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A connection to the past: Monodelphis domestica provides insight into the organization and connectivity of the brains of early mammals

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A connection to the past: Monodelphis domestica provides insight into the organization and connectivity of the brains of early mammals
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                         James C Dooley 1 , João G. Franca 2 , Adele M. H. Seelke 1 , Dylan F. Cooke 1,3 , Leah A. Kr!"#$er  1,3 1 Cen#er %or &erosc"ence and 3 De'ar#men# o% (sycholo)y *n"+ers"#y o% Cal"%orn"a, Da+"s Da+"s, Cal"%orn"a, -1/, *SA 2 0ns#"##o de "o%s"ca Carlos Cha)as F"lho, *n"+ers"dade Federal do "o de Jane"ro, "o de Jane"ro, 2141562, ra$"l nn"n) Head7 Connec#"ons o% soma#osensory cor#e8 "n )ray shor#5#a"led o'ossms Key ;ords7 Mars'"al, cor#"cal e+ol#"on, ml#"modal cor#e8, 3a, 3!, 'os#er"or 'ar"e#al Corres'ond"n) A#hor7 Leah Kr!"#$er Cen#er %or &erosc"ence 1-44 &e:#on C#. Da+"s, CA -1 (hone7 -365<-<5/// 9ma"l7 lakr!"#$er=cda+"s.ed S''or#7 >h"s 'ro?ec# :as s''or#ed !y %nds #o Leah Kr!"#$er %rom &0&DS @21&S6<122- and &90 @61 9B622/< #o Joao Franca %rom C&(  ra$"l @'roc. no. 266<13E266/5 and James Dooley %rom &90 @>3259B61-3/<56-. Research ArticleThe Journal of Comparative NeurologyResearch in Systems NeuroscienceDOI 10.1002/cne.23383This article has been accepted for publication and undergone full peer review but has not beenthrough the copyediting, typesetting, pagination and proofreading process which may lead todifferences between this version and the Version of Record. Please cite this article as an‘Accepted Article’, doi: 10.1002/cne.23383© 2013 Wiley Periodicals, Inc.Received: Mar 06, 2013; Revised: May 29, 2013; Accepted: Jun 07, 2013     >he crren# e8'er"men# "s one o% a ser"es o% com'ara#"+e s#d"es "n or la!ora#ory des")ned #o de#erm"ne #he ne#:ork o% soma#osensory areas #ha# :as 'resen# "n #he neocor#e8 o% #he mammal"an common ances#or. Sch kno:led)e "s cr"#"cal %or a''rec"a#"n) #he !as"c %nc#"onal c"rc"#ry #ha# all mammals 'ossess and ho: #h"s c"rc"#ry :as mod"%"ed #o )enera#e s'ec"es s'ec"%"c, sensory med"a#ed !eha+"or. r an"mal model, #he )ray shor#5#a"led o'ossm @    "s a mars'"al #ha# "s 'ro'osed #o re'resen# #h"s ances#ral s#a#e more closely #han mos# o#her mars'"als and #o some e8#en#, e+en mono#remes. ;e "n?ec#ed neroana#om"cal #racers "n#o #he 'r"mary soma#osensory area @S1, ros#ral and cadal soma#osensory %"elds @S and SC, res'ec#"+ely, and ml#"modal cor#e8 @MM and de#erm"ned #he"r connec#"ons :"#h o#her arch"#ec#on"cally de%"ned cor#"cal %"elds. r resl#s sho: #ha# S1 has dense "n#r"ns"c connec#"ons, dense 'ro?ec#"ons %rom #he %ron#al myel"na#ed area @FM, and modera#e 'ro?ec#"ons %rom S2 and SC. S has s#ron) 'ro?ec#"ons %rom se+eral areas, "ncld"n) S1, S, FM and '"r"%orm cor#e8. SC has dense 'ro?ec#"ons %rom S1, modera#e #o s#ron)  'ro?ec#"ons %rom o#her soma#osensory areas, FM, alon) :"#h connec#"+"#y %rom #he 'r"mary @1 and second +"sal areas. F"nally, MM had dense "n#r"ns"c connec#"ons, dense 'ro?ec#"ons %rom SC and 1, and modera#e 'ro?ec#"ons %rom S1. >hese da#a s''or# #he 'ro'os"#"on #ha# ances#ral mammals l"kely had a# leas# %or s'ec"%"cally "n#erconnec#ed soma#osensory areas, alon) :"#h a# leas# one ml#"modal area. ;e d"scss #he 'oss"!"l"#y #ha# #hese add"#"onal soma#osensory areas @SC and S are homolo)os #o soma#osensory areas "n e#her"an mammals. Page 2 of 57John Wiley & SonsJournal of Comparative Neurology     >he emer)ence o% #he neocor#e8 and "#s e8'ans"on "s #he hallmark o% mammal"an e+ol#"on @Kr!"