I()l lttNAl- ()t. NEUII()trlyst()L()(iy
Vtrl.7.1.
No.3,
Septc'nrbcr
1995. I'rinred
RAPID PUBLICATION
in ll.S.A
Existencein the NucleusIncertusof the Cat of Horizontal-EveMovement-RelatedNeuronsProjectingto the CerebellarFlocculus
GUY CHERON, SVEN SAUSSEZ,NICO GERRITS,AND EMILE GODAUX
Laborcttorl of Neurosciences, [Jniversity of Mons-Hainaut, Mons-Hcrinctut, Belgiutl;
Era.sntus University of Rotterdam, Rotterdam, The Netherlands
S U M M A R YA N D C O N C L U S I O N S
1. Propertiesof nucleus incertus(NIC) neuronsprojecting to
the cerebellarflocculus were studiedin aler-tcats by using chronic
unit and eye movement recording and antidrornicactivation.projection of these neurons onto the flocculus was verified with retrograde transport of horseradish peroxidase after injections in the
floccnlus.
2. Bipolar stirnulationelectrodeswere implantedinto the ,,rniddle" zone of each flocculus becausethis zone is known to be
involved in tlre contlol of horizontal eye movements. The dorsomedial aspectof the pontine tegmentumwas explor-edwith microelectrodesduring stirlulation of both flocculi. The rnajority of
nellrons antidlomically activatedfrom the flocculuswere for-rndin
thc caudal part of the NIC.
J. Of the 69 neurons activated frorn the flocculus. 44 were
classifiedas burst-tonic (BT) neurons;34 dischar-ged
in relation
with horizonlal movementsof the eye, l0 in relationwith vertical
movements.Of the l4 rernainingneurons,6 were not related to
eye nrovementsand 8 were classifiedas burst neurons.The BT
neuronsof the NIC displayeda great sensitivityto both horizontal
eye position and horizontal eye velocity.
4. This study demonstratesthe presenceof a new gr.oupof
horizontal eye ntovelnentrelatedBT neuronssituatedin the NIC.
The fact that they project to the horizontal floccular zone emphasizesthe importanceof the functionalspecialization
of the dilferent
Purkinic cell zones.
Ii.vTRODUCTION
Although the flocculus has been extensively stucliedin
different species(Graf et al. 1988;Ito et al. 1977;Noda and
S u z u k i 1 9 7 9 ;W a e s p ee t a l . l g S l ) , i t s m o d e o f i n f o r r n a t i o n
processingrentainsunknown. In contrastwith this unsatisfying observation, the neuroûnatomicorganizationof the
flocculus is well known (Gerrits and Voogd 1982; Gerrits
e t a l . 1 9 8 4 ;S a r oe r a l . l 9 8 3 a , b ;T a n e t a l . 1 9 9 5) a n d o f ï e r sa
great opportunityto undertakean electrophysiological
inputoutput approachtoward the different floccular Purkinje cell
zones.
In the flocculus, three longitudinal Purkinje cell zones
have been describedthat respond selectivelyto large-field
visual pattern rnovernent.Thus Purkinje cells in a centrally
located zone control horizontal eye movements,whereas
those in the flanking zones contl.olvertical eye movements
( Sato and Kawasaki 1990). The centralpositionof the "horizontal" zone facilitares its electrophysiologicallocalization. Stirnulation of tl.riszone was recently performeclto
enabieantidromic identificationof its r.nossy
fiber inputswith
a n o r i g i r . irn t h e m e d i a l v e s t i b u l a rn u c l e u s( M V N ) ( C h e r o n
antl Department ctf 7,n61,,11111y,.
e t a l . 1 9 9 5 ) a n d t h e n u c l e u sp r e p o s i r u sh y p o g l o s s i( N p H )
(Escuderoet al. 1995). Although these two nuclei ar.etwo
important soLlrcesof flocculal mossy fibers (Epema et al.
1990; Tan and Gen'its 1992), several studieshave shown
that the pontine reticular fonnation (PRF), including the
raphe nuclei, provides another mossy fiber input (Alley
1 9 7 7 ;S a t oe t a l . 1 9 8 3 b ) .
