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Electrophysiological investigation of the connection between the substantia nigra and the amygdala in rat
Ne~e~nee © E~
265
LeCtern, 17 ( 1980} 2~5--2~9
.Holland Selene[fie ~ a b ~ e ~ Ltd.
ELE~OP~$~OLO~ICAL LNVE~77GATTON OF THE- C O ~ C i ~ I O N BE~~N S~~ANTIA.~G~,AN T H E k~MYGDALA ~%~ A T
8. BAI%A~.~I* a~ of
8H
PAY , P.O. B o x 7 8 , O-nfvemfty College, Cardff~, CFI !XL (U.tL)
(R November 27th, 1979) (Re~d n January 22nd, 1980) (Accep~d J a n ~ 24~h, 1980)
SUMMARY
The present study concerns an electrophysiologieat investigation of the reciprocal neuronal connections between the SN ,and the amygdata in the rat, Using the eollisiono~est technique the e~istenee of a slowly conducting nigro~my~ata ~ been confirmed° tn addition a pathway originating in the c e n t ~ nueteu~ of the amygdala ~ d terminating in th~ SN h ~ also been demonstrated,
Recent evidence h~¢5 s ted that the substantia nigra {SN) may be involved in nociceptive mech raisins [ 1,7,I2,13]° One possibility is that the SN may modify a e t i ~ t y ~ t h i n the limbic system thus influencing the affec~ive c o m p o n e n t of the response to a noxious st,ira ~ius, existence of a leaved from both (HBP} studies i t h the recipIocal ......... )retie md a electro° ese two nude1 a ~ ~ exist we t h e r e f o ~ d e e l d e d , o Ftudy these p r o p o ~ d sod Wisgsr ~spo~lses 7! Blue ~£ 42 m
from
~
[9].
4°5--8°0 ~
accozd~g to @e a t ~ of
Lug
es
(Ehod~ M ~ ~ e n ~ S ~ 1 0 0 } were i~pLan~d k ~ e i cenlTA n of ~he a m y , S . ~ on b ~ ] o C c ~ e x ~ a f i o n , the f o l I o \ ~ co-o~na~e~ h ~ e been fo-~d ~ be the m ~ :pp~p~mte: A: 4A ram; L: 3.7 ram; V: 7.0 ~r,~,. S ~ . v a ~ o : of We amygdala was effec~e.d w w 4 ~ u a ~ wave ~ 0.05--0.2 ~ in dura~on with a ~'~m in~r~kW of Od5 m A ( t ~ o ~ i n ~ ~ app~om O.I ~ ) o The effe~ of ~ n y ~ s ~ u t a t ~ o a was on @ontaneoa~y active ~eu~o~es ~ecorded in the SN, The c o n ~ n 4 e $ ; tecbr~que was ed £n ever~ study to df~gngu~h between or~hc~i~omic and antid~omma~y ac'~vated neamne~ m G~e SNo A ~ h o ~ ea~e~ repor~ h~'e reh'edupon @~ constant ]stoney of the e v o k ~ ~e~ponse as a caledon for an~/d~om~ n, f~e ~e~ulf~ ~ o w n in Fig. l b conf~m a zecent suggest/on that ~¢oked z e s p o ~ in an~dmmic pathways a~e offen of variable ~atency [10]~ ~t i~n o w generallya~cepted that the collision-testtechnique i~ the most stringenttech~que enabling anfid~omic ac~4by to be rddab|y demon,%rated [6), A totalof 51 non,ones have been ~ecorded within the SNo Fo~y (78%) of these neuron~ did not ~espond to a~nygdah~~rau~t~on. Of ~he ~ema[ning 11 neu~na~, 8 (18%) were o~thod~n/cally activated and 8 (6%) were elea~lyant~dzomiea~y act/rated.F~a~e ~ ~/]ust~tes~ecordin~ made fxom an antidmm~caUy activated SN neurone. Tm~e la show~ the evidence of collision (ablate of an evoked r~ponse foHow~ng amygd~/a stirauL~tion) and the co~/~ion time can be obtained from the ]ower ~t of ~ s (Ib). The average latency of the antid~miea~[y conducted _ac~ivltywithln the ni~o~ amygd.