#$er, 266<. ;h"le !o#h com'ara#"+e 'aleon#olo)y and modern )enom"c analys"s ha+e 'ro+"ded e8c"#"n) ne: "ns")h#s "n#o #he chronolo)y @Lo e# al., 2663 Lo e# al., 2611 ILeary e# al., 2613, !ra"n s"$e and ence'hal"$a#"on @o:e e# al., 2611, and "n#erord"nal rela#"onsh"'s @Halls#rom and Janke, 266/ o% early mammals, or nders#and"n) o% ances#ral  !ra"n or)an"$a#"on rema"ns l"m"#ed !ra"n #"sse does no# %oss"l"$e, and cran"al endocas#s 'ro+"de "n%orma#"on only on )ross !ra"n mor'holo)y and s"$e. Be# !ra"n or)an"$a#"on "s a :"ndo: "n#o #he !eha+"or o% or earl"es# ances#ors, no# only 'ro+"d"n) a +"e: o% ho: #hey 'erce"+ed and "n#erac#ed :"#h #he :orld, !# also :ha# #y'es o% sensory5med"a#ed !eha+"ors :ere s!?ec# #o selec#"on @Kr!"#$er and Seelke, 2612. >he )oal o% #he 'resen# "n+es#")a#"on "s #o "llm"na#e #he  !as"c 'lan o% cor#"cal or)an"$a#"on and connec#"+"#y o% early mammals !y e8am"n"n) #he )ray shor#5#a"led o'ossm, 'ro'osed #o resem!le #h"s early ances#or more #han o#her l"+"n) s'ec"es. Al#ho)h mono#remes %orm #he earl"es# mammal"an rad"a#"on :hose ances#ors d"+er)ed a''ro8"ma#ely 26<523< m"ll"on years a)o @MBA, #hey are h")hly der"+ed, so s#d"es o% #he"r  !ra"n or)an"$a#"on and connec#"+"#y 'ro+"de se%l, !# some:ha# l"m"#ed "n%orma#"on on #he  !ra"ns o% early, ances#ral mammals @;ood!rne e# al., 2663 (ere"ra and aker, 266 +an heede e# al., 266 H)all e# al., 266<. Me#a#her"ans, "ncld"n) mars'"als, d"+er)ed la#er #han mono#remes @12<.-516 MBA Mered"#h e# al., 2611 ILeary e# al., 2613 and nl"ke mono#remes, many small !ra"ned, less der"+ed mem!ers o% #h"s clade are #ho)h# #o !e mor'holo)"cally s"m"lar #o ances#ral mammals @;on) and Kaas, 266 o:e e# al., 2611. >here are :ell o+er 366 s'ec"es o% mars'"als "n As#ral"a and #he Amer"cas, and #he"r e8#ernal mor'holo)y and !eha+"or e+ol+ed "n 'arallel #o #ha# o% e#her"an mammals #o ada'# #o a Page 3 of 57John Wiley & SonsJournal of Comparative Neurology    ml#"#de o% #erres#r"al, ar!oreal and aa#"c en+"ronmen#s @Karlen and Kr!"#$er, 266<, s))es#"n) #ha# a !as"c 'lan o% !ody and !ra"n or)an"$a#"on #rans%ormed "nde'enden#ly, !# "n a s"m"lar manner, "n #hese #:o ma?or l"nea)es. Des'"#e #he"r 'rol"%"cacy and #he"r "m'or#ance %or nders#and"n) !ra"n e+ol#"on, rela#"+ely l"##le "s kno:n a!o# #he cor#"cal sensor"mo#or c"rc"#ry #ha# dr"+es #he"r !eha+"or.   >he )ray shor#5#a"led o'ossm @     "s a small cre'sclar mars'"al na#"+e #o So#h Amer"ca, and one o% #he %e: mars'"al s'ec"es crren#ly !red "n la!ora#ory cond"#"ons. ;e s#dy    %or se+eral cr"#"cal reasons. F"rs#, as no#ed a!o+e, !ecase mars'"als ances#ors arose +ery early "n mammal"an e+ol#"on, e8am"n"n) #he cor#"cal or)an"$a#"on and connec#"+"#y o% modern mars'"als cold 'ro+"de "m'or#an# "ns")h#s "n#o #he  !ra"ns o% #he %"rs# mammals, allo:"n) s #o a''rec"a#e #he !as"c cor#"cal c"rc"#ry common #o all mammals. A second reason "s #ha# s#d"es o% mars'"al mo#or cor#e8 "nd"ca#e #ha# "# "s com'le#ely em!edded "n or o+erla''"n) :"#h soma#osensory cor#e8 @e.). Lende, 13a Lende, 13! Lende, 13c ees and Hore, 1<6 Ma)alhaes5Cas#ro and Sara"+a, 1<1 eck e# al., 1 Fros# e# al., 2666 Karlen and Kr!"