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Crowded jewel fish show changes in dendritic spine density and spine morphology
277 hem L%d.
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D
J.W.
BU
and:~G.
n$ v,f P~ych
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S~OW C~C=~ MOi~21RO~Y
~ D~NDRg~C
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COSS , Unh, er~i~ o f Oatf~rrda, Dav;,a, CA Y'~616 (U.S.A.)
o= receivedFebru~" ~h, 1980)
Febma~ ~%h, 1980)
SU~J~Y
s t u d y d e m o ~ t m b e s ~ a t neuronal deveiopment can ~ advemely sho~~ crowding, C o m p ~ e d ~ c r o w d e d sibhngs {15 fish/78-titre), j ~ jewel ~ h ( I 5 ~ h / 3 . G l i e r e ) crowded for 60 days e x h i b i ~ 50--5g% fewer d e n d ~ c s p m ~ and spines with n a ~ o w e r heads on p ~ f o ~ i n ~ m e u r o n s m d ~ p ~ct,~ ~ ~ . These findings indicate that ~ o w d ~ env~aonmen~ ~ produce a b e ~ t neuronal development similax that ~ n in ~ ~ i y deprived jewel fish.
Pre~:ous rm, h e ~ have demonstrated that deveiopment h~ er(~wded e ~ w k o n m ~ c ~ result in. delayed matumtion coupled with hype~espon o give ~ h a v i o r in mamemu~ maramai5 and neonat~ leth~gy or soeia! v~tho _ . d.raw~ in c:hitdren [1,2,3,10,12,18]0 ~fa{~ effects s u r e s t that cro " v~~chng '
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w ~ briefly ~ 0.75% ~ e r ~ o w e d by i onin ~ e ~ 0~75% diver ~ t e for 2 days. ~ e r w ~ and d ~ a g ~ ~ e ~ absolute ethaaol, ~ : ~ y ~ : ~ a t e ~ ~y1~e, co~o:~: ~ o ~ of the o ~ ~ w ~ m o u n ~ and ~ ~ a random number code w*~jch was not b , ~ k ~ un~f ~I n ~ n ~ quan~ficat~o~ was completed, $p:ny p y ~ o ~ :a~er~eum~ we~ ~ ~ for s ~ d y ~ a ~ the~ c o u n ~ and me~ured 37~2 d e n d ~
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279
in~meurons, A 70o#m ~ e n t from the soma to the deepest plexiform h~yer o f ~ e ~tmt~m $ r ~ u m c e n t r e was traced at 1875X using an Olympus mi~sempe e q u ~ p ~ w~th a Zd~s 100X neofluar objec~ve and drawing tube redesigned by Coss to yield neua~na~ d r a ~ of very largescale (I # m = 5.9 ~ ) . Dend~tic branch and spine counts were made from these drawings ( 1)~ of evidence from jewel f~h %~hatspine heads become larger [5], the m a x i m u m spree head widths of allvisually un spines were measured %o the nearest 0.25 nun by aligninga ~e~ pe~cu!ar %0 the spine stem ~.~. Finally, reticlemeasurements were made of ~ec~ @iekness at the locus of each inte~aeurono Data were averaged from 2- 7 intemeurons/f~h in I0 ~ m increm~'n~ from the soma, so ~ t ~ h rather than n e o n popula~ons could be compared by one° factor ana~y~ of vananceo The crowded group exhibi#~edaberrant neuronal developmento Compared w i ~ uncrowded con%ro~ (Fig. 2A), the crowded group had 50% fewer spines be~veen I0 and 20 g m and 58% fewer spines between 20 and 30 g m from t h e soma [ F ( 1 , 8 ) = 1~.42, P < 0°01; F(I~8) = 7.23, P < 0.05]. ~fhus the