~a pathw~y was found to be i0 ~ . A~umi~g a path ]en~h of 3 rnm~ [4,9] the average conduction veJocity~sthus 0.S m s ~ ~. Activity withi:~the au%y~da~o-ni~i pathway can [end to both exciSe/on and inhabit/onof m ~ neurones. The ea~H~st component of the ~e~po ~se was usuallyan evoked action potent(s) having a mean la~ney of 14 reset. ~n 4 neu~ones (a][found in the zona retieu~ata)~ eaHy componemt was the only type of activityre~o~d~ in response to amygdgla sti.m~l~on. H o w ° eveL four neurones located w~th~ the zona eomp~ta ai~o e~v/~bitedan inhibitory response.This W~ manffes~ asa ¢ on o spon~eous f~mg and lastedup to ~00 mSeCo The ~e~o~ing ~/]u~ in Fig. 2a ~hows an ex~.p]e of a va~dab~elatency orthod~omiea~y conducted re~ponse. Fibre 2b depicts the inh~ition of spontaneous ae~/vity fo~/ow~ug amygdab stimu]afiono Fo~owh~g the iontopho~et/c egmfion of PSB from the re~ord~g elee-ttode it has been possible to dete_~hle ~he location of alln~uron~ studied° In this study the ni&~o-an~y~daJaou~pu~ neumon~s have been found v~thin the late~ asp~t ~of the ~:ona Meibach [11] noted %hat c, amygd~/ao in addition th~ i8o~oo
267 a
d
b
, A 16~0!
"I s
Hg. 1. ~ p ~ of a zo~ r e ~ c u ~ neurone projectingto the central nuc~eu~ of amygd~. Tvace~ a and b ~ e ~ ob~ned frora the ~ e neurone. (a) Five con~ecu~ve trace~ of ~ ~ f~om a ~ona r e ~ c u ~ neurone ~ re~on~e to amygda~a ~timu]at~on {~imulu$ art~a~ indica~d by ~he arrow). ~n ~he ~econd ~ace a ~pon~neou~ action po~n~al (ind~ca~d by the ~ k ) c ~ l y precede~ ~timulation, resu]~ng in collision. ~ charae'~e~d by ~ ab~en~ of an evoked action polariS. Calibrationbar = 2 ~c, (b) ~ the u~er ~ee, a ~mnWneou~ action po~n~a~ ~gger~ the ~tirnulu~ after ~ ~ ~ of 7 r~ec.~ evoking an a~ion po~enti~ ~ each i r ~ c e . No~ ~he vaMable |a~ncy of ~ evoked r e ~ ~ . ~ the lower ~race,the interval between the ~pont~ne.ou~ e~:~on ~ t i ~ ~ d s ~ m ~ ~ dec~ec~edby i ~ec. ~ulthag in coOl,ion. Each trace co~ of ~ ~wee~. C ~ b ~ o n bar - 2 ~ c . (e) ~ a g ~ m of ~t~n~ula~ion ~i~ b ~ d on the ~n~g and ~ p p e l rat br~n atla~ [9]. ac, nuc~eu~ a~nygdaloideu~ centrali$; cai. in,real ~ u ~ ° (d) ~ t i o n of the z~na reticu~a neurone recorded in the sub, tanaka nigra (82q.). a m y g d a ~ neurones are a ~ o ]oca~
b
d
269
Efferent c~nnec~ior~ o~ the ~
~ . ~ 175 (1979) i 9 ~
4
, B ~ . and A ~ t ~ ~ G.K°, The p ~ Itemization of nigral afferen~ in the by a r e ~ ~raeSng ~_ehnique, ~ n ~ . , 117 (1976) 422--435° j~ , ., e inaervat2on of R e ~ forebrain (IV).