#$er, 266<. >h"s %ea#re o% #he mars'"al cor#e8 "s re%lec#ed "n 'a##erns o% connec#"+"#y o% S1, :h"ch rece"+es "n'#s assoc"a#ed :"#h !o#h soma#"c and mo#or cor#e8 %rom #he #halams @K"llackey and 9!ner, 1<3 Joschko and Sanderson, 1/<. Ho: #h"s #y'e o% or)an"$a#"on l#"ma#ely e%%ec#s !eha+"or "s nclear s"nce !as"c 'a##erns o%  !eha+"or "n mars'"als are remarka!ly s"m"lar #o #he"r mor'holo)"cally e"+alen# e#her"an con#er'ar#s @e.). As#ral"an s#r"'ed 'ossm +s. Mala)sy aye aye 9r"ckson e# al., 1/ a:l"ns and Handasyde, 2662. >h"rd, mars'"als are !orn e8#remely "mma#re, a# de+elo'men#al #"me  'o"n#s #ha# corres'ond #o em!ryon"c e+en#s "n e#her"an mammals. >hese an"mals #here%ore make e8cellen# models o% cor#"cal de+elo'men#. For#h, a'ar# %rom #h"s me#hodolo)"cal ad+an#a)e "s Page 4 of 57John Wiley & SonsJournal of Comparative Neurology    #he o+erlooked e%%ec# o% #h"s 'rema#re !"r#h on #he de+elo'men# o% #he soma#osensory and mo#or sys#ems. *nl"ke mos# e#her"an mammals, mars'"als @'ar#"clarly #hose #ha# de+elo' "n a  'sedo'och l"ke )ray shor#5#a"led o'ossms ha+e access #o e8#remely early #ac#"le "n'#s  !e%ore and dr"n) #he de+elo'men# o% cen#ral soma#osensory 'a#h:ays. Ho: #h"s "m'ac#s #he or)an"$a#"on, connec#"+"#y and l#"ma#e sensory med"a#ed !eha+"or o% mars'"als "s an "m'or#an# "sse #ha# has ye# #o !e addressed. Mars'"als "ncld"n)     ha+e !een sho:n #o ha+e #:o com'le#e soma#o#o'"c re'resen#a#"ons :"#h"n #he cor#e8, #he 'r"mary soma#osensory area, S1, and #he second soma#osensory area, S2 @H%%man e# al., 1 Ca#an"a e# al., 2666 Fros# e# al., 2666 Karlen and Kr!"#$er, 266<. ased on elec#ro'hys"olo)"cal record"n)s, arch"#ec#on"c analys"s and 'a##erns o% connec#"ons, some s#d"es "nd"ca#e #ha# mars'"als ha+e #:o #o #hree add"#"onal %"elds assoc"a#ed :"#h soma#osensory 'rocess"n) a ros#ral %"eld #ermed  or S, a cadal %"eld #ermed C or SC, and a 'ar"e#al +en#ral area, ( @eck e# al., 1 9ls#on and Man)er, 1 H%%man e# al., 1 ;on) and Kaas, 266 Anomal e# al., 2611. Des'"#e #he "m'or#an#  'hylo)ene#"c 'os"#"on o% mars'"als, and #he "m'l"ca#"ons #ha# cor#"cal 'rocess"n) ne#:orks o% early mammals may !e more com'le8 #han :ere 're+"osly #ho)h#, l"##le "s kno:n a!o# #he cor#"cal connec#"+"#y o% soma#osensory areas "n #h"s )ro' o% mammals @see d"scss"on. >he s'ec"%"c a"m o% #he 'resen# "n+es#")a#"on :as #o e8am"ne #he cor#"cal connec#"ons o% #hree soma#osensory %"elds "n    , S1, S and SC. >h"s :as done !y "n?ec#"n) ana#om"cal #racers "n#o arch"#ec#on"cally andEor elec#ro'hys"olo)"cally de%"ned loca#"ons :"#h"n #hese %"elds, and rela#"n) 'a##erns o% connec#"+"#y #o arch"#ec#on"cally de%"ned cor#"cal %"elds "n #he "'s"la#eral and con#rala#eral hem"s'here. >hese da#a %rom each hem"s'here :ere #hen an#"%"ed so #ha# rela#"+e dens"#y o% connec#"ons cold !e assessed. Com'ar"sons o% Page 5 of 57John Wiley & SonsJournal of Comparative Neurology
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