Network Architecture of the Long-Distance Pathways in the Macaque Brain

Modha, D. S. & Singh, R. (July 12, 2010) Proc. Natl. Acad. Sci. USA, 10.1073/pnas.1008054107

Dharmendra S ModhaIBM Research – Almaden

Raghavendra Singh IBM Research – India

Consensus dendrogram of a network of speciesClauset, Moore, Newman, Nature, 2008

Topological modules in E. coli metabolismRavasz, Somera, Mongru, Oltvai, Barabasi

Science, 2002

Cartographic representation of the metabolic network of E. Coli

Guimera, Amaral, Nature 2005Map of protein–protein interactions

Jeong, Mason, Barabasi, Oltvai, Nature 2001

Networks are Everywhere

The human brain is the most complex mass of protoplasm on earth-perhaps even in our galaxy.

Marian C. Diamond, Arnold B. Scheibel

Gray and White Matter

Multiple Scales of The Brain Network Brainbow

Livet et al, Nature 2007 Denk, Seung, et al, 2007

Hagman et al, PLoS Biology 2008

Binzeggar, Douglas, Martin, J. Neurosci. 2004

Nicolaus Steno, 1669

“white matter is nature’s finest masterpiece”

CoCoMac

413 literature reports

7007 brain sites

8003 mapping details

2508 tracer injections

39748 connection details

Rolf Kotter, Klass Stephen, 2000

FV91-V1

AP84-TE

PG91b-IT

BP82-46

SP89a-46

FV91-V4FV91-TF

RV99-TFRV99-CA1

BR98-CA1

FV91-TH

BR98-TH

=

כ כ

PFCd 9=

PCi IPL PF#1 7b= =

CCa 24 24d 24c CMAr

24c

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Divergent Nomenclature and Abundant Conflicts

Occipital Lobe: 23 Brain Regions

Temporal Lobe: 88 Brain Regions

Insula & Cingulate Cortex: 12 & 18 Brain Regions

Parietal Lobe: 41 Brain Regions

Frontal Lobe: 81 Brain Regions

Thalamus: 75 Brain Regions

Basal Ganglia: 41 Brain Regions

383 Brain Regions

1 connection

6,602 Connections

Bundling Algorithm by Holten, 2006

Species Study Brain Regions

Connections

Monkey Felleman, Van Essen, 91 32 305

Young, 93 70 700

Kaiser, Hilgetag, 06 95 2,402

Cat Scannell et al., 95 65 1,139

Scannell et al., 99 95 1,500

Notable Collations

Species Study Brain Regions

Connections

Monkey Felleman, Van Essen, 91 32 305

Young, 93 70 700

Kaiser, Hilgetag, 06 95 2,402

Cat Scannell et al., 95 65 1,139

Scannell et al., 99 95 1,500

Monkey This Collection 383 6,602

Notable Collations

Kaiser, Hilgetag, 2006

Felleman, Van Essen, 1991

Ungerleider, Mishkin, 1982

Arcuate Fasciculus

Schmahmann & Pandya, 2006

Cingulum BundleSchmahmann & Pandya, 2006

Extreme CapsuleSchmahmann & Pandya, 2006

Fronto-occipital Fasciculus

Schmahmann & Pandya, 2006

Inferior Longitudinal Fasciculus

Schmahmann & Pandya, 2006

Middle Longitudinal Fasciculus

Schmahmann & Pandya, 2006

Superior Longitudinal FasciculusSchmahmann & Pandya, 2006

Uncinate Fasciculus

Schmahmann & Pandya, 2006

Connectivity between Cortex and Thalamus

Connectivity between Cortex and Amygdala

Connectivity between Cortex and Striatum/Claustrum

Connectivity between Amygdala and Diencephalon

Comprehensive Includes every study in CoCoMac

Consistent Every connection can be tracked back

Concise 6,877 areas to 383

Coherent Unified hierarchical parcellation

Colossal 3 times larger than previous network

C, C, C, C, and C

Brain is small-world

Brain Random(100 trials)

Diameter 6 3.93

Characteristic Path Length 2.62 2.30

Average Clustering Coefficient 0.33 0.0528

Reciprocity 42% 5.34%

SCC: 351 brain regions, 6,491 projections; Sparse: 4.5%

DiE BG OC#2 Pl#6 TL#2 FL#2 CgG#2 InsulaDiE 10 10 37 160 105 600 25 26BG 37 186 8 8 140 95 14 24OC#2 61 16 77 53 77 46 6 0Pl#6 103 47 38 178 83 251 55 21TL#2 92 172 60 99 684 388 70 28FL#2 197 145 12 178 238 695 151 32CgG#2 37 22 0 48 63 202 39 10Insula 15 44 0 41 78 101 13 14#Areas 75 41 23 41 88 81 18 12In-Degree (avg) 8.5 15.83 11.09 20.67 17.67 30.16 21.94 14.27Out-Degree (avg) 14.16 14.25 15.85 20.45 19.16 20.71 24.64 27.45

“Organized Complexity” – Weaver, 1948

Degree Distribution Consistent with Exponential

302 Neuron Network in C. Elegans is Exponential

Watts and Strogatz; Amaral et al, 2000

Characteristic Rank 1 2 3 4 5 6 7 8 9 10

Integrator In-Degree 32 46 12o 12l 11 24 F7 14 8A LIP

In-Closeness 46 12o 32,11 24 12l MD 8A 23c 8B LIP,F7

Authorities 32 12o 46 11 12l 24 14 F7 MD 9

Distributor Out-Degree 46 24 TF 9 13 13a TH TE,LIP PGm V2

Out-Closeness 46 24 TF TE 9 TH LIP PGm 45,23 12

Hubs 46 24 9 TF TE TH 13 32 23 PM#3

Intermediary Betweeness 24 46 LIP 13a MD 32 TF PIT 13 PS

PageRank 32 MD 46 36r PIT 12o 24 23c 12l 11

Metrics for Topologically Centrality

Characteristic Rank 1 2 3 4 5 6 7 8 9 10

Integrator In-Degree 32 46 12o 12l 11 24 F7 14 8A LIP

In-Closeness 46 12o 32,11 24 12l MD 8A 23c 8B LIP,F7

Authorities 32 12o 46 11 12l 24 14 F7 MD 9

Distributor Out-Degree 46 24 TF 9 13 13a TH TE,LIP PGm V2

Out-Closeness 46 24 TF TE 9 TH LIP PGm 45,23 12

Hubs 46 24 9 TF TE TH 13 32 23 PM#3

Intermediary Betweeness 24 46 LIP 13a MD 32 TF PIT 13 PS

PageRank 32 MD 46 36r PIT 12o 24 23c 12l 11

Prefrontal Cortex is Topologically Central

Yellow = PfC

Brain is small-world, Core is “tiny”-world!

Brain Core

Diameter 6 4

Characteristic Path Lengh 2.62 1.95

Average Clustering Coefficient 0.33 0.39

Core contains only 32% of vertices yet 88% of all edges originate or terminate in the core

Core contains correlated-anti-correlated networksand may be a key to higher cognition & consciousness

Fox, Snyder, Vincent, Corbetta, Van Essen, and Raichle, 2005

Rachel Jones, Nature Rev. Neurosci., 2002

Sherbondy, Ananthanrayanan, Dougherty, Wandell, and Modha, HBM, 2009

Binzegger, Douglas, Martin, J. Neurosci., 2004