Neuroseiencc Lelter~', 136 (1992) 47 50
47
llsevier Scientific Publishers Ireland Ltd. NSL 08402
Antidromic and synaptic activation of Deiters' neurons induced by stimulation of red nucleus in the cat V.H. S a r k i s i a n a n d V.V. F a n a r d j i a n Lahoralory (?l Physiolo~v o[ ('entral Nervous System, Orbeli lnslitute of Physioh~gy, Academy qf Scienees ol Armenia. )~'revan {Armenia)
(Received 21 August 1991: Revised version received 11 November 1991: Accepted 18 November 1991) Key word.s: Lateral vestibular nucleus of Deiters: Red nucleus: Vestibulospinal neuron; Cat
Antidromic and orthodromic action potentials of neurons located in the lateral vestibular nucleus of Deiters' evoked by stimulation of red nucleus were studied in anaesthetized cats. Vestibulospinal neurons were identified by stimulation of the lateral vestibulospinal tract. The "second-order' vestibular neurons were revealed by mean of stimulation of the ipsilateral Vlllth nerve. Stimulation of the red nucleus is shown to lead mainly to antidromic, as well as mono-, oligo- and polysynaptic activation of Deiters' neurons. Not any inhibitory reaction was obser,,ed in vestibular neurons m response to stimulation of the red nucleus. Ascending axon collaterals of the vestibulospinal neurons to this brainstem structure were revealed. The peculiarities and functional significance of the effects mentioned are discussed.
The lateral vestibular nucleus (LVN) is shown to be related to the large n u m b e r of brainstem structures and plays a significant role in the modification o f muscle tone, maintenance o f equilibrium, orientation in threedimensional space and in general the control o f movement [8, 20.21]. On the other hand, the red nucleus (RN) is also k n o w n to participate largely in the regulation o f m o v e m e n t [11, 17, 18]. Both LVN and R N are demonstrated to be somatotopically organized [7, 12, 15, 16] and by means o f their descending lateral vestibulospinal (VS) and rubrospinal (RS) tracts affect extensor and flexor m o t o n e u r o n s , respectively [11, 14, 19]. A n o t h e r important property o f the organization of these descending systems is the collateral axonal branching o f their neuronal elements at m a n y spinal levels. It has been revealed that 50% of VS neurons give collaterals to cervical and lumbar segments o f the spinal cord [1] and 5% o f rubrospinal neurons" collaterals reach the mentioned spinal levels [17]. Recent experiments with horseradish peroxidase ( H R P ) injection to LVN revealed direct reciprocal proiections from R N to all parts o f Deiters' nucleus [13]. In order to test the possible interactions between LVN and R N and taking into account the prominent role o f each o f lhese structures in coordinating complex m o t o r
('orre.~7~omh'nce:V.H. Sarkisian, Orbeli Institute of Physiology, Academy of Sciences of Armenia. 22 Orbeli Brothers Sir.. 375028, Yerevan, Armenia.
reactions, the present experiments for the study o f rubrovestibular relations were performed. Experiments were carried out on 7 cats (2.5 3.5 kg b o d y weight) anesthetized with pentobarbitone (Nembutal, Tallinn, 45-50 mg/kg, i.p.). Bipolar tungsten electrodes with an interpolar distance o f 1.0 m m were used to stimulate the contralateral R N . Electrodes were inserted in R N according to the following stereotaxic coordinates: L 2, H - 3 . 5 and A 3.5 [3]. VS neurons were identified according to their antidromic activation to stimulation o f the lateral VS tract [7, 10]. Stimulation of the ipsilateral vestibular nerve was carried out by a pair of tungsten electrodes placed into the owtl (cathode) and round (anode) windows o f the middle ear. Rectangular electric pulses o f 0.1--0.5 ms duration, 1.0 10.0 V and 0.1 0.15 m A were used for stimulation. Skull bone in the area o f the cerebellar posterior vermis was removed for a dorsal a p p r o a c h to Deiters' nucleus. The activity o f LVN neurons were recorded by glass micropipettes filled with 2 M potassium chloride. Their resistance ranged from 2 to 10 M,Q. Stimulating and recording electrode tip locations were verified histologically [3]. Intracellular activity o f 74 LVN neurons responding to the stimulation o f RN was recorded. Single stimulation o f R N evoked antidromic action potentials (APs) in 50 LVN cells (Fig. IA>BI,E~). The latencies of lhe antidromic potentials ranged from 0.2 to 0.7 ms (mean 0.38 _+ 0.1 ms, S.D., it = 50: Fig. IG). 17 out of 50 LVN cells were identified as VS neurons (Fig. IA~,B2,E2: G , columns with circles). They were characterized by a fixed
48
B 20mv ii
I
m t
LL_
2omv
7ram
"";-
~r-
ms"
I
10-
III
il I i i
2ms
n
2ms
,luliHi J
2ms
ms
G
_
n
.
