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Relation between motoneuron position and lateral rectus motor unit contraction speed: An intracellular study in the cat abducens nucleus
49 Ltd.
RELA'HONB~EN M~£ONEURON POSITION AND LATERAL RECTUS MOTOR UNIT CONTRACHON S P ~ D : AN INTRAC]ELLULAR STUDY CAT ~ D U ENS N U ~ E U S
STEPHEN J. GOLDBERG, H, PETER CLAMANN and J, ROSS McCLDNG
Delmrtments o f Anatomy a n d Physiology, Medical College of Virginia, Virginia Commonwealth University, Richmond, VA 23298 (U.S.A.) (Received December 3rd, 1980; Revised version received January 27th, 1981; Accepted January 30th, 1981).
Thirty-one single muscle traits of the cat lateral rectus muscle were activated through intraceUular stimulation of their motoneurons in the principal abducen~ nucleus. Motoneuroas encounter~ from dorsal W ventral in the nucleus tended '.o innervate muscle units with progressively slower contraction times, lnaddition, two cells innervated muscle units which did not exhibit twitch contra ,fions and three cells innervated muscle units with ,musually strong twitch contractions.
Previous investigations have indicated that there may be different types of organizational tendencies in motoneuron (MN) pools. In the spinal cord, the rostral third of the eat medial gastrocnemius (MG) nucleus contains more large alpha-MNs than the caudal two-thirds and they tend to innervate muscle units in the dorsal margin of the MG muscle [3]. The dorsal margin of the IViG muscle also contains a
these authors emphasi~ that there is no strict segregation of MNs according to size o r motor unit t y ~ [3|: Other investigators [9] have observed a somatotopic relation between the Caudocranial ~sition of ventral rootlets and the area of evoked cat MG muscle contraction, but any organization in relation to MN s i x has been challenged [4]~ In the extraocular mmcle nuclei, an antidromic field potential profile of the cat trochlear nucleus !ed to the presumption that smaller MNs were located in the dorsomedial aspe~ of the nucleus [I], but!no distribution according to MN size has ~en nucleus [8]. The~e previous reports con~rning possible motorzuronal organizational tendencies, as well as an earlier report which tentatively indicated that lateral rectus MNs were organized in relation to the twitch contraction speed of ~he muscle units t h ~ innervated [5~, l ~ u s to the present study. This ~udy Was d ~ i ~ motoneur~n organ~ation i~ the with eg d to motor nnit m ha 0at
A ~ u c e m r m c I ~ MNs were i d e n t i ~
of ~ e
u n t i l a s + m ~ +~ti<:m +
~bserved ~ y in con: twitcF~s and respon~
gauge (sensitive from < | rng isolated lateral rectus m ~ l e in the orbit. T ~ detaii+ of these +~ocedures have ~ + :previously [5+++6]. 0.89 to 2.92 nun (average ~ h = 1.68 ~ ) beneath the floor ofthe tVth ventricle. Accurate depth measurements could not ~ ~ i n e d for 5 o f the ~ s , Intracellular stimulation of 3t MNs elicited mechanical responses at the lateral rectus muscle. Twitch contraction characteristics were obtained in 29 muscle units. while 2 muscle units only contracted in response to tetanic stimulation. Responses to tetanic stimulation were recorded m !7 muscle m ~ , including tile 2 listed in the previous sentence, The 9 ~ l s which mechanical r e s p o ~ following intrace|lular stimulation t o innervate the retractor bulbi muscle. Fig. 1A-C illustrates the antidromic identification of a lateral rectus MN ~.3 mm beneath the floor of the IVth ventricle and its muscle unit characteristics. Fig. I D - F illustrates similar findings for a MN found 2.3 mm deep. Significant differences in twitch contraction time and fusion frequency are apparent for the MNs at the different depths. The graphs in Fig. 2A and B illustrate the correlation of depth with fusion frequency and contraction time. The different symbol g r ~ used in the graphs indicate :ells found in different experimental animals. The correlation coefficient in
............ the IVth Ventricle, T h ~ are not contractionsi M e respon~ t~ ....................... simi (MII the twit( In r
floor of
of mu~
51
A
D
i2oo,
J 20mY 0,5 ms
O,Sms F~
5ms
5m$
C
$
106 m~ $0 ms S
I ~'6mg 50 ms
W
|23m~
SO.~s Fig. 1, A: antidromic identification of an abducens nucleus motoneuron ~,t 1.3 mm beneath the floor of the IVth ventricle, B: lwitch contraction o f lateral rectus muscle writ in response to single pulse intracellular stimulation of cell in A. C: tetanic contractions of muscle unit in B at ~0, |00, 150 and 200 pulses per second from bottom to top, D: antktromic identification of an abducens nucleus motoneuron at 2,3 mm beneath the floor of the IVth ventricle. E: twitch contraction of lateral cectus muscle uni~ in response to single pulse intraccHular ~imulation o f eel| in D. F: tetanic contraction of muscle unit in E at 50, I00, 125, 150 and 200 pulses per second from bottom to top. G: t~a~ic contra~ion o f a 'non-twitch" muscle unit a t 50, i00, 150 and 200 pulses per second from bottom ~o top. Bar ~abeled S indicates duration of stimulus train for C, F and G. Arrow~ in A and D indicate antidromic stimulus onset.
