Theeconomicsofbrainnetwork organization

EdBullmore

CABDyNComplexityCentre,SadBusinessSchool UniversityofOxford University of Oxford November8,2011

Aneconomicalmodelofbrainnetworks An economical model of brain networks

Brainsmakeadaptivevalueatsomephysicalcost
Adaptivevalue:perceptions,cognitions,behaviours thathelptheorganismsurvive inachanging,competitiveenvironment g g, p Physicalcost:volume,wiringandmetaboliccostsofnervoussystems

In brain networks the topological properties that add the most adaptive Inbrainnetworks,thetopologicalpropertiesthataddthemostadaptive valueareoftenthemostcostly
Longdistanceconnectionsneededforintegrativeprocessing Central hubs that mediate a lot of inter modular connections Centralhubsthatmediatealotofintermodularconnections

Likeprofitablebusinesses,brainnetworksnegotiateaneconomictrade offbetweenaddingvalueandcontrollingproductioncosts ff b t ddi l d t lli d ti t

Howdidwestartthinkingaboutbrainnetworks?
Macro Micro

Mayo,Meynert
(1827,1870)

Ramny Cajal
(1890)

Explosionofhighqualityneuroimaging datanowmakes connectomes d t dauntinglyaccessible ti l ibl

About100,000,000,000neuronsinthe humanbrain(100billion) About100,000synapsesperneuron , y p p 1quadrillioncellularconnections(1015) inhumanbrainconnectome 1000sofstructuralandsignalling proteinspersynapticconnection

Sporns,Tononi &Ktter (2005)PLoS CompBiol

Graphtheorypowerfullysimplifiesthetopologyofcomplex systems s stems

Pathlength Path length Efficiency

Clustering

Bassett&Bullmore(2006) Neuroscientist

Degree Hubs

Topology:thestudyofpropertiesthatarepreservedundercontinuousdeformationofobjects

Thesmallworldofthewormsbrain
Caenorhabditiselegans

Smallworld Highclusteringorcliquishnessofconnections
betweenneighboringnodes Shortpathlengthorhighefficiencyof communicationbetween anypairofnodes

Anatomy(277neurons,7000synapses)

Costefficient
46%maximumefficiencyofinformationtransferfor about4%maximumconnectioncost
Watts&Strogatz (1998)Nature;Latora &Marchiori (2001)PhysRevLett

Topology(277nodes,7000edges)

Vertes etal(2011)YouTube (searchonneuro tweets)

Fromneuroimaging tobraingraphs

1. Estimateanassociationmatrixfrom thedata
Whatarethenodes? Whatmetricofconnectivity?

2. Generateanadjacencymatrixfromthe 2 Generate an adjacency matrix from the associationmatrix

Whataretheedges?

3. Measuretopologicalpropertiesofeach graph 4. Makecomparisonsbetweengraphs

Fornito etal(2010)FrontSysNeuro

Brain graphs are statistical models entailing assumptions and tradeoffs which influence parameter values Brain graph parameters make sense relativistically, not absolutely; comparison between graphs is not trivial
Bassett&Bullmore(2010)Curr OpNeurol;Bullmore&Bassett(2011)Annu RevClin Psychol

Manynetworkpropertiesareconservedacrossmanyscalesandkinds andspeciesofbraingraphs and species of brain graphs

Smallworldness
highclustering shortpathlengthorhighefficiency

Costefficiency
highefficiencyofinformationtransferforrelativelylow connectioncost

Hubnodes fattaileddegreedistributions Modularity nodesaremoredenselyconnectedtoothernodesinthe

samemodulethantonodesinothermodules

Bullmore&Sporns (2009)NatRevNeurosci Sporns etal(2007)PLoS ONE;Yuetal(2008)Cereb Cortex;Meunier etal(2010)FrontNeurosci

Humanbraingraphsandotherinformationprocessingnetworksare hierarchicallymodular hierarchically modular

Nodesinthesamemoduleareoften,butnotalways,anatomicalaswellastopologicalneighbours:sointramodular edgeswillbeshorterdistancethanintermodularedges Braingraphstypicallyhavemoduleswithinmodules

Meunier etal(2010)FrontNeurosci;Bassettetal(2010)PLoS CompBiol;Chenetal(2008)Cereb Cortex

Whatsspecialandwhatsuniversalabouthumanbrains comparedtootherinformationnetworks? d t th i f ti t k?

HumanBrain Network RestingstateFMRI

EconomicNetwork NewYorkStockExchange

SocialNetwork Twittergadaffi

Blue =Brain Green =Market

Vertes etal(2011)FrontSysNeurosci

Backtoanatomy Countingthematerialandmetaboliccostsofbrainnetworks Counting the material and metabolic costs of brain networks

Cajals economicalprinciple:
Werealizedthatallofthevarious conformationsoftheneuronanditsvarious componentsaresimplymorphological adaptationsgovernedbylawsof conservationfortime,space,andmaterial. Increasingawarenessalsoofthemetabolic orenergycostsofthenervoussystemand thebiologicaldrivetocontrolmetabolicas wellasmaterialcostsofbrains

VanEssen(1997)Nature Niven &Laughlin(2008)JExpBiol GarciaLopez(2010)FrontNeuroanatomy

Brainnetworksareeconomicallywiredbut donot strictlyminimise wiringcost do not strictly minimise wiring cost