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~g, 2. C ~ ~ ia d~d~tie ~ h o l ~ j af~ i n ~ e~owdinl for apron0 60 day~. A: ~owd~ f ~ ( o ~ ba~) h~v~ f ~ e r ~ on a ~ dend~ ~s t h ~ uncrowded
affected ~ay tm~ ed condi~n~ t~ ~ week o f t ~ sxpezimenL ~ o w d ~ fi~h ~ ~ on hu ~ e at~ks° T~rae-samp~ p h o ~ p h i c m e ~ m r ~ e n ~ of ~ c ~ in ~ ancrowded novel aqua~um tha~ as wi~ ~wded ~b~,~ crowded ~ h m a h ~ co~ntIy ck~eer-d~t~uce~ ~ w a r d their nearest neighbor. The apparent a ~ x ~ d devetop~n~ of d e n d ~ sprees h~ our crowded fi~h ( B u ~ e ~ ~ d Co~, in p } e~ the effects of soch~l deprivation obserced m our p z e ~ work w~h t~r~ species [5,6]. Neumr~ in ~ a t~an cereb~al cor~x a~o show lower s~ne [8,14,18,17] and smaller spines [7~ after ~ e ~ r y depr~vatio~, but the effec~ of c ~ w d ~ have ye~ to be ~tudied. ~n our behavioral raeasum~, ~he c~o~r ~w~ o~ed ia the crowded f~h re~mb~ed the effecf~ o:~ ~ o ~ ] d~p~ivation ~ n in other f ~ ~pectes [t3~i5], Since cm p~uces w~dzawai in many an~m~l$, ir~cluding m ~ [2~I0,12~ thi~ c c ~ d be t~ible for the ho~ation effect~~en m ou~ f~h. ~if ~m.~ show similar changes in spine density ( ~ d conso r~ in hut~::::~ neural connectivity), this effec~ ~ y pv~sibty con to the e ~ v e dysfunctioning, h y p e ~ e ~ n s i v e n ~ , ~ d ne~r~t~ i ~ under high density At le~ Increage sma~! sp levek~° .4
cha~act~ concen~ ......... significance for other'~pecies. ACKNOWLEdgMENTS The autho~ R.Go Coss and
~ to
281 ~FEP~NC~ 1 Au~, H. and HoLt, Z., Sozb/er "-S%ress'~hi Tupajas (Tapaia g.~) und seine Wirkvmg auf Wachst~, Korpergewicht umd Fo~pflanzung, Z. Velgl~ich Physiol., 58 (i968) 347--355. 2 ~ua, J~., P o p v ~ o n density and socb/pa%hoic~gy~ ScL Amaer°, 206 (1962) 139--148. 3 C h r i S % J.J. and D a ~ , D.E., Endocrines, behaviom and population~ Science, IC4 ( i ~ ) i550--i550. 4 ~ , R.G., Development of face aversionby %he jewel fish (H2mich~om~ bimacu!a~,e, 1862), Z. T~erpsycho1.,48 (1978) 28--46. 5 C c ~ R~G. and G ] o b ~ A., S_~ne stems on tectalinterneurons in jewei fishare sho~ n e d by ~ a l s%imu~tion, Science, 200 (1978) 787--790. S C ~ , R.G. a~d G ] o b ~ A., So~zialexperience affec~ the development of dendritic sprees ~ d branches or tectalinveraeumrs in the jewel fimh,Dev. Psychobiol°~ 12 (1979) 847--858. 7 Friere,M.J., Effec~ of dark reari~ on dendrite spines in |ayer iV of the mouse vi~a] cortex. A quan~a~/ve e{ect~on microscopic~ s%udy, J. Ana~.: !26 (197g) 198--201. f)Iohus, A. and S~heibel~ A.B, The effeet of visua} depri~a~ion on cor~ic~/neurons: i Golg~ ~udy, Eap. Neurol., 19 (1967) 331--345. 