The first electrophysiologicalanalysis of these floccular
projections fl'om the PRF, performed in the anesthetizedcat
( Nakaoet al. I 980 ), showedthat electricalstimulationof the
ipsilateralflocculuselicited antidron.ric
activationof neurons
locatedin and around the medial longitudinalbunclle(mlb),
i n t h e n u c l e u sr a p h e p o n t i s ( N R a P ) , a n d i n t h e n u c l e u s
reticularistegmentipontis.Furthermoreit was dernonstratecl
that thesePRF neuronsplovide the flocculr-rs
with eye-movem e n l - r e l a t e di n f o r r n a t i o n .
The exploredbrain sternregion containsa variety of neurons, locatedin and around the mlb and the adjacentperiaqueductalgray. In the latter, a prominent cluster of neurons
is presentas the nlrcleusincertus( NIC ) ( Papez 1929) . Until
now, this nucleus has only been implicated is ascending
connectionsto the medial preoptic area (Vertes 1988) and
the interpeduncularnucleus (Hemmendinger and Moore
1 9 8 4 ;S h i b a t ae t a l . 1 9 8 6 ) .
In the preser.rtstudy we describethe propertiesof horizontal-eye-movetnent-related
neurons in the NIC and the
adjacentdorsomedialPRF with a projectionto the flocculus
in the alert cat.
MEl'HODS
Four adult cats wel'e prepared for chronic recording of neuronal
activity in the brain stetnand the cerebellumand for eye movement
recording(rnagneticscarchcoil technique).Undergeneralanesthesia and asepticconditions,scleralsearcl-r
coils wer-eirnplantedsubconiunctivally on both eyes, bipolar silver stimulation electrodes
were itnplantedintl'acraniallyon each sixth nerve at its exit ft-om
the brain stetr, and three bolts were cernentedto the skull to intntobilize the head during the cxper-in'rental
sessions.Three holes, a
centralone and two lateralones, were rnadein the skull. The dura
mater was removed and a dental cement chanrberwas constructed
aroundthe holes.Bipolar tungstenrricroelectrodeswere in-rplanted
i n t h e m i d d l e z o n c o f e a c h f l o c c u l u s( F i g . l A ) . F u r t h e rc l e t a i l s
of this chronic pleparation have been describedby Cheron et al.
( r 9 9 -) 5.
Eight days afÏer surgely, each animal was trained to acceptrestlaining conditionswithout stress.Special care was taken to pr-event any discomfbrt in the anintals. Antidr.ornicfield potentials
evokedby stintulationof the abducensnerve were usedto rnap the
0 0 2 2 - f 0 7 1 / 9 5$ 3 . 0 0 C o p y l i g h t O 1 9 9 5 T h c A r r e r i c a n p h y s i o l o _ q i c aSl o c i e t y
I367
GODAUX
G. CHERON,S. SAUSSEZ'N. GERRITS,AND E.
neut'onsfot
focused our attention only on antidromically activated
fol which
and
constant
short and
which the latency was reiatively
'ihe
PRF
identified
each
of
activity
succesful'
coilision tests were
ln
movements
eye
n.uron *at recorded 1 ) during spontaneous
of the
stimulation
sinusoidal
horizo-ntai
during
ihe light and 2)
(amplitudes of
u..tiuîtoo.utor iefl"x (VoR) in complete darkness
VOR slow
the
of
Idêntification
1
Hz)'
0.
at
deg
f ô, ZO,:0, or'40
developed
ohaseswas perfortned automatically, using arnalgorithm
(R')-of
sensitivitv
velocitv
saccâdic
The
[; B^l;;; Jt-.i. iisszl.