6--
o o o o o o
4--
o o
oo oo
o o oo oo oo oo
o o • o
oo o l
• o
I
0
0.!
0.2
0.3
0.4
0.5
I
I
0.6
0.7
ms
0
0.8
l
I
I
!.0
1.2
1.4
ms
Fig, 1. Antidromic and synaptic activation of Deiters" neurons evoked by stimulation of RN. As, B~, El: antidromic APs of three Deiters' neurons evoked by over-threshold (As) and just-threshold (B~, E3) stimulation of RN. A~, Bz, E2: antidromic APs of the same cells evoked by over-threshold stimulation of the lateral VS tract. A2,3, A6,7: effects of paired shocks with shortened interval between stimuli applied on lateral VS tract and RN, respectively. A4, As: APs at frequencies of 850 (A4)and 600 (As) per second. E3: orthodromic AP of the cell evoked by stimulation of the VIIIth nerve. C~, D. F~: orthodromic APs of three Deiters' neurons evoked by stimulation of RN. F2: EPSP evoked by stimulation of VIIIth nerve. C2: antidromic AP evoked by stimulation of the lateral VS tract. Lower records in A~, B-E are extracellular controls. G, H: latency distribution histograms of the antidromic (G) and orthodromic (H) APs of Deiters' neurons to stimulation of RN. Columns with circles indicate the identifiedVS neurons; abscissa: time in milliseconds;ordinate: number of cells (n). Potentials are recorded with a DC amplifier, 5-10 superimposed sweepsi frequency 5/s.
latency at just-threshold (Fig. 1B~,E 0 a n d supra-threshold (Fig. 1As) intensities of stimulation, W h e n stimulating with a pair o f shocks at short intervals they had a short refractory period (Fig. 1A2.3, A6.7). A n t i d r o m i c APs
could follow the high frequency s t i m u l a t i o n at 600-1000 imp/s (Fig. 1As,A4). The average distance between R N a n d LVN was 12 m m a n d the calculated c o n d u c t a n c e velocity o f the v e s t i b u l o r u b r a l fibers ranged from 17.1 to
49
PyrC •
I
midline
mf ## # #
F1
_VN
Fig. 2. Schematic representation of neuronal relations of Deiters" ILVN) neurons with cerebral cortex pyramidal (Pyr. C), red nucleus IRN), cerebellar Purkinje (PC), fastigial (FN), interposite (IP} and lateral reticular nucleus (LRN) cells. PT, RST and LVST - pyramidal. rubrospinal and lateral vestibulospinal tracts, respectively, m f - .
60 m/s. According to the data of earlier reports [7. 10], the cells from which these fibers originated can be attributed to the 'rapid' type of VS cells. A m o n g the antidromically activated cell population, 7 neurons were orthodromically activated by the stimulation of the ipsilateral vestibular nerve as well. Four of them were activated monosynaptically, thus being attributable to 'second-order' vestibular neurons [2] (Fig. 1E3). Stimulation of RN in 24 Deiters' neurons evoked orthodromic APs (Fig. 1C,, D, F~). They were generated at latencies of 0.7- 1.4 ms (mean 1.0 _+0.21 ms, S.D.; n = 24, Fig. I H). In some Deiters' neurons gradual increase of RN stimulation intensity did not affect the latent period. suggesting their mono- or oligosynaptic origin (Fig. 1C,, D). As far as the EPSPs of Deiters' neurons are concerned, it was impossible to record them separately because of the low threshold at the AR Eight out of 24 orthodromically activated Deiters" neurons were identified as VS cells (Fig. 1C>H: colunms with circles). Three cells of this population were orthodromically activated by ipsilateral VIII nerve stimulation (Fig. IF2), among them one cell was at 'second-order' vestibular
neuron. No inhibitory potentials were observed in LVN neurons in response to RN stimulation. Thus, the results of the present study suggest that similarly to other brainstem structures [8] the RN establishes bidirectional connections with Deiters" nucleus as well (Fig. 2). Polysynaptic excitatory efl'ects o1" RN on Deiters ~ neurons can be elicited via the lateral reticular nucleus (LRN), inferior olive, facial nucleus and caudal trigeminal nucleus [6, 9] (l\~r simplicity, the last thrcc nuclei are not presented in Fig. 2). In this case RN as well as L R N can be functionally considered to be relay s t a t i o n s for c o m m a n d signals from m o t o r cortex to Deiters" nucleus [4. 5] (Fig. 2). Moreover, neurons of Deitcrs" nucleus by means of RN receive inl\)rmation from the cerebellar interpositus nucleus too. thus utilizing one more neuronal pathway through which the cerebellar Purkinje cells af['ecl Deiters" neurons. Antidromic activation of lateral VS neurons by RN stimulation suggests that Deiters neurons in their turn modil}' the activit\ of RN neurons. RN and LVN are known to be inlport'ant centers |\)r control of flexor and extensor muscle actixity [11, 19]. Reciprocal connections between LVN and RN possibly provide the basis t\~r a coordinated aclivit3 of both structures during the development of vestibulospinal and rubrospinal motor events.