9 Gree~ho~gJh, W.T., Enduring effec~ of different~a~experience and training.In i%ioi%. ~ n z w e ~ g and E.L. Bennett (Eds.),Neural Mech ards~rsof Learning and Merno~y, MIT ~ , Cambridge, t976, pp. 255--278. I0 H~t2~ C. and Va~zey, M.J., ~fferen~al effectsof group density on socialbehavior, Nature (Lend.), 209 (1966) 1371--1372. t i Keppel~ Q . D e ~ and Analys~s.A researcher'shandbook, Prentice Hil, New Jersey~ 1973, p. 551. 12 McGrew~ W.C., An e~hologica] study of children% beha~dor~ Acad~:~mic ~re~, New Y~rk~ 1970. 13 ~ h e L T ~ . ~ o r y informat.ion and ~he organizatio~ of beha~siour in a ~choaHng typhoid f~sh, Anita. ~hav.~ 27 (1979) 1 2 ~ 1 4 9 ° 14 ~eig~ M ~ . and ~nne%, EoL,, ~nr~ched e_nvironmen~,s: f~c'b~, factors and f~acie~. In L. Pei~rinovich ~ d J.L. Mc~augh (Ed~.), Knowing~ thin,king and beiiev~g, ~enun~ Pre~, New York~ 1976, pp. 179=-213. 15 ~ a w , E., ~ d u ~ f i ~ of ~ h ~ i n g a r a ~ g ~ h separa~d and ~h~e no~ separa~d by ba~ Amer~ M ~ . N~i~a~e,, 2373 (t9~9) 1--13. 16 V~v~:~, F, ~ a ~ e~en$ of ~ v e r y fro~ dark ~a~ng in the v~u~l cortex of the ~ o ~ e , Br~n ~ 0 ~ 3S {1971) I--ii, 17 V~] ~ F.R, and G ~ e e ~ , W.T, ~ a n n g ~ m p b ~ t y affect~~ranch~ng of deadeye, in ~h, visuM ~ ~ of ~he t e l ~ b ~ % 17~ (1972) 1445--1447. 18 W~ddr~p.M. arm ~ | | ~ R.Q. E f f e ~ of f a ~ y ~i~ and den~¢y on newborn characterizes, ~. Jo ~hop~ych., 3~ (19~6) 544--550.
' '
D
J.W.
BU
and:~G.
n$ v,f P~ych
(~d (
S~OW C~C=~ MOi~21RO~Y
~ D~NDRg~C
$P~
COSS , Unh, er~i~ o f Oatf~rrda, Dav;,a, CA Y'~616 (U.S.A.)
o= receivedFebru~" ~h, 1980)
Febma~ ~%h, 1980)
SU~J~Y
s t u d y d e m o ~ t m b e s ~ a t neuronal deveiopment can ~ advemely sho~~ crowding, C o m p ~ e d ~ c r o w d e d sibhngs {15 fish/78-titre), j ~ jewel ~ h ( I 5 ~ h / 3 . G l i e r e ) crowded for 60 days e x h i b i ~ 50--5g% fewer d e n d ~ c s p m ~ and spines with n a ~ o w e r heads on p ~ f o ~ i n ~ m e u r o n s m d ~ p ~ct,~ ~ ~ . These findings indicate that ~ o w d ~ env~aonmen~ ~ produce a b e ~ t neuronal development similax that ~ n in ~ ~ i y deprived jewel fish.
Pre~:ous rm, h e ~ have demonstrated that deveiopment h~ er(~wded e ~ w k o n m ~ c ~ result in. delayed matumtion coupled with hype~espon o give ~ h a v i o r in mamemu~ maramai5 and neonat~ leth~gy or soeia! v~tho _ . d.raw~ in c:hitdren [1,2,3,10,12,18]0 ~fa{~ effects s u r e s t that cro " v~~chng '
:
j!Li~L
D /!i
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i¸¸¸¸¸%¸/
:17
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urn. A~: ddee o: ~
e~h
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~
were
~
m ~ ~u~
~ ,
~:~g
u
.