52
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Fig. 2. A: the depths at ,"hich ia)eral rectus m~oneurons were encxranterecl plott~ against the fusion frequencies of the mTasele units innervated. [~fferent symbol group~ indh:ate ~lls from differem e×perJmental animals B: the depths at which ~eral rectus moto~'uro~ were encountered plotted against the twitch contraction times of the muscl,, unit,o innervated.
only injected 3 cells which innervate unusually strong muscle units, it is of interest to note that all 3 exhibited axons which cour~ed dorsally before turning ven*.rally into the Vlth nerve and all were large cells. We have noted no other lateral rectus MNs with dorsally directed axons. The average twitch contraction time of the muscle units, exclusive of the two units which did not exhibit twitch contraction, was 6.2 msec: and the average fusion frequency was 151.5 pulses per second. Twitch and tetanic tensions were generally similar to those of previous reports [5, 6], except for the 3 unusually strong muscle units° The res,alts of this study indicate that cat abducens MNs v, hich innervate the lateral rectus muscle tend to be anatomically organized within the principal abducens nucleus with regard to the co:4traction speed of single muscle units: dorsal MNs innervate fast contracting muscle units while ventral MNs innervate slower contracting ~ i t s . This type of motor unit organization may be related to muscle unit location in the lateral ~ectus muscle or to the embryological development of the ~ucleuso It also appears that muscle units wi:.h non-propogated electrical activity are present iv the cat lateral rectus muscle, as has been reported for the cat inferior oblique muscle [6]. In addition, a small population of muscle units with
53
Fig. 3. Light micrographs of motoneurons from the principal abducens nucleus following intracellular injections of HRP (DAB histochemistry). A: this cell was shown to innervate a lateral rectus muscle unil of unusually high twitch contraction strength ( > I00 rag). The light labeling~ as a resutt of intraaxonaI injection, allows demonstration of the nucleus of the cell, indicating the central location thus ~he accuracy of the average diameter readings (50 #m). B: this cell (intrasomatic injection) was ~hown ~o inner, ate a lateral rectus mu~le unit of average twitch contraction strength ( = 15 rag) and ~o have a raean diameter of = 50 #ra. Arrows indicate axons in A and B.
,~nusually high twitch tensions have been identified. These powerful muscle units may be i~nervated by cells among the small population of large MNs ( > 50 #m in diameter) as observed anatomicaUy [8], but not all large MNs innervate powerful muscle units. This research was supported by Grants EY 01442 and NS 11677 from the National Institutes of Health. 1 Baker~ R, and Precht, W., ElectrophysiologJcal properties of trochlear motoneurons as revealed by lVth nerve stiraulation, Eng. Brain Res., 14 (t972) |27-157. 2 Burke, R.E., Motor unit types o f the cat triceps surae rausc[e, J. Physiol. (Lond.L 193 (1967) !41-[60o 3 Burke, R.E., Strick, P.L., Kanda, K., Kim, CoC. and Wa~ms[e.y, B.~ Anatomy o f media[ gastrocnemius and soleu~ c~ot-or nadei in cat. spinal cord, J, Neurophysiol., 40 (1977) 667-680.
,
_-, .’