(1989)'
al
et
Berthoz
the neuronswas obtarnedby the method of
fixation (Ki)'
The sensitivityto eye position during intersaccadic
(K') and to
VOR
the
and the sensitivitiesto eye position during
a method
by
ob,trined
wele
the"VOn
tn"l
"v. u"fo.ity during
(codou* a'd cl.reronlee3)' Recording and
;Ë;;;;;1";;Û
from histological
'lesion
stimulation sites were verified and reconstt'ttcted
electrolytic
sections according to micrometer readirrgsand
which horseradish
marks. Two addùonal cats were available in
into the caudal
o..o*iau." (0.4 pl, 3O7oin saline) was injected
the stin.rulation
where
position
same
the
in
no."Ii""
;;;;';f ;;
(Fig' I )'
il..,rod., were placed in the other animals
;'i"r;:il-:--t
ii;;,Q5 mm
RESULTS
#r,t,.f-l
.' .:,
O.5mm".,.1''.
actiA total of 69 neurons were analyzecl,anticlromically
and
contralateral
the
(38
fiom
flocculus
either
vated from
the
in
situated
tô i.o- the ipsilateral side; l2 rleuronswere
the
in
located
rniatin.). The majority (57 neurons) Y9I:
c
o
l
l
e
c
tion
i
s
a
N
I
C
t
h
e
c
a
t
,
t
h
e
Niô fnig z, c aia D\.In
oval-to-fusiform
an
with
neurons
medium-sized
tf rtnott"to
periaq"i9"i^
rfr"p"ief g 2, E andF). They are located in the
stereotactlc
the
between
tat gtay iirectly dorsal to the rnlb
1
9
2
9
)
'
.
C
a
u
d
a
l l y t' h e N I C
(
P
a
p
e
z
pf"i"t'p S.Sana P 1.5
genu'
fàcial
capping
nucleus
supragenual
abuts on the
-the
reThe
but its lateral ând-rostral borders are indistinct'
the
to
close
located
maining PRF neurons(12 units) lere
nucleusof the
midlinJin the NRaP and the central superior
D
)
'
a
n
d
C
(
F
i
g
.
2
,
(
C
S
)
raphe
^".'Fiil;t'shiws.the
antidromicactivationof a NIC neuthe laok of
.on i.o- the contralateral flocculus (/efr) and
flocculus
ipsilateral
the
from
unit
activation of the same
collstalll'
was
neuron
this
of
latency
response
(right). The
variation in
The
n""ons'
oth"t
the
all
for
case
the
ïut
àt
expected fbr
the peak latency was <30 /r's, .11 would be
testcollision
the
illustrates
2B
antiâromicactivation.Figure
responses'
antidromic
and
spikes
ing between spontaneous
flocThe 38 NIC neurons actiïatecl fiom the contralateral
-f 0'41
1'32
of
latency
culus had an antidromic response
activatedfrom the ipsilatiS;l ;t. For the l9 NIC n"ut'o"t
1'16 -t 0'34 ms'
was
latency
antidromic
àil ria", the
flocculus'
Of the 69 PRF neurons activated tiorn either
p t c . 1 . A : t r a n s v e r s es e c t i o ns h o w i n g t h e t r a c k o f t h e s t i m u l a t i o ne l e c B: diagrarn of the^
trJe, which ends in the middle zone oT the flocculus
t h e e x t e n to f
n"..uf t'complex (atter Genits and Voogd 1982)illustrating
(H9924 and C276; hatchthe horsera<lishperoxidase (HRP) injection sites
(
here represented
ing ) anOthe clear overlap with the horizontal zone black ) '
cap of the inferior
as the climbing fiber zone originating in the cau<laldorsal
of the sections
olive (Gerrits'and Voogtl t9iZl' Hlrizc'ntal line: position
injection site of
fl.o'-r A and c. c: transverse iection through the HRP
H 9 9 2 4 a t i t s l a r g e s td i a l r e t e r .
was used as r
location and extent of the abclucensnucleus' which
in the PRF
a,ctivity
neuronal
The
recolcling'
further
landrnark for
-2 nA! impedance) durw:rs explored with glass rniclo-pipettes t t
both flocculi' We
i.rg ùipif ut stimulaiion of the^ middle zone of
42neuronsmodulatedtheirfiringrateduringSpontaneous
two categorles'
horizontalsaccadesand could be divided into
ratejn a burstfiring
their
changed
neurons
ôn" g.orp of 34
eight neurons
of
toniJfashion (BT neurons)' Another group
and not
saccades
dr'rring
modulatecltheir burst activity only
conNIC
The
(B
neurons)'
during subsequentgazeholding
in tl.re
located
were
neurons
BT
3
neurons;
tained 31 BT
The BT neurotis
NRap ana the CS (Fig.2, C and D' O)'
I or type II' detype
as
of the NIC were furthËr classifiecl
during horiincieased
rate
firing
p."àing on whether their
side,
recording
the
from
i*uy
o.