1 Abzug, C.. Maeda, M., Peterson, B.W. and Wilson, V..I., ('crxical branching of lumbar vcstibulo-spinal axons, ,I Physiol., 243 (1974) 499 522. 2 Akaike, T.. Comparison of neuronal composition of the xcstibulospinal system bctx~cen cat and rabbit. Brain Res., IS {1973)428 432. 3 Bcrman, A.L., The Brain Stem of the ('at: A (',,.Ioarchitcclonic Atlas with Stcreotaxic Coordinates. Madison, Wisconsin. 1968, 175 pp. 4 Brukmosscr, P., Hepp-Rcymond. M. and Wicscndangcr, M., Cortical influence on single neurons of the lateral rclictllar nuclctls ol the cat. Exp. Neurol,, 26 (1970) 239 252. 5 Brukmosser, P., Hepp-Reymond, M. and Wicscndanger, M., Effects of peripheral, rubral and fastigial stimulation on neurons of the lateral reticular nuclcus of the cat, Exp. Ncurol.. 27 t l971 I 388 398. 6 Ed,sards, S.B.. The ascending and descending projections of the red nucleus in the cat: an experimental study using kill auloradiographic method. Brain Res.. 48{1972)45 6:L 7 Fanardjian, V.V. and Sarkisian, V.H., Spatial organization of the cerebellar cortico~estibular projection in the cat, Ncuroscicncc. 5 (1980) 551 558. 8 Fanardjian, V.V. and Sarkisian, V.H., S_~naptic meclmnisms ol interaction of lateral vcstibulospinal neurt)ns x~ith :,omc brainstcm structures. In O. Pompciano and J.H.J. Allure (lkl:,.), Vcstibuhu Control of Posture and Locomotion. Progrcss in | h a i n Research, Vol. 76. Elsevicl-, Amsterdam, 1988. pp. 45 61). 9 Holstege, G. and Tan, J., Proieclions I'rom thc red nucleus and surrounding area to the brainstem and spimil cord in the cat. An HRP and autoradiographical tracing slud_~, Behax. Brain Res.. 28 (1988) 33 57.
50 10 Ito, M., Hongo, T., Yoshida, M., Okada, K. and Obata, K., Antidromic and trans-synaptic activation of Deiters' neurons induced from the spinal cord, Jpn. J. Physiol., 14 (1964) 638 -658. 11 Massion, J., The mammalian red nucleus, Physiol. Rev., 47 (1967) 383436. 12 Nyberg-Hansen, R. and Brodal, A., Sites and mode of termination of rubrospinal fibers in the cat: an experimental study with silver impregnation methods, J. Anat., 98 (1964) 235 253. 13 Pogosyan, V.I. and Fanardjian, V.V., Afferent connections of the cat lateral vestibular nucleus, Neurofisiologija (Kiev), 20 (1988) 494-503 (in Russian). 14 Pompeiano, O., Functional organization of the cerebellar projections to the spinal cord. In C.A. Fox and R.S. Snider (Eds.), The Cerebellum, Progress in Brain Research, Vol. 25, Elsevier, Amsterdam, 1967, pp. 282-321. 15 Pompeiano, O. and Brodal, A., The origin of vestibulospinal fibers in the cat. An experimental-anatomical study with comments on the descending medial longitudinal fasciculus, Arch. Ital. Biol. 95 (1957) 166-195.
16 Pompeiano, O. and Brodal, A., Experimental demonstration of a somatopical origin of rubrospinal fibers in the cat, J. Comp., Neurol., 108 (1957) 225-252. 17 Shinoda, Y., Ghez, C. and Arnold, A., Spinal branching of rubrospinal axons in the cat, Exp. Brain Res., 30 ( t 977t 203- 218. 18 Tsukahara, N., Toyama, K. and Kosaka, K., lntracellularly recorded responses of red nucleus neurons during antidromic and orthodromic activation, Experientia, 20 ( 19641 632-633. 19 Wilson, V.J., Physiological pathways through the vestibular nuclei. In C.C. Pfiffer and J.R. Smythies (Eds.), International Review of Neurobiology, Vol. 15, Academic Press, New York, 1972, pp. 27 81. 20 Wilson, V.J. and Jones, G.M., Mammalian vestibular physiology, Plenum, New York, 1979, 356 pp. 21 Wilson, V.J. and Peterson, B.W., Peripheral and central substrates of vestibulospinal reflexes, Physiol. Rev., 58 (1978) 80 !05.