Developmental changes in brain connectivity assessed using t

Developmental changes in brain connectivity assessed using the sleep EEG

DEVELOPMENTAL CHANGES IN BRAIN CONNECTIVITY ASSESSED USING THE SLEEP EEG

L.TAROKH,a,b,c*M.A.CARSKADON a,b AND

P.ACHERMANN c,d,e

a E.P.Bradley Sleep Research Laboratory,Providence,RI,USA

b Department of Psychiatry and Human Behavior,Alpert Medical School of Brown University,Providence,RI,USA

c Institute of Pharmacology an

d Toxicology,University of Zurich,Zu-rich,Switzerland

d Zurich Center for Integrativ

e Human Physiology,University o

f Zurich, Zurich,Switzerland

e Neuroscience Center,University and ETH Zurich,Zurich,Switzerland Abstract—Adolescence represents a time o

f signi?cant cor-tical restructuring.Current theories posit that durin

g this period connections between frequently utilized neural net-works are strengthened while underutilized synaptic connec-tions are discarded.The aim of the present study was to examine the developmental evolution of connectivity be-tween brain regions using the sleep EEG.All-night sleep EEG recordings in two longitudinal cohorts(children and teens) followed at1.5–3year intervals and one cross-sectional co-hort(adults)were analyzed.The children and teen cohorts were9/10and15/16years at the initial assessment;ages of the adults were20to23years.Intrahemispheric,interhemi-spheric,and diagonal coherence was measured between all six possible pairings of two central(C3/A2and C4/A1)and two occipital(O2/A1and O1/A2)derivations during slow wave,stage2,and,REM sleep.Within-subjects analyses were performed for the children and teen cohorts,and a linear regression analysis was performed across every as-sessment of all cohorts.Within-subject analyses revealed a maturational increase in coherence for bot

h age cohorts, though the frequencies,sleep states,and regions differed between cohorts.Regression analysis across all age cohorts showed an overall linear increase in left and right intrahemi-spheric coherence for all sleep states across frequencies. Furthermore,coherence between diagonal electrode pairs also increased in a linear manner for stage2and REM sleep. No age-related trend was found in interhemispheric coher-ence.Our results indicate that sleep EEG coherence in-creases with age and that these increases are con?ned to speci?c brain regions.This analysis highlights the utility of the sleep EEG to measure developmental changes in brain maturation.©2010IBRO.Published by Elsevier Ltd.All rights reserved.

Key words:sleep EEG,brain development,coherence,longi-tudinal.As childhood ends,a period of expansive brain reorgani-zation begins.A decline in synaptic density is observed in the healthy human cortex starting near ages9or10and continuing into early adulthood.This decline is re?ected in a number of neural measures.MRI studies—including a longitudinal study(Gogtay et al.,2004)—have shown sig-ni?cant decreases in cortical and subcortical grey matter across adolescent development(Steen et al.,1997;Pfef-ferbaum et al.,1994;Shaw et al.,2008;Giedd et al.,1999). These changes are mirrored by declines in blood glucose metabolism assessed by PET(Chugani et al.,1987)and by reduced synchronous neural activity indexed by waking (for a review see Segalowitz et al.,2010)and sleep elec-troencephalogram(EEG)(Campbell and Feinberg,2009; Tarokh and Carskadon,2010a)power.A relatively steady state in these measures is not reached until early adult-hood,between the ages of19and25.

In addition to the maturational decline in the number of cortical synapses,adolescent development is accompa-nied by modi?ed connectivity between brain regions. Stevens(2009)has proposed that a decline in EEG power and an increase in regional connectivity are complemen-tary processes that support cognitive gains observed dur-ing this period.According to this model,adolescent brain development involves“discarding”unused synapses thereby decreasing the amplitude of neural activity.Con-currently,connections frequently utilized are strengthened, leading to the emergence of more complex and ef?cient networks.Stevens’proposal aligns with the prominent the-ory of cognitive development called“neural constructiv-ism,”which postulates that age-related cognitive improve-ments result from increased inter-connectivity and func-tional specialization of neural networks(Quartz and Sejnowski,1997).

Connectivity between brain regions is inferred from temporal associations between spatially remote neuro-physiological events.One such measure of connectivity is correlation between two simultaneously recorded signals in the frequency domain,called coherence,which can be assessed in humans using fMRI and EEG.A major as-sumption is that strong correlation of neural activity be-tween two distal brain regions provides evidence that those regions are connected or that a common third region drives the activity of both regions.A corollary assumption is that coherence depends on axonal anatomical linkage between brain regions;however,coherence can also re-?ect dynamic and transient activity between brain regions. One way to distinguish between these two possibilities is by examining coherent activity in different neurophysiolog-ical states:coherence based on anatomical linkage should

*Correspondence to:L.Tarokh,E.P.Bradley Sleep Research Labo-

ratory,300Duncan Drive,Providence,RI02906,USA.Tel:?1-401-

421-9440;fax:?1-401-453-3587.

E-mail address:Leila_Tarokh@brown.edu(L.Tarokh).

Abbreviations:EMG,electromygram;NREM,non-REM;REM,rapid

eye movement;TIB,time in bed.

Neuroscience171(2010)622–634

0306-4522/10$-see front matter©2010IBRO.Published by Elsevier Ltd.All rights reserved. doi:10.1016/j.neuroscience.2010.08.071

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Developmental changes in brain connectivity assessed using the sleep EEG

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