toward
iontat Ëeadrorarion
in
located
were
respectively.The majority 91'ttr1.Éneurons
the
On
À)'
D'
and
C
(Fig'
2'
the CS, the NRaP, oi the'mlb
EYE-MOVEMENT-RELATEDNEURONS IN NUCLEUS INCERTUS
Stimulation
of the left
flocculus
+
A
ï
B
Stimulation
of the right
Ilocculus
antidromicactivation
+
collisiontest
W
0 . 5m V
i:*--X3&*:
E f:''s
C
*a.:.rù
|
:4"':il,
't
*,'r.
.,' ,&.,1"
. *
a:._,
ç.i!'r
i ", ,,, l.
' **;1u.
'ljl
-- ,':1ç*,1,: l',
F
F I G . 2 . A : s u p e r p o s i t i o no f 3 r e c o r . c l i ntgr a c c s
showing the antidromic activzttionof a burst-tonic
( B T ) n e u r o no f t h e n u c l e u si n c e r t u s( N I C ) f b l l o w ing stimulation of the contralateral flocculus ancl
t h e l a c k o f a c t i v a t i o no f l h e s a m e u n i t f i o m t h e
i p s i l a t e r a lf l o c c u l u s .B : c o l l i s i o n t e s t i n g .S r a r :a b s e n c eo f t h e a n t i d r o m i cs p i k e w h e n i t c o l l i d e dw i t h
t h e s p o n t ù n e o u ss p i k e . C a n d D : l o c a l i z a t i o no f
t h e f l o c c u l a rp r o j e c t i n gn e u r o n si n t h e p o n t i n e r e ticular lbrm:rtion ( PRF ) ( see nEsur-'r's
for explanat i o n o f s y l n b t ' l s) . E : c l u s l c r o l f e t r . o g r t t l c l iyb e l e r l
s m a l l n e u r o n si n t h e c o n t r a l a t e r aN
l I C ( P . 1 ,N i s s l
c o u n t e r s t a i n ) .F : r e t r o g r a d e l yl a b e l e d s m a l l o v a l
and fusiforn.r nellrons in the contralateral NIC
(P3). G: retrogradely labeled mediunt-sized
polygonal neuron at the dorsontedialcorner of the
m e d i a l l o n g i t u d i n a lb u n d l e ( r n l b ) ( P 3 . 5 ) . B a r i n
E - G : 2 5 p m . C S , c e n t r a l s u p e r i o rn u c l e u so f r . a p h e ; N R a P , n u c l e u sr a p h e p o n t i s ; C E R , c e r e b e l lum: V4, fourth ventricle.
?e
{Ëcp'""'
D
/
/ t\
l
tÊ
o
a
I
I
.
a
mlb
I
..r.. . I
7-,Ç\1 ,,3
.u{
$r
border between the NIC and the mlb, l0 other BT neurons
were fourrd that did not respondto horizontalhead rotation
but modulatedtheir activity exclusivelyduring spontaneous
vertical saccades( Fig. 2, C andD, C ) . Retrograclely
labeled
neuronsin this location were slightly bigger than the labelecl
N I C n e u r o n s( F i g . 2 G ) . T h e l 7 r e m a i n i n gn e u r o n sw e r e n o t
r e l a t e dt o e y e m o v e m e n t s( F i g . 2 , C a n d D , I ) .