5
, ~,,
ra~ ~
6
J;H. ~
8 9 10 11 12 13 14 15
R,Y., Subs~nl2a nigra d o p ~ i n e neurone~: the n e ~ t r i a t u m ~Jad ail~or~e~:, Neurosci. L e t t . 7
, J.D., ~ r m i n a f i o n of anfi4romic e~:eitation by ?:he cot~sionof inVerpret~on, Brain Res., 112 (1976) 283--298. M., Nico~u, N.M., ~fliock, : . F , WrighL A.K. and Arbuthnott, G.W., Feedb~mk l ~ p or output pathway in ~aC~onigral fibres? NaCre (Lond.), 265 (!977) 363--365. Jurna, I., Heinz, G., Btinn, G. and Nell, T., The effect of substantia rAgra stimulation and morphine on ~-motoneurones and the taft flick response, Europ. J. PharraacoL, 51 ( 1978) 239--250. KSnig, J.F°R. and Klippet, R.A., The rat brain, Wiliiams& Wflkin~, Baitiraore, 19~3. Mayer, M . L , Variable latency an~idro~c re~po~e~ of preoptic-an~erior h:~pothalamic neumne~ in ~he tail, J. Phy~ioi (Load.), 289 (1979) 80P. Meibach, R . C , Evidence for a duat dopaminergic ~ b ~ a n t i a ~igro-arnygdaia pro~ec° tion in ~:he caL Ana~. Rec., I93(3)(1979) ~21. Price, H.T.C. and Fibiger~ H.C., Ascending catecholamine ~s~eras and morphine anaigeuia~ Brain Re~., 99 (1975) 189-193. Sandberg, D.Eo and Seg~l, M., Pharraacoiogical anaiy~i~ of anslge~a and ~e!f stimuta o tion elicited by eiectrical ~¢imulation of catecho~ami~e nuclei it: the ra~ brain. Brain Reu., 152 (1978) 529--542. Simon, H,, Le Mout, M. and Ca~a~, A., Efferent~ and afferent~ of the ventral ~egraenta] A~lO region ~ d i e d afl~r ioca~ ion i~H]tencine and i~)r~eradish ~ r o ~ d a ~ Brain Reu., 178 (t978) 17~40o Ur~gc~dt~ U., S~creol;a~:ic ~nappir~ of. ~he monoamine pathways in the ra~ brain~ Acta phy~ioL ~cand. (Suppi.) ~67 (1971) 1.
¢~: 7
y, H;
265
LeCtern, 17 ( 1980} 2~5--2~9
.Holland Selene[fie ~ a b ~ e ~ Ltd.
ELE~OP~$~OLO~ICAL LNVE~77GATTON OF THE- C O ~ C i ~ I O N BE~~N S~~ANTIA.~G~,AN T H E k~MYGDALA ~%~ A T
8. BAI%A~.~I* a~ of
8H
PAY , P.O. B o x 7 8 , O-nfvemfty College, Cardff~, CFI !XL (U.tL)
(R November 27th, 1979) (Re~d n January 22nd, 1980) (Accep~d J a n ~ 24~h, 1980)
SUMMARY
The present study concerns an electrophysiologieat investigation of the reciprocal neuronal connections between the SN ,and the amygdata in the rat, Using the eollisiono~est technique the e~istenee of a slowly conducting nigro~my~ata ~ been confirmed° tn addition a pathway originating in the c e n t ~ nueteu~ of the amygdala ~ d terminating in th~ SN h ~ also been demonstrated,
Recent evidence h~¢5 s ted that the substantia nigra {SN) may be involved in nociceptive mech raisins [ 1,7,I2,13]° One possibility is that the SN may modify a e t i ~ t y ~ t h i n the limbic system thus influencing the affec~ive c o m p o n e n t of the response to a noxious st,ira ~ius, existence of a leaved from both (HBP} studies i t h the recipIocal ......... )retie md a electro° ese two nude1 a ~ ~ exist we t h e r e f o ~ d e e l d e d , o Ftudy these p r o p o ~ d sod Wisgsr ~spo~lses 7! Blue ~£ 42 m
from
~
[9].
