identifies small-world topology of neuronal avalanches
  • PLoS Comp. Biol., 5, e1000271
  • 21) Stewart CV, Plenz D (2008)
  • Homeostasis of neuronal avalanches during postnatal cortex development in vitro
  • J Neurosci Meth, 169, 405-416
  • 22) Gireesh, E. D. and D. Plenz (2008)
  • Neuronal avalanches organize as nested theta and beta/gamma-oscillations during development of cortical layer 2/3
  • Proc. Natl. Acad. Sci. U. S. A., 105, 7576-7581
  • 23) Plenz D, Thiagarajan T (2007)
  • The organizing principles of neuronal avalanches: cell assemblies in the cortex
  • TINS, 30, 101 - 110
  • 24) Stewart CV, Plenz D (2006)
  • Inverted-U profile of dopamine-NMDA-mediated spontaneous avalanche recurrence in superficial layers of rat prefrontal cortex
  • J Neurosci, 26, 8148-8159
  • 25) Petridou N, Plenz D, Silva AC, Loew M, Bodurka J, Bandettini PA (2006)
  • Direct magnetic resonance detection of neuronal electrical activity.
  • Proc Natl Acad Sci U S A, 103, 16015-16020
  • 26) Plenz D (2005)
  • Comment on 'Critical branching captures activity in living neural networks and maximizes the number of metastable states'
  • Phys Rev Lett, 95, 219801
  • 27) Gustafson N, Gireesh-Dharmaraj E, Czubayko U, Blackwell KT, Plenz D (2005)
  • A comparative voltage and current-clamp analysis of feedback and feedforward synaptic transmission in the striatal microcircuit in vitro.
  • J Neurophysiol, 95, 737-752
  • 28) Kerr JN, Plenz D (2004)
  • Action potential timing determines dendritic calcium during striatal up-states
  • Journal of Neuroscience, 24, 877-885
  • 29) Pfeffer, L., Ide, D., Stewart, C.V., and D. Plenz (2004)
  • A life support systems for stimulation of and recording from rodent neuron networks grown on multi-electrode arrays
  • Proceedings 17th IEEE Symposium on Computer-Based Medical Systems: CBMS 2004, Eds. R. Long, S. Atani, 473-478
  • 30) Beggs JM and D Plenz (2004)
  • Neuronal avalanches are diverse and precise activity patterns that are stable for many hours n cortical slice cultures
  • Journal of Neuroscience, 24, 5216-5229
  • 31) Plenz D (2003)
  • When inhibition goes incognito: feedback interaction between spiny projection neurons in striatal function.
  • Trends Neurosci , 26 , 436-43
  • 32) Blackwell KT Czubayko U Plenz D (2003)
  • Quantitative estimate of synaptic inputs to striatal neurons during up and down states in vitro.
  • J Neurosci , 23 , 9123-32
  • 33) Beggs JM Plenz D (2003)
  • Neuronal Avalanches in Neocortical Circuits.
  • J Neurosci , 23 , 11167-11177
  • 34) Karpiak, V. C. and D. Plenz (2002)
  • Preparation and maintenance of organotypic cultures for multi‐electrode array recordings
  • Current Protocols in Neuroscience , UNIT 6.15
  • 35) Kerr JN Plenz D (2002)
  • Dendritic calcium encodes striatal neuron output during up-states.
  • J Neurosci , 22 , 1499-512
  • 36) Czubayko U Plenz D (2002)
  • Fast synaptic transmission between striatal spiny projection neurons.
  • Proc Natl Acad Sci U S A , 99 , 15764-9
  • 37) Plenz D Kital ST (1999)
  • A basal ganglia pacemaker formed by the subthalamic nucleus and external globus pallidus.
  • Nature , 400 , 677-82
  • 38) Plenz D Herrera-Marschitz M Kitai ST (1998)
  • Morphological organization of the globus pallidus-subthalamic nucleus system studied in organotypic cultures.
  • J Comp Neurol , 397 , 437-57
  • 39) Plenz D Kitai ST (1998)
  • Up and down states in striatal medium spiny neurons simultaneously recorded with spontaneous activity in fast-spiking interneurons studied in cortex-striatum-substantia nigra organotypic cultures.
  • J Neurosci , 18 , 266-83
  • 40) Plenz D Kitai ST (1998)
  • Regulation of the nigrostriatal pathway by metabotropic glutamate receptors during development.
  • J Neurosci , 18 , 4133-44
  • 41) Plenz D Aertsen A (1996)
  • Neural dynamics in cortex-striatum co-cultures--I. anatomy and electrophysiology of neuronal cell types.
  • Neuroscience , 70 , 861-91
  • 42) Plenz D Aertsen A (1996)
  • Neural dynamics in cortex-striatum co-cultures--II. Spatiotemporal characteristics of neuronal activity.
  • Neuroscience , 70 , 893-924
  • 43) Plenz D Kitai ST (1996)
  • Organotypic cortex-striatum-mesencephalon cultures: the nigrostriatal pathway.
  • Neurosci Lett , 209 , 177-80
  • 44) Plenz D Kitai ST (1996)
  • Generation of high-frequency oscillations in local circuits of rat somatosensory cortex cultures.
  • J Neurophysiol , 76 , 4180-4
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