All 34 horizontal-eye-movement-related
BT neurons(17
activated frotn the contt'alateraland 14 from the ipsilateral
flocculus.and 3 ner,rrons
locatedin the rniclline)rcsponcled
to head rotation (27 as type I, zl as type II). Figure 3 illustrates the spiking behavior of a representativeBT neuron
of the NIC activatedantidromically from the contralateral
flocculus.Befbre and during rapid eye movements,this ner_rron pausedwhen the eyes moved toward the recordingsidc
and burst wl.renthe eyes moved in the opposite direction
( F i g . 3 , A a n d B ) . D u r i n g i n t e r s a c c a d ifci x a t i o n ,t h e t o n i c
dischargerate of this neuron increasedwith more eccenh-ic
G. CHERON,S. SAUSSEZ,N. GERRTIS,AND E. GODAUX
C
BO
o
o
o
a
:
OU
a
a
t
c
q)
(u 40
'=
2î
R
^
-l
10"
0
I
-5
+10 +5
0
horizontal
eyeposition(deg)
-lI 0"
I
1
I
J r, n" o
L
D
80
o.
o
0)
a
a
a
o
o
a
a
a
40
(g
'
a
'a 60
I
a
a
a
a
l ( n
a
:E
l o
a
o
a
a
l v,
a
ln
a
a
-
t
araoaa
a
+
5
0
5
vedicaleye position(deg)
160
5s
F
IZ+U
itzo
R
I
x {nn
o-'--
Iuo"9o B o
I
Eoo
I
oo
,3
-20
L
R
II
-15 -25
+25 +15 +5 0-5
horizontaleye velocity(deg.s-1;
I
|'0"
I
I
90
F
oU)
o - ^
x t u
'Â
L
f\)
o
o
L C U
l a
:=
o Z o
..t/t'
l o
l a
5s
JU
-5
+5
+10
0
horizontaleye posilion(deg)
rtc.3.
A a n c lB : b e h a v i o ro f z rr e p r e s e n t a t i v B
e T n e u r o no f t h e N I C d u r i n g s p o n t a n e o l l e
s y e m o v e m e n t s( A ) a n d d u l i n g
t h e h o r i z o r . r t a vl e s t i b u l o o c u l a rr e f l e x ( V O R ) ( B ) . e v , v e l t i c a l e y e p o s i t i o n ; e h , h o r i z o n t a le y e p o s i t i o n ; f . r . . f i r ' i r r gl r t e : h .
h e a d p o s i t i o n . N o t e t h a t i n t h i s c a s et h e p h a s el e a d o f t h e f i r i n g r a t e m o d u l a t i o ni s l 8 ' w i t h l e s p c c tt o e y e p o s i t i o n .C : s c a t t e r
p l o t o f m e a n i n s t a n t a n e o u st r i n g r a t e o f t h e s a r n e B T n e u r o n o v c r h o r i z o n t a le y e p o s i t i o n d u r i n g i n t e r s a c c a d i cf i x a t i o n
p e l i o d s . T h e s l o p e ( K r ) o f t h c l i n e a l r e g l e s s i o nb e t r . v e etnh e h o r i z o n t a le y e p o s i t i o na n d t h e f i r i n g r a t s ( r - - 0 . 8 - 5) c o r l c s p o n d s
t o t h e s e n s i t i v i t y t o h o r i z o n t a l e y e p o s i t i o n ( K , : 6 . 6 5 s p i k e s .' 'sd " g ' ) . D : s c a t t e r p l o t o f n t e a n i n s t a n t a 8 e o u s f i r i n g r a t e
o f t h e n e u r o n o v e r v e r t i c a le y e p o s i t i o n .N o t e t h e a b s e n c eo f a n y s i g n i f i c a n rt e l a t i o n .E : a n a l y s i so f t h e e y e v e l o c i t y s e n s i t i v i t y
( R , ) o f t h i s B T n e u r o n . T h e s l o p e o f t h e s e d i f f e r e n t l a t e - v e l o c i t yr e s r e s s i o n s( R , ) v a r i e d w i t h e y c p o s i t i o n f r o m l . 5 l t o
, 1 . 0 2 s p i k e s ' s - ' ' d c g' ' s e c ' . F o r e a c h o f t h e s e l i n e s , t h e f i r i n g r a t e a t 0 v e ) o c r t y , F ( 0 ) , w a s c a l c bu yl ai nt et ec rl p o l a t i o n .