RELA'HONB~EN M~£ONEURON POSITION AND LATERAL RECTUS MOTOR UNIT CONTRACHON S P ~ D : AN INTRAC]ELLULAR STUDY CAT ~ D U ENS N U ~ E U S
STEPHEN J. GOLDBERG, H, PETER CLAMANN and J, ROSS McCLDNG
Delmrtments o f Anatomy a n d Physiology, Medical College of Virginia, Virginia Commonwealth University, Richmond, VA 23298 (U.S.A.) (Received December 3rd, 1980; Revised version received January 27th, 1981; Accepted January 30th, 1981).
Thirty-one single muscle traits of the cat lateral rectus muscle were activated through intraceUular stimulation of their motoneurons in the principal abducen~ nucleus. Motoneuroas encounter~ from dorsal W ventral in the nucleus tended '.o innervate muscle units with progressively slower contraction times, lnaddition, two cells innervated muscle units which did not exhibit twitch contra ,fions and three cells innervated muscle units with ,musually strong twitch contractions.
Previous investigations have indicated that there may be different types of organizational tendencies in motoneuron (MN) pools. In the spinal cord, the rostral third of the eat medial gastrocnemius (MG) nucleus contains more large alpha-MNs than the caudal two-thirds and they tend to innervate muscle units in the dorsal margin of the MG muscle [3]. The dorsal margin of the IViG muscle also contains a
these authors emphasi~ that there is no strict segregation of MNs according to size o r motor unit t y ~ [3|: Other investigators [9] have observed a somatotopic relation between the Caudocranial ~sition of ventral rootlets and the area of evoked cat MG muscle contraction, but any organization in relation to MN s i x has been challenged [4]~ In the extraocular mmcle nuclei, an antidromic field potential profile of the cat trochlear nucleus !ed to the presumption that smaller MNs were located in the dorsomedial aspe~ of the nucleus [I], but!no distribution according to MN size has ~en nucleus [8]. The~e previous reports con~rning possible motorzuronal organizational tendencies, as well as an earlier report which tentatively indicated that lateral rectus MNs were organized in relation to the twitch contraction speed of ~he muscle units t h ~ innervated [5~, l ~ u s to the present study. This ~udy Was d ~ i ~ motoneur~n organ~ation i~ the with eg d to motor nnit m ha 0at
A ~ u c e m r m c I ~ MNs were i d e n t i ~
of ~ e
u n t i l a s + m ~ +~ti<:m +
~bserved ~ y in con: twitcF~s and respon~
gauge (sensitive from < | rng isolated lateral rectus m ~ l e in the orbit. T ~ detaii+ of these +~ocedures have ~ + :previously [5+++6]. 0.89 to 2.92 nun (average ~ h = 1.68 ~ ) beneath the floor ofthe tVth ventricle. Accurate depth measurements could not ~ ~ i n e d for 5 o f the ~ s , Intracellular stimulation of 3t MNs elicited mechanical responses at the lateral rectus muscle. Twitch contraction characteristics were obtained in 29 muscle units. while 2 muscle units only contracted in response to tetanic stimulation. Responses to tetanic stimulation were recorded m !7 muscle m ~ , including tile 2 listed in the previous sentence, The 9 ~ l s which mechanical r e s p o ~ following intrace|lular stimulation t o innervate the retractor bulbi muscle. Fig. 1A-C illustrates the antidromic identification of a lateral rectus MN ~.3 mm beneath the floor of the IVth ventricle and its muscle unit characteristics. Fig. I D - F illustrates similar findings for a MN found 2.3 mm deep. Significant differences in twitch contraction time and fusion frequency are apparent for the MNs at the different depths. The graphs in Fig. 2A and B illustrate the correlation of depth with fusion frequency and contraction time. The different symbol g r ~ used in the graphs indicate :ells found in different experimental animals. The correlation coefficient in
............ the IVth Ventricle, T h ~ are not contractionsi M e respon~ t~ ....................... simi (MII the twit( In r
floor of
of mu~
51
A
D
i2oo,
J 20mY 0,5 ms
O,Sms F~
5ms
5m$
C
$
106 m~ $0 ms S
I ~'6mg 50 ms
W
|23m~
SO.~s Fig. 1, A: antidromic identification of an abducens nucleus motoneuron ~,t 1.3 mm beneath the floor of the IVth ventricle, B: lwitch contraction o f lateral rectus muscle writ in response to single pulse intracellular stimulation of cell in A. C: tetanic contractions of muscle unit in B at ~0, |00, 150 and 200 pulses per second from bottom to top, D: antktromic identification of an abducens nucleus motoneuron at 2,3 mm beneath the floor of the IVth ventricle. E: twitch contraction of lateral cectus muscle uni~ in response to single pulse intraccHular ~imulation o f eel| in D. F: tetanic contraction of muscle unit in E at 50, I00, 125, 150 and 200 pulses per second from bottom to top. G: t~a~ic contra~ion o f a 'non-twitch" muscle unit a t 50, i00, 150 and 200 pulses per second from bottom ~o top. Bar ~abeled S indicates duration of stimulus train for C, F and G. Arrow~ in A and D indicate antidromic stimulus onset.