4°5--8°0 ~
accozd~g to @e a t ~ of
Lug
es
(Ehod~ M ~ ~ e n ~ S ~ 1 0 0 } were i~pLan~d k ~ e i cenlTA n of ~he a m y , S . ~ on b ~ ] o C c ~ e x ~ a f i o n , the f o l I o \ ~ co-o~na~e~ h ~ e been fo-~d ~ be the m ~ :pp~p~mte: A: 4A ram; L: 3.7 ram; V: 7.0 ~r,~,. S ~ . v a ~ o : of We amygdala was effec~e.d w w 4 ~ u a ~ wave ~ 0.05--0.2 ~ in dura~on with a ~'~m in~r~kW of Od5 m A ( t ~ o ~ i n ~ ~ app~om O.I ~ ) o The effe~ of ~ n y ~ s ~ u t a t ~ o a was on @ontaneoa~y active ~eu~o~es ~ecorded in the SN, The c o n ~ n 4 e $ ; tecbr~que was ed £n ever~ study to df~gngu~h between or~hc~i~omic and antid~omma~y ac'~vated neamne~ m G~e SNo A ~ h o ~ ea~e~ repor~ h~'e reh'edupon @~ constant ]stoney of the e v o k ~ ~e~ponse as a caledon for an~/d~om~ n, f~e ~e~ulf~ ~ o w n in Fig. l b conf~m a zecent suggest/on that ~¢oked z e s p o ~ in an~dmmic pathways a~e offen of variable ~atency [10]~ ~t i~n o w generallya~cepted that the collision-testtechnique i~ the most stringenttech~que enabling anfid~omic ac~4by to be rddab|y demon,%rated [6), A totalof 51 non,ones have been ~ecorded within the SNo Fo~y (78%) of these neuron~ did not ~espond to a~nygdah~~rau~t~on. Of ~he ~ema[ning 11 neu~na~, 8 (18%) were o~thod~n/cally activated and 8 (6%) were elea~lyant~dzomiea~y act/rated.F~a~e ~ ~/]ust~tes~ecordin~ made fxom an antidmm~caUy activated SN neurone. Tm~e la show~ the evidence of collision (ablate of an evoked r~ponse foHow~ng amygd~/a stirauL~tion) and the co~/~ion time can be obtained from the ]ower ~t of ~ s (Ib). The average latency of the antid~miea~[y conducted _ac~ivltywithln the ni~o~ amygd.~a pathw~y was found to be i0 ~ . A~umi~g a path ]en~h of 3 rnm~ [4,9] the average conduction veJocity~sthus 0.S m s ~ ~. Activity withi:~the au%y~da~o-ni~i pathway can [end to both exciSe/on and inhabit/onof m ~ neurones. The ea~H~st component of the ~e~po ~se was usuallyan evoked action potent(s) having a mean la~ney of 14 reset. ~n 4 neu~ones (a][found in the zona retieu~ata)~ eaHy componemt was the only type of activityre~o~d~ in response to amygdgla sti.m~l~on. H o w ° eveL four neurones located w~th~ the zona eomp~ta ai~o e~v/~bitedan inhibitory response.This W~ manffes~ asa ¢ on o spon~eous f~mg and lastedup to ~00 mSeCo The ~e~o~ing ~/]u~ in Fig. 2a ~hows an ex~.p]e of a va~dab~elatency orthod~omiea~y conducted re~ponse. Fibre 2b depicts the inh~ition of spontaneous ae~/vity fo~/ow~ug amygdab stimu]afiono Fo~owh~g the iontopho~et/c egmfion of PSB from the re~ord~g elee-ttode it has been possible to dete_~hle ~he location of alln~uron~ studied° In this study the ni&~o-an~y~daJaou~pu~ neumon~s have been found v~thin the late~ asp~t ~of the ~:ona Meibach [11] noted %hat c, amygd~/ao in addition th~ i8o~oo
267 a
d
b
, A 16~0!