I ' : r e l a t i o n s h i p b e t w e e n F ( 0 ) a n d h o r i z o n t a l e y e p o s i t i o n . T h e d a t a p o i n t s a r e w e l l I i t t e d b y a l i n c a r r e g r e s s i o nl i n e .
T h e s l o p e ( ( , ) o f t h i s l i n e c o r r e s p o n d st o t h e s e n s i t i v i t yo f t h i s n e u r o n t o e y e p o s i t i o n d r , r r i n gt h e V O R ( K , = . 1 . 5 2
sprKes's .deÊ ).
EYE.MOVEMENT-RELATEDNEURONS IN NUCLEUS INCERTUS
(contralateral side) gaze position (Fig. 3C), but it did not
change as a function of vertical eye position (Fig. 3D).
During sinusoidal vestibular stimulation, the firing rate of
this BT neuron showed a type I sinusoidal modulation
interrupted by burstlike increasesand by pausescorresponding to the quick phases, directed away or toward the recording side, respectively(Fig. 3B). For BT neuronsin the
NIC, the value of K1@ :24) ranged from 1.70 to l'7.40
spikes.s-r.deg-r with a mean -f SD of 8.68 + 4.55
s p i k e s . s - ' . d e g ' . T h e v a l u eo f R . ( n : 1 l ) r a n g e df r o m
2 . 3 8 t o 1 2 . 4 3s p i k e s . s - r . d e g - t . s I w i t h a m e a no f 6 3 6
t - 3 . 4 9 s p i k e s ' s r . d e g - t . s - ' . T h e v a l u eo f K , ( n : 2 4 )
r a n g e df r o m 2 . 6 3 t o 1 6 . 6s p i k e s . s r . d e g - r w i t h a m e a n o f
' 7 . 6 3- r
3.57 spikes.s-I.deg-t. The R, during the slow
phases of the BT neurons (n : 24) ranged from 0.94 to
1 7 . 0 3s p i k e s . s - ' . d e g . I ' s - r w i t h a m e a n o f 3 . 1 5 - f 1 . 9 8
s p i k e s s' - ' . d e g - ' . s - ' .
131|
functional role related to eye movements.Nevertheless,their
high sensitivity for both eye position and eye velocity might
indicate that they provide an efference copy of eye movement commandsto the flocculus.The anatomicand physiological characteristics of the NIC neurons show a strong
correspondencewith the NPH floccular projecting neurons
(Escuderoet al. 1995), i.e., the superficiallocalization,the
specific projection to the horizontal ffoccular zone and the
spiking behavior. The convergence onto a single floccular
zone of very similar eye-movement-relatedsignals from different brain stem nuclei could representan important element
in the signal processingof the flocculus.
Furthermore, it remains to be determined whether single
NIC axons collateralize to both cerebellum and basal forebrain. Apart from this question, it is important to determine
which type of the efferent NIC neurons contains peptides
and which of the peptidergic neurons are involved in oculomotor and cerebellarfunction.
DISCUSSION
We acknowledge M.-P. Dufief for excellent technical assistanceduring
In the explored region of the PRF, the rnajority of BT experiments and histology. We thank C. Buson for secretarialassistance,
neurons that project to the horizontal zone of either the ipsi- M. Baligniez and B. Foucart for taking care of the mechanicaland electronic
lateral or contralateral flocculus were located in the caudal equipment, and E. Dalm for photographic assistance.
This research was supported by the Fonds National de la Recherche
aspect of the NiC. Most of them (877o) respondedto horiS c i e n t i fqi u e ( B e l g i u m ) .
zontal head rotation in a type I fashion. These neurons proAddress for reprint requests:G. Cheron, Laboratory of Neurosciences,
vide the flocculus with a signal related to both the velocity University of Mons-Hainaut, Place du Parc 20*7000, Mons-Hainaut, Beland the position of the eye. The BT neurons in the NIC g i u m .
that project to the flocculus showed a spiking behavior very
Received 3 April 1995; acceptedin final form 5 June 1995.
similar to the BT neuronsobservedin the NPH (Escudero
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