ofO.~ ¢mnum ~o::e
w ~ briefly ~ 0.75% ~ e r ~ o w e d by i onin ~ e ~ 0~75% diver ~ t e for 2 days. ~ e r w ~ and d ~ a g ~ ~ e ~ absolute ethaaol, ~ : ~ y ~ : ~ a t e ~ ~y1~e, co~o:~: ~ o ~ of the o ~ ~ w ~ m o u n ~ and ~ ~ a random number code w*~jch was not b , ~ k ~ un~f ~I n ~ n ~ quan~ficat~o~ was completed, $p:ny p y ~ o ~ :a~er~eum~ we~ ~ ~ for s ~ d y ~ a ~ the~ c o u n ~ and me~ured 37~2 d e n d ~
~20
and 305 ~ c h ~ o~ 42 ~
279
in~meurons, A 70o#m ~ e n t from the soma to the deepest plexiform h~yer o f ~ e ~tmt~m $ r ~ u m c e n t r e was traced at 1875X using an Olympus mi~sempe e q u ~ p ~ w~th a Zd~s 100X neofluar objec~ve and drawing tube redesigned by Coss to yield neua~na~ d r a ~ of very largescale (I # m = 5.9 ~ ) . Dend~tic branch and spine counts were made from these drawings ( 1)~ of evidence from jewel f~h %~hatspine heads become larger [5], the m a x i m u m spree head widths of allvisually un spines were measured %o the nearest 0.25 nun by aligninga ~e~ pe~cu!ar %0 the spine stem ~.~. Finally, reticlemeasurements were made of ~ec~ @iekness at the locus of each inte~aeurono Data were averaged from 2- 7 intemeurons/f~h in I0 ~ m increm~'n~ from the soma, so ~ t ~ h rather than n e o n popula~ons could be compared by one° factor ana~y~ of vananceo The crowded group exhibi#~edaberrant neuronal developmento Compared w i ~ uncrowded con%ro~ (Fig. 2A), the crowded group had 50% fewer spines be~veen I0 and 20 g m and 58% fewer spines between 20 and 30 g m from t h e soma [ F ( 1 , 8 ) = 1~.42, P < 0°01; F(I~8) = 7.23, P < 0.05]. ~fhus the
l
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28°38
~g, 2. C ~ ~ ia d~d~tie ~ h o l ~ j af~ i n ~ e~owdinl for apron0 60 day~. A: ~owd~ f ~ ( o ~ ba~) h~v~ f ~ e r ~ on a ~ dend~ ~s t h ~ uncrowded
affected ~ay tm~ ed condi~n~ t~ ~ week o f t ~ sxpezimenL ~ o w d ~ fi~h ~ ~ on hu ~ e at~ks° T~rae-samp~ p h o ~ p h i c m e ~ m r ~ e n ~ of ~ c ~ in ~ ancrowded novel aqua~um tha~ as wi~ ~wded ~b~,~ crowded ~ h m a h ~ co~ntIy ck~eer-d~t~uce~ ~ w a r d their nearest neighbor. The apparent a ~ x ~ d devetop~n~ of d e n d ~ sprees h~ our crowded fi~h ( B u ~ e ~ ~ d Co~, in p } e~ the effects of soch~l deprivation obserced m our p z e ~ work w~h t~r~ species [5,6]. Neumr~ in ~ a t~an cereb~al cor~x a~o show lower s~ne [8,14,18,17] and smaller spines [7~ after ~ e ~ r y depr~vatio~, but the effec~ of c ~ w d ~ have ye~ to be ~tudied. ~n our behavioral raeasum~, ~he c~o~r ~w~ o~ed ia the crowded f~h re~mb~ed the effecf~ o:~ ~ o ~ ] d~p~ivation ~ n in other f ~ ~pectes [t3~i5], Since cm p~uces w~dzawai in many an~m~l$, ir~cluding m ~ [2~I0,12~ thi~ c c ~ d be t~ible for the ho~ation effect~~en m ou~ f~h. ~if ~m.~ show similar changes in spine density ( ~ d conso r~ in hut~::::~ neural connectivity), this effec~ ~ y pv~sibty con to the e ~ v e dysfunctioning, h y p e ~ e ~ n s i v e n ~ , ~ d ne~r~t~ i ~ under high density At le~ Increage sma~! sp levek~° .4
