- Email: [email protected]
Optimal response planes and canal convergence in secondary neurons in vestibular nuclei of alert cats
Brain Research, 294 (1984) 133-137 Elsevier
133
BRE 20046
Optimal response planes and canal convergence in secondary neurons in vestibular nuclei of alert cats J. BAKER, J. GOLDBERG, G, HERMANN and B. PETERSON Dept. Physiology, Northwestern University School of Medicine, Chicago, 1L 60611 ( U. S.A.) (Accepted November 1st, 1983) Key words': vestibular neurons - - semicircular canal convergence - - 3-dimensional sensitivity
Responses to natural stimulation were studied in electrically identified secondary vestibular neurons of awake cats. A class of neurons was identified whose response dynamics and responses to rotations in several vertical and horizontal planes indicated that they received semicircular canal input. Each canal neuron had clearly defined planes of maximal and null sensitivity to rotation. The orientation of these planes indicated that 44% of the neurons received input from one pair of canals, 40% from two, and 16~ from all 3 canal pairs. Many cells also had oculomotor-related discharges and/or responded weakly to neck rotation. The brainstem vestibular nuclei receive inputs from many sources 2~, including the semicircular canals and otoliths ~,6,m,~9, contralateral vestibular nuclei m,16, somatic sensory afferents 20, oculomotor system ~,t~, visual system~:,~8, and cerebellum 9. These inputs are capable of carrying information on dynamics of a stimulus or muscle action, and about its direction in space. How are the inputs combined in their action on single neurons in vestibular nuclei? A vestibular neuron that receives excitation from a semicircular canal receives inhibition from the complementary contralateral canall,>.~6. There is evidence that many vestibular neurons receive input from more than one pair of canals6, but there are also reports that this kind of convergence is rare, especially at the level of second order vestibular neurons~,lo,13,19. Vestibular and non-vestibular information can converge on single neurons 6,s,12,1s,20,21 . The results we report here extend findings of input convergence to neurons that were monosynaptically excited by labyrinth stimulation in awake cats. Such secondary neurons have been thought to receive their dominant input from a single canal pair, and have been routinely tested with rotation in only one or two planes to determine their canal input. Here we show that canal-canal convergence occurs commonly among secondary neurons, resulting in a wide variety
of optimally excitatory planes of rotation. Convergence of inputs from canals, neck afferents, and oculomotor sources also occurred on secondary neurons. In an accompanying report -~, we show that otoliths must also be included among the convergent inputs to secondary vestibular neurons. Five cats were anesthetized with halothane and nitrous oxide and fitted with a head fixation chronic implant, electro-oculographic ( E O G ) electrodes, and a recording chamber that provided access to the left vestibular nuclei. In a second operation, silver ball electrodes were implanted against the oval and round windows via an opening made in the left tympanic bulla. During recording sessions, a cat was placed in an apparatus that allowed servo motor-controlled positioning and rotation in horizontal and vertical planes. Single neurons were isolated with epoxylite insulated tungsten microelectrodes and tested for monosynaptic activation from the labyrinth by delivering 0.I ms, 0.1-2.0 m A bipolar stimuli across the oval and round window electrodes. We studied only neurons that responded within 1.3 ms to a stimulus current < 5 x threshold for a vestibular N1 potentiaU~. Rotational stimulation and collection and analysis of data on apparatus position,horizontal and vertical eye position, and unit responses were under computer controP.~.
Correspondence: J. Baker, Ward 5, NU Med. School, 303 E. Chicago Ave., Chicago, IL 60611. U.S.A. (J006-8993/84/$03.00 © 1984 Elsevier Science Publishers B.V.