Original Minimal

Macaque

C.elegans
Kaiser&Hilgetag (2006)PLoS CompBiol

Tradeoffsbetweenconnectiondistanceand topologyinhumanbrainnetworks l i h b i k

AlexanderBlochetal(2011)inreview

Costefficiencyanditsheritabilityinhumanbrainnetworks

Ifbrainnetworkshadbeenselectedby If brain networks had been selected by competitivecriteriaofminimising costand maximising efficiencywemightpredictthat costefficiencyisheritable Tradeoffbetweentopologicalefficiencyand connectioncost(Euclideandistance betweenfunctionallyconnectedregions)was measuredin16MZand13DZtwinpairs Globalcostefficiencywasheritable~0.6and nodalcost efficiencywasheritable 0.8in nodal costefficiency was heritable ~0 8 in symmetricalcorticalregions,includingDMN components

Fornito etal(2011)JNeurosci

Expensive,longrangeintegrativeconnectionsmaybeworthit forextracognitivecapacity

Greaterefficiency(orshorterpathlength) y( p g ) ofhumanbrainnetworksiscorrelatedwith higherIQ

VandenHeuvel etal(2009)JNeurosci;Lietal(2009)PLoS Comp Biol;Bassettetal(2010)PLos CompBiol;

Global(neuronal)workspacetheory Gl b l ( l) k th predicts integrativenetworkswillbe requiredforconscious,effortful processing

Dehaene etal(1998)ProcNatl Acad Sci Baars (1993)Acognitivetheoryofconsciousness

Workingmemoryloadbreaksmodularityanddrivesworkspace configurationoffunctionalbrainnetworks configuration of functional brain networks

Modules

Clustering

Longdistance edges
bandfrequencynetworks band frequency networks recordedusingMEGinhealthy volunteersperformingNback workingmemorytask

Intermodular edges
Kitzbichler etal(2011)JNeurosci

Changesincognitiveloadareassociatedwithrapidreconfiguration ofnetworktopologyandconnectiondistance

Kitzbichler etal(2011)JNeurosci

Cartooninterpretationofeconomicalsmallworldarchitecturein termsofcognitiveprocesses terms of cognitive processes

Integratedprocesses
General egexecutive Isotropic(IQ) Distributed Conscious Effortful Eff tf l

Highefficiency Shortpathlength (Highercost) (Higher cost)

Highclustering Modularity (Lowercost)

Segregatedprocesses
Specialised egfacevision Encapsulated Localised Unconscious Automatic

Normalbraindevelopmentisassociatedwithchangesinnetwork efficiencyandconnectioncost efficiency and connection cost

FunctionalMRInetworks
Connectiondistanceincreases withage
Fairetal(2007)ProcNatl Acad Sci Hagmann etal(2010)ProcNatl Acad Sci

AnatomicalDTInetworks
Topologicalefficiencyincreases withage

Functionalnetworksandconnectorhubsareless parsimoniouslyconnectedinschizophrenia i i l t di hi h i

AlexanderBlochetal(2011)inreview

Whatcouldbegood abouttheschizophrenia connectome? ?

Connectorhubsaddvaluebutarealso pointsofvulnerabilityifthenetworkis attackedorlesioned

Schizophrenicbrainnetworkshavegreater robustness,perhapsrepresentinggreater resilienceagainstpathologicalattack

Achardetal(2006),JNeurosci;Honey&Sporns(2008)HumBrainMapp; Lynalletal(2010)JNeurosci;Vertesetal(2011),inreview

Conclusions
Brainsmakeadaptivevalueatsomephysicalcost Inbrainnetworks,thetopologicalpropertiesthataddthemostadaptivevalueareoftenthemostcostly Likeprofitablebusinesses,brainnetworksnegotiateaneconomictradeoffbetweenaddingvalueandcontrolling productioncosts

Brainnetworkshavecomplextopologyembeddedinanatomicalspace
Longdistanceconnections,oftenbetweenmodules,areimportantforefficiencyofinformationtransferandformationof workspaces Topologicalpropertiessuchasefficiencyandrobustnesshaveadaptivevalueintermsofsupportingeffortfulcognitiveprocesses l l h ff d b h d l f ff f l andresiliencetoadverseperturbation Brainscanrapidlyandslowlyreconfigurethemselvesintermsofconnectiondistanceandtopology TradeoffsbetweenwiringcostandtopologicalefficiencyhavebeendemonstrateddirectlyinCelegans and,lessdirectly,in humans Itisplausiblethataneconomicaltradeoffbetweentopologicalandspatialpropertiesisanimportantcriterionfordevelopmental andevolutionaryselectionofbrainnetworks Braindisordersimpactingoncognitivefunctionhaveabnormalnetworkproperties,spatiallyandtopologically,suggestingthat i di d i i ii f i h b l k i i ll d l i ll i h neurologicalandpsychiatricsymptomsariseespeciallywhenthemorecostlycomponentsofnetworksarelesioned ordevelop abnormally

Aneconomicalmodelofbrainnetworkorganizationisnotyetrefutedandcouldbenefitfrom furthertesting
Moreprecisecharacterizationofwiringcostinhumannetworks Morestudiesofbrainnetworksinexperimentallytractableanimalmodels Morecomputationalmodelingofnetworkselectionbyeconomiccriteria Morecomprehensiveandlargersamplemappingofnetworkabnormalitiesacrossarangeofbraindisorders

ManyThanks! y

SophieAchard AaronAlexanderBloch Dani Bassett RichardCoppola AlexFornito JayGiedd Carsten Giessing Nitin Gogtay Rik Henson ManfredKitzbichler M f d Kit bi hl Renaud Lambiotte Naaman Mammuz DavidMeunier AndreasMeyerLindenberg JudithRapoport J dith Rapoport RaymondSalvador OlafSporns PetraVertes

HumanBrainProject,NIBIB/NIMH NIH/CambridgePhDProgram CBDB,NIMHIntramuralProgram CBDB NIMH Intramural Program

MRC/Wellcome TrustBehavioural& ClinicalNeurosciencesInstitute MRCCognition&BrainSciencesUnit GlaxoSmithKlineR&D

etb23@cam.ac.uk