cha~act~ concen~ ......... significance for other'~pecies. ACKNOWLEdgMENTS The autho~ R.Go Coss and
~ to
281 ~FEP~NC~ 1 Au~, H. and HoLt, Z., Sozb/er "-S%ress'~hi Tupajas (Tapaia g.~) und seine Wirkvmg auf Wachst~, Korpergewicht umd Fo~pflanzung, Z. Velgl~ich Physiol., 58 (i968) 347--355. 2 ~ua, J~., P o p v ~ o n density and socb/pa%hoic~gy~ ScL Amaer°, 206 (1962) 139--148. 3 C h r i S % J.J. and D a ~ , D.E., Endocrines, behaviom and population~ Science, IC4 ( i ~ ) i550--i550. 4 ~ , R.G., Development of face aversionby %he jewel fish (H2mich~om~ bimacu!a~,e, 1862), Z. T~erpsycho1.,48 (1978) 28--46. 5 C c ~ R~G. and G ] o b ~ A., S_~ne stems on tectalinterneurons in jewei fishare sho~ n e d by ~ a l s%imu~tion, Science, 200 (1978) 787--790. S C ~ , R.G. a~d G ] o b ~ A., So~zialexperience affec~ the development of dendritic sprees ~ d branches or tectalinveraeumrs in the jewel fimh,Dev. Psychobiol°~ 12 (1979) 847--858. 7 Friere,M.J., Effec~ of dark reari~ on dendrite spines in |ayer iV of the mouse vi~a] cortex. A quan~a~/ve e{ect~on microscopic~ s%udy, J. Ana~.: !26 (197g) 198--201. f)Iohus, A. and S~heibel~ A.B, The effeet of visua} depri~a~ion on cor~ic~/neurons: i Golg~ ~udy, Eap. Neurol., 19 (1967) 331--345. 9 Gree~ho~gJh, W.T., Enduring effec~ of different~a~experience and training.In i%ioi%. ~ n z w e ~ g and E.L. Bennett (Eds.),Neural Mech ards~rsof Learning and Merno~y, MIT ~ , Cambridge, t976, pp. 255--278. I0 H~t2~ C. and Va~zey, M.J., ~fferen~al effectsof group density on socialbehavior, Nature (Lend.), 209 (1966) 1371--1372. t i Keppel~ Q . D e ~ and Analys~s.A researcher'shandbook, Prentice Hil, New Jersey~ 1973, p. 551. 12 McGrew~ W.C., An e~hologica] study of children% beha~dor~ Acad~:~mic ~re~, New Y~rk~ 1970. 13 ~ h e L T ~ . ~ o r y informat.ion and ~he organizatio~ of beha~siour in a ~choaHng typhoid f~sh, Anita. ~hav.~ 27 (1979) 1 2 ~ 1 4 9 ° 14 ~eig~ M ~ . and ~nne%, EoL,, ~nr~ched e_nvironmen~,s: f~c'b~, factors and f~acie~. In L. Pei~rinovich ~ d J.L. Mc~augh (Ed~.), Knowing~ thin,king and beiiev~g, ~enun~ Pre~, New York~ 1976, pp. 179=-213. 15 ~ a w , E., ~ d u ~ f i ~ of ~ h ~ i n g a r a ~ g ~ h separa~d and ~h~e no~ separa~d by ba~ Amer~ M ~ . N~i~a~e,, 2373 (t9~9) 1--13. 16 V~v~:~, F, ~ a ~ e~en$ of ~ v e r y fro~ dark ~a~ng in the v~u~l cortex of the ~ o ~ e , Br~n ~ 0 ~ 3S {1971) I--ii, 17 V~] ~ F.R, and G ~ e e ~ , W.T, ~ a n n g ~ m p b ~ t y affect~~ranch~ng of deadeye, in ~h, visuM ~ ~ of ~he t e l ~ b ~ % 17~ (1972) 1445--1447. 18 W~ddr~p.M. arm ~ | | ~ R.Q. E f f e ~ of f a ~ y ~i~ and den~¢y on newborn characterizes, ~. Jo ~hop~ych., 3~ (19~6) 544--550.