134
B
A
C
IO
10
z
O,
S -lO
-IO
90
0
180
0
-90
90
-10 -90
-J 90
0
180
180
'=° tf
4-
++++
+++ ++4_
+4-1O{
4-4-++ +
l
4_++++++++ -180 I
-180 0
90
180
-80
_H_++ +
+ 0
-180 90 -90
ORIENTAl" ION
ORIENTATION
ORIENTATION
F
E
D
30
4
4
90
0
z
0
\
z J
18o
0
-4 90
180
-SO
0
90
30
180
180 I
z
+
++.+4-+++++++
+
°t
0
-180
I
90
180
o 18o
£
+ + ++~-+_~_ o
-180 I
90
-90
ORIENTATION
ORIENTATION
0,~
I
10
FREOUENCY
Fig. 1. A-E: gain and phase of responses to rotation at 0.5 Hz in different vertical and horizontal planes. Vertical rotation at orientation 0° = pitch, at 90° = roll, horizontal rotation at 0° = yaw in null plane of vertical canals. A: cell I082's response to vertical., plane rotation was nearly maximal with the cat in the 135° position, where the left posterior-right anterior canal (LPC-RAC) pa~r ts nearly in the plane of rotation, and null in the 45° position, where the LPC-RAC pair is orthogonal to the plane of rotation and not stimulated. B: cell I082's response to horizontal rotation was nearly null in the 0* rolled yaw position, indicating very little horizontal canal input. Thus, this cell received almost pure LPC-RAC input. The pitch response predicted from the sine fit curve at +90 ° rolled yaw matches the observed response in A. C: cell I082's responses to pitched yaw horizontal rotations. The cell's predicted response to +90 ° pitched yaw is a close match to the roll response in Figure 1A. D: cell I091's maximum response to vertical rotation occurred near the roll plane, indicating roughly equal input from the LPC-RAC and left anterior-right posterior (LAC-RPC) canals. E: cell 1091's responses to horizontal rotation were strong when the cat was positioned near 0°, indicating horizontal canal input. Thus, the cell received input from all three canal pairs. The gains of the cell's responses to horizontal roll rotation (1E, 9&) and vertical roll rotation (1D, 90°) were the same. F: relative gain (decibels) and phase (deg.) of cell 1091's responses during a sum of ten sinusoids rotation stimulus in the 0° horizontal plane (top) and 80° vertical plane (bottom).
135 The cat was positioned at one of a variety of orientations in the apparatus before applying a rotation stimulus. Rotation via the vertical servo with the cat at our 0 ° horizontal orientation angle presented a pitch stimulus. Vertical rotation with the cat in the horizontal 90 ° orientation (clockwise from zero as seen from above) presented a roll stimulus. Typically, 12 vertical rotation planes at 15° intervals were tested in non-sequential order at 0.5 Hz with response data averaged over 20--40 cycles in each plane. Horizontal or yaw rotation was done in a similar way, orienting the cat at one of several pitch or roll vertical angles (pitched yaw, rolled yaw). Extremes of pitched or rolled yaw were limited by considerations of recording stability and the cat's comfort. We tried to gather data over + 40 °. The head fixation bars pitched the head 28 ° nose down from stereotaxic horizontal plane when the cat was in the 0 ° pitched or rolled yaw position, to minimize vertical canal stimulation. The platform rotation waveform was a sinusoid or sum of 4-10 sinusoids, with amplitude generally + 15° or less. We tested for oculomotor input related to eye position by recording a neuron's activity during gaze fixation at several vertical and horizontal eccentricities, and for neck afferent input by fixing the head in space during vertical or horizontal body rotation. Small electrolytic lesions were made at some recording sites, and after 1-3 months of recording the cat was deeply anesthetized, perfused, and electrode tracks located in vestibular nuclei on Luxol blue/cresyl violet stained sections. Of 137 monosynaptically responsive neurons isolated, 79 were studied with rotation in typically 13-30 planes. A m o n g cells responsive to vertical rotation, we observed two patterns of response as a function of rotation plane orientation angle. Forty-three cells had responses indicative of semicircular canal input (C cells), 26 cells more complex properties indicative of convergent inputs that differed in their spatial orientation and dynamic properties (spatial-temporal convergence or STC cells). In addition, 3 cells had response patterns strongly suggestive of pure otolith input as described by Schor and Miller14. Seven cells responded only to horizontal rotation and were included as C cells based on horizontal rotation responses, making a total of 50 C cells. This report focuses on our analysis of C cell responses; an accom-