52
°\ 27..,
A
\
3° 1
ZS.
4 24! 22.
E
20
1o.
1
N
,c.,
~8
•
00°
0
I
i
74
.21 i0-
\
I
tO0
]25
I5.0
175
0
/-
08" L--
75
0
200
255
.
,
4
5
6
7
8
9
~0
~
FL~C~ FREOLt.EI~CV (Ix~e~ pet ~ ¢ ~ }
Fig. 2. A: the depths at ,"hich ia)eral rectus m~oneurons were encxranterecl plott~ against the fusion frequencies of the mTasele units innervated. [~fferent symbol group~ indh:ate ~lls from differem e×perJmental animals B: the depths at which ~eral rectus moto~'uro~ were encountered plotted against the twitch contraction times of the muscl,, unit,o innervated.
only injected 3 cells which innervate unusually strong muscle units, it is of interest to note that all 3 exhibited axons which cour~ed dorsally before turning ven*.rally into the Vlth nerve and all were large cells. We have noted no other lateral rectus MNs with dorsally directed axons. The average twitch contraction time of the muscle units, exclusive of the two units which did not exhibit twitch contraction, was 6.2 msec: and the average fusion frequency was 151.5 pulses per second. Twitch and tetanic tensions were generally similar to those of previous reports [5, 6], except for the 3 unusually strong muscle units° The res,alts of this study indicate that cat abducens MNs v, hich innervate the lateral rectus muscle tend to be anatomically organized within the principal abducens nucleus with regard to the co:4traction speed of single muscle units: dorsal MNs innervate fast contracting muscle units while ventral MNs innervate slower contracting ~ i t s . This type of motor unit organization may be related to muscle unit location in the lateral ~ectus muscle or to the embryological development of the ~ucleuso It also appears that muscle units wi:.h non-propogated electrical activity are present iv the cat lateral rectus muscle, as has been reported for the cat inferior oblique muscle [6]. In addition, a small population of muscle units with
53
Fig. 3. Light micrographs of motoneurons from the principal abducens nucleus following intracellular injections of HRP (DAB histochemistry). A: this cell was shown to innervate a lateral rectus muscle unil of unusually high twitch contraction strength ( > I00 rag). The light labeling~ as a resutt of intraaxonaI injection, allows demonstration of the nucleus of the cell, indicating the central location thus ~he accuracy of the average diameter readings (50 #m). B: this cell (intrasomatic injection) was ~hown ~o inner, ate a lateral rectus mu~le unit of average twitch contraction strength ( = 15 rag) and ~o have a raean diameter of = 50 #ra. Arrows indicate axons in A and B.
,~nusually high twitch tensions have been identified. These powerful muscle units may be i~nervated by cells among the small population of large MNs ( > 50 #m in diameter) as observed anatomicaUy [8], but not all large MNs innervate powerful muscle units. This research was supported by Grants EY 01442 and NS 11677 from the National Institutes of Health. 1 Baker~ R, and Precht, W., ElectrophysiologJcal properties of trochlear motoneurons as revealed by lVth nerve stiraulation, Eng. Brain Res., 14 (t972) |27-157. 2 Burke, R.E., Motor unit types o f the cat triceps surae rausc[e, J. Physiol. (Lond.L 193 (1967) !41-[60o 3 Burke, R.E., Strick, P.L., Kanda, K., Kim, CoC. and Wa~ms[e.y, B.~ Anatomy o f media[ gastrocnemius and soleu~ c~ot-or nadei in cat. spinal cord, J, Neurophysiol., 40 (1977) 667-680.
,
_-, .’