"I s
Hg. 1. ~ p ~ of a zo~ r e ~ c u ~ neurone projectingto the central nuc~eu~ of amygd~. Tvace~ a and b ~ e ~ ob~ned frora the ~ e neurone. (a) Five con~ecu~ve trace~ of ~ ~ f~om a ~ona r e ~ c u ~ neurone ~ re~on~e to amygda~a ~timu]at~on {~imulu$ art~a~ indica~d by ~he arrow). ~n ~he ~econd ~ace a ~pon~neou~ action po~n~al (ind~ca~d by the ~ k ) c ~ l y precede~ ~timulation, resu]~ng in collision. ~ charae'~e~d by ~ ab~en~ of an evoked action polariS. Calibrationbar = 2 ~c, (b) ~ the u~er ~ee, a ~mnWneou~ action po~n~a~ ~gger~ the ~tirnulu~ after ~ ~ ~ of 7 r~ec.~ evoking an a~ion po~enti~ ~ each i r ~ c e . No~ ~he vaMable |a~ncy of ~ evoked r e ~ ~ . ~ the lower ~race,the interval between the ~pont~ne.ou~ e~:~on ~ t i ~ ~ d s ~ m ~ ~ dec~ec~edby i ~ec. ~ulthag in coOl,ion. Each trace co~ of ~ ~wee~. C ~ b ~ o n bar - 2 ~ c . (e) ~ a g ~ m of ~t~n~ula~ion ~i~ b ~ d on the ~n~g and ~ p p e l rat br~n atla~ [9]. ac, nuc~eu~ a~nygdaloideu~ centrali$; cai. in,real ~ u ~ ° (d) ~ t i o n of the z~na reticu~a neurone recorded in the sub, tanaka nigra (82q.). a m y g d a ~ neurones are a ~ o ]oca~
b
d
269
Efferent c~nnec~ior~ o~ the ~
~ . ~ 175 (1979) i 9 ~
4
, B ~ . and A ~ t ~ ~ G.K°, The p ~ Itemization of nigral afferen~ in the by a r e ~ ~raeSng ~_ehnique, ~ n ~ . , 117 (1976) 422--435° j~ , ., e inaervat2on of R e ~ forebrain (IV).
5
, ~,,
ra~ ~
6
J;H. ~
8 9 10 11 12 13 14 15
R,Y., Subs~nl2a nigra d o p ~ i n e neurone~: the n e ~ t r i a t u m ~Jad ail~or~e~:, Neurosci. L e t t . 7
, J.D., ~ r m i n a f i o n of anfi4romic e~:eitation by ?:he cot~sionof inVerpret~on, Brain Res., 112 (1976) 283--298. M., Nico~u, N.M., ~fliock, : . F , WrighL A.K. and Arbuthnott, G.W., Feedb~mk l ~ p or output pathway in ~aC~onigral fibres? NaCre (Lond.), 265 (!977) 363--365. Jurna, I., Heinz, G., Btinn, G. and Nell, T., The effect of substantia rAgra stimulation and morphine on ~-motoneurones and the taft flick response, Europ. J. PharraacoL, 51 ( 1978) 239--250. KSnig, J.F°R. and Klippet, R.A., The rat brain, Wiliiams& Wflkin~, Baitiraore, 19~3. Mayer, M . L , Variable latency an~idro~c re~po~e~ of preoptic-an~erior h:~pothalamic neumne~ in ~he tail, J. Phy~ioi (Load.), 289 (1979) 80P. Meibach, R . C , Evidence for a duat dopaminergic ~ b ~ a n t i a ~igro-arnygdaia pro~ec° tion in ~:he caL Ana~. Rec., I93(3)(1979) ~21. Price, H.T.C. and Fibiger~ H.C., Ascending catecholamine ~s~eras and morphine anaigeuia~ Brain Re~., 99 (1975) 189-193. Sandberg, D.Eo and Seg~l, M., Pharraacoiogical anaiy~i~ of anslge~a and ~e!f stimuta o tion elicited by eiectrical ~¢imulation of catecho~ami~e nuclei it: the ra~ brain. Brain Reu., 152 (1978) 529--542. Simon, H,, Le Mout, M. and Ca~a~, A., Efferent~ and afferent~ of the ventral ~egraenta] A~lO region ~ d i e d afl~r ioca~ ion i~H]tencine and i~)r~eradish ~ r o ~ d a ~ Brain Reu., 178 (t978) 17~40o Ur~gc~dt~ U., S~creol;a~:ic ~nappir~ of. ~he monoamine pathways in the ra~ brain~ Acta phy~ioL ~cand. (Suppi.) ~67 (1971) 1.
¢~: 7
y, H;