panying report 2 describes STC cells. The distinguishing characteristics of C cell responses were sinusoidal variation in response gain as a function of rotation plane orientation and a constant response phase of roughly 90 ° relative to position in the sinusoidal rotation cycle (velocity response), except when rotation was in a plane near the null orientation. Fig. 1A and 1D show gains and phases of responses of two C cells to vertical rotations. Least square sine fits to the gain of C cell responses as a function of rotation plane are shown by curves. Fig. 1B, C, and E show C cell responses to rolled yaw (B) and pitched yaw (C, E) horizontal rotations. Many C cells were studied with sum of sinusoids stimuli, and as shown in Fig. IF, response phase remained approximately constant at about 90 ° relative to position, and gain increased in proportion to frequency. On the assumption, discussed below, that C cell responses to rotation at 0.5 Hz were produced primarily by input from semicircular canals, we used the sinusoidal fits to gain as a function of orientation angle to find the plane of rotation in three dimensional space at which a C cell's response would be maximal. We then found the relative strengths of inputs to the cell from the three canal pairs. A vector representing the axis of a cell's maximal response plane was determined from the fitted sine function values of response gain for vertical rotation in the pitch (0 °) and roll (90 °) planes, and from a fitted or average value to horizontal rotation in the 0 ° yaw plane. Median vector magnitude (sensitivity at 0.5 Hz), was 4.39 spikes/s per degree of rotation, or 1.40 spikes/s per deg./s velocity. C cell maximal response vectors are shown from front and top views in Fig. 2A. Clustering of vectors around the canal plane vectors (shown separately) indicates that many secondary vestibular neurons received input primarily from one canal pair; the dispersion of vectors in other directions indicates that convergence of canal inputs occurred commonly among secondary cells. We found the strength of inputs to each C cell from the three canal pairs using its response vector and a matrix defining canal sensitivities to roll, pitch, and yaw rotation3.1•, calculated from data by Curthoys et alS. The normalized values or canal components for all C cells are plotted in Fig. 2B. Filled circles represent C cells with significant input from only one pair
136
LPC
A
/
/
P~%~i
LfM;~ChL,,
" "
L A(
.......
~ i ~
¸
I P(:
'\\
', \'\
i
.j
il
] (
Fig. 2. A: normalized C cell vectors representing optimal axes of rotation, as seen in our coordinate system from front (left) andabove (right), Shorter vectors are those not in the plane of the graph. The axes of the 3 canal pairs 5 are superimposed on cat drawings shown above for comparison. B: relative contributions of the three canal pairs to each C cell's responses. Positive values correspond to type I responses. Cells that met our criterion for canal convergence (see text) are plotted with X's. The figure shows that canal convergence could occur regardless of whether a neuron received its strongest input from the left horizontal-right horizontal (LHC-RHC), left anterior-right posterior (LAC-RPC), or left posterior-right anterior (LPC-RAC) canal pair. A chi-square test did not reveal any difference in likelihood of convergence when neurons were grouped by their strongest input.
of canals, as defined by an optimal plane at an angle of > 75 ° from the planes of the other canal pairs. This +_ 15 ° error allowance exceeds the uncertainty in the canal orientations 5 and our measurements. All single canal pair input cells were type I of Duensing and Schaeffer 21, except for two horizontal canal cells. By the 75 ° criterion, 22 C cells received input from one canal pair, 20 from two, and 8 from 3 canal pairs. Ten of 18 C cells tested quantitatively showed horizontal or vertical eye position sensitivity of > 0.5 spikes/s per degree (6/9 one canal pair cells, 4/9 convergent cells). Unit activity during saccades was excluded from eye position sensitivity analysis, although obvious sensitivity to saccades was rare. Eleven of 20 C cells responded to horizontal or vertical neck rotation with the head fixed in space (median sensitivity 0.42 spikes/s per degree). It is possible that cutaneous as well as muscle afferents mediated neck rotation responses, as some cells were quite sensitive to light touch around the face and upper neck (often bilaterally). We conclude that C cells are secondary neurons with vestibular input predominantly from semicircular canals, for 3 reasons: (1) the gain and phase of C cell and semicircular canal afferent responses are
quite similar over the range of frequencies we studied 7, (2) the constant phase and sinusoidal variation in gain of C cell responses as a function of rotation plane orientation are predicted from linearly summed canal inputs, and (3) C cell responses to vertical rotations were closely predicted from their responses to rotations in earth horizontal planes. Our results are in strong agreement with M a r k h a m and Curthoys' findings of canal convergence in vestibular nuclei 6, and extend results on natural stimulation to secondary neurons in awake cats. Previous studies of convergence in identified second order vestibular neurons have employed electrical rather than natural stimulation, and have concluded that these neurons rarely receive monosynaptic input from more than one canallJ0,t3J 9. Those results suggest that the neurons on which we observed convergent inputs may have received monosynaptic input from only one canal, coupled with polysynaptic input from others. Why does extensive convergence occur at the first central vestibular relay? The organization of vestibular reflexes requires convergence of vestibular inputs at some point on the pathway to muscles. For example, the spatial orientations of the semicircular canals
137
a n d t h e eye m u s c l e s d i c t a t e t h a t to p r o d u c e p r o p e r l y
essary in 3 n e u r o n v e s t i b u l o - o c u l a r a n d vestibuloospi-
compensatory
each
nal reflex arcs, w h e r e o n l y t w o s y n a p t i c relays are
eye m u s c l e m u s t r e c e i v e i n p u t f r o m all 3 p a i r s of ca-
a v a i l a b l e to t r a n s f o r m s e n s o r y i n f o r m a t i o n i n t o ap-
nals 15,17. O u r d a t a s u g g e s t t h a t s p a t i a l t r a n s f o r m a t i o n
propriate motor commands.
vestibulo-occular
movements,
of h e a d r o t a t i o n signals f r o m t h e s e m i c i r c u l a r c a n a l c o o r d i n a t e s y s t e m to m o t o r c o o r d i n a t e s y s t e m s be-
S u p p o r t e d by E Y 0 4 0 5 8 , E Y 0 0 2 3 1 .
gins at s e c o n d o r d e r n e u r o n s . P e r h a p s this is nec-
1 Abend, W. K , Functional organization of the superior vestibular nucleus of the squirrel monkey, Brain Research, 132 (1977) 65-84. 2 Baker, J., Goldberg, J., Hermann, G. and Peterson, B., Spatial and temporal response properties of secondary neurons receiving convergent input in vestibular nuclei of alert cats, Brain Research, this issue. 3 Baker, J., Goldberg, J., Peterson, B. and Schor, R., Oculomotor reflexes after semicircular canal plugging in cats, Brain Research, 252 (1982) 151-155. 4 Bilotto, G., Goldberg, J., Peterson, B. W. and Wilson, V. J., Dynamic properties of vestibular reflexes in the decerebrate cat, Exp. Brain Res., 47 (1982) 343--352. 5 Curthoys, I. S., Blanks, R. H. I. and Markham, C. H., Semicircular canal functional anatomy in cat guinea pig and man, Acta otolaryng., 83 (1977) 258-265. 6 Curthoys, I. S. and Markham, C. H., Convergence of labyrinthine influences on units in the vestibular nuclei of the cat. I. Natural stimulation, Brain Research. 35 (197I) 469-490. 7 Fernandez, C. and Goldberg, J. M., Physiology of peripheral neurons innervating semicircular canals of the squirrel monkey. I1. Response to sinusoidal stimulation and dynamics of peripheral vestibular system, J. Neurophysiol.. 34 (1971) 661-675. 8 Fuchs, A. and Kimm, J., Unit activity in vestibular nucleus of the alert monkey during horizontal angular acceleration and eye movement, J. Neurophysiol., 38 (1975) 1140-1161. 9 Ito, M., Nisimaru, N. and Yamamoto, M., Specific patterns of neural connections involved in the control of the rabbit's vestibulo-ocular reflexes by the cerebellar flocculus, J. Physiol. (Lond.), 265 11977) 833--854. 10 Kasahara, M. and Uchino, Y., Bilateral semicircular canal inputs to neurons in cat vestibular nuclei, Exp. Brain Res.. 20 (1974) 285-296. ll Keller, E. L. and Kamath, B. Y., Characteristics of head
rotation and eye movement related neurons in alert monkey vestibular nucleus, Brain Research. l(ll) (1975) 182-187. 12 Keller, E, L. and Precht, W., Visual-vestibular responses in vestibular nuclear neurons in the intact and cerebellectomized, alert cat, Neuroscience, 4 (1979) 1599-1613. 13 Markham, C. H. and Curthoys, I. S., Convergence of labyrinthine influences on units in the vestibular nuclei of the cat. If. Electrical stimulation, Brain Research, 43 (1972) 383--397. 14 Schor, R. H. and Miller, A. D., Relationship of cat vestibular neurons to otolith-spinal reflexes. Exp. Brain Res., 47 (1982) 137-144. 15 Schultheis, L. W. and Robinson, D. A., The brainstem matrix of the vestibulo-ocular reflex. In A. Roucoux and M. Crommelinck (Eds.), Physiological and Patholo~,ical Aspects of Eve Movements, W. Junk, The Hague, 1982. pp. 121-125. 16 Shimazu, H. and Precht, W., Inhibition of central vestibular neurons from the contralateral labyrinth and its mediating pathway, J. Neurophysiol.. 29 (1966) 467-492. 17 Simpson, J. I. and Graf, W., Eye-muscle geometry and compensatory eye movements in lateral-eyed and frontaleyed animals, Ann. N. Y. Acad. Sci.. 374 ( 1981 ) 20-30. 18 Waespe, W. and Henn, V., Conflicting visual-vestibular stimulation and vestibular nucleus activity in alert monkeys, Exp. Brain Res., 33 11978) 203-211. 19 Wilson, V. J. and Felpel, L. P., Specificity of semicircular canal input to neurons in the pigeon vestibular nuclei, J. Neurophysiol., 35 (1972) 253-264. 20 Wilson, V. J,, Kato, M.. Thomas, R. C. and Peterson. B. W., Excitation of lateral vestibular neurons by peripheral afferent fibers, J. Neurophysiol., 29 (1966) 508-529. 21 Wilson, V. J. and Melvill Jones, G., Mammalian Vestibular Physiology. Plenum, New York, 1979.
133
BRE 20046
Optimal response planes and canal convergence in secondary neurons in vestibular nuclei of alert cats J. BAKER, J. GOLDBERG, G, HERMANN and B. PETERSON Dept. Physiology, Northwestern University School of Medicine, Chicago, 1L 60611 ( U. S.A.) (Accepted November 1st, 1983) Key words': vestibular neurons - - semicircular canal convergence - - 3-dimensional sensitivity
Responses to natural stimulation were studied in electrically identified secondary vestibular neurons of awake cats. A class of neurons was identified whose response dynamics and responses to rotations in several vertical and horizontal planes indicated that they received semicircular canal input. Each canal neuron had clearly defined planes of maximal and null sensitivity to rotation. The orientation of these planes indicated that 44% of the neurons received input from one pair of canals, 40% from two, and 16~ from all 3 canal pairs. Many cells also had oculomotor-related discharges and/or responded weakly to neck rotation. The brainstem vestibular nuclei receive inputs from many sources 2~, including the semicircular canals and otoliths ~,6,m,~9, contralateral vestibular nuclei m,16, somatic sensory afferents 20, oculomotor system ~,t~, visual system~:,~8, and cerebellum 9. These inputs are capable of carrying information on dynamics of a stimulus or muscle action, and about its direction in space. How are the inputs combined in their action on single neurons in vestibular nuclei? A vestibular neuron that receives excitation from a semicircular canal receives inhibition from the complementary contralateral canall,>.~6. There is evidence that many vestibular neurons receive input from more than one pair of canals6, but there are also reports that this kind of convergence is rare, especially at the level of second order vestibular neurons~,lo,13,19. Vestibular and non-vestibular information can converge on single neurons 6,s,12,1s,20,21 . The results we report here extend findings of input convergence to neurons that were monosynaptically excited by labyrinth stimulation in awake cats. Such secondary neurons have been thought to receive their dominant input from a single canal pair, and have been routinely tested with rotation in only one or two planes to determine their canal input. Here we show that canal-canal convergence occurs commonly among secondary neurons, resulting in a wide variety
of optimally excitatory planes of rotation. Convergence of inputs from canals, neck afferents, and oculomotor sources also occurred on secondary neurons. In an accompanying report -~, we show that otoliths must also be included among the convergent inputs to secondary vestibular neurons. Five cats were anesthetized with halothane and nitrous oxide and fitted with a head fixation chronic implant, electro-oculographic ( E O G ) electrodes, and a recording chamber that provided access to the left vestibular nuclei. In a second operation, silver ball electrodes were implanted against the oval and round windows via an opening made in the left tympanic bulla. During recording sessions, a cat was placed in an apparatus that allowed servo motor-controlled positioning and rotation in horizontal and vertical planes. Single neurons were isolated with epoxylite insulated tungsten microelectrodes and tested for monosynaptic activation from the labyrinth by delivering 0.I ms, 0.1-2.0 m A bipolar stimuli across the oval and round window electrodes. We studied only neurons that responded within 1.3 ms to a stimulus current < 5 x threshold for a vestibular N1 potentiaU~. Rotational stimulation and collection and analysis of data on apparatus position,horizontal and vertical eye position, and unit responses were under computer controP.~.
Correspondence: J. Baker, Ward 5, NU Med. School, 303 E. Chicago Ave., Chicago, IL 60611. U.S.A. (J006-8993/84/$03.00 © 1984 Elsevier Science Publishers B.V.
134
B
A
C
IO
10
z
O,
S -lO
-IO
90
0
180
0
-90
90
-10 -90
-J 90
0
180
180
'=° tf
4-
++++
+++ ++4_
+4-1O{
4-4-++ +
l
4_++++++++ -180 I
-180 0
90
180
-80
_H_++ +
+ 0
-180 90 -90
ORIENTAl" ION
ORIENTATION
ORIENTATION
F
E
D
30
4
4
90
0
z
0
\
z J
18o
0
-4 90
180
-SO
0
90
30
180
180 I
z
+
++.+4-+++++++
+
°t
0
-180
I
90
180
o 18o
£
+ + ++~-+_~_ o
-180 I
90
-90
ORIENTATION
ORIENTATION
0,~
I
10
FREOUENCY
Fig. 1. A-E: gain and phase of responses to rotation at 0.5 Hz in different vertical and horizontal planes. Vertical rotation at orientation 0° = pitch, at 90° = roll, horizontal rotation at 0° = yaw in null plane of vertical canals. A: cell I082's response to vertical., plane rotation was nearly maximal with the cat in the 135° position, where the left posterior-right anterior canal (LPC-RAC) pa~r ts nearly in the plane of rotation, and null in the 45° position, where the LPC-RAC pair is orthogonal to the plane of rotation and not stimulated. B: cell I082's response to horizontal rotation was nearly null in the 0* rolled yaw position, indicating very little horizontal canal input. Thus, this cell received almost pure LPC-RAC input. The pitch response predicted from the sine fit curve at +90 ° rolled yaw matches the observed response in A. C: cell I082's responses to pitched yaw horizontal rotations. The cell's predicted response to +90 ° pitched yaw is a close match to the roll response in Figure 1A. D: cell I091's maximum response to vertical rotation occurred near the roll plane, indicating roughly equal input from the LPC-RAC and left anterior-right posterior (LAC-RPC) canals. E: cell 1091's responses to horizontal rotation were strong when the cat was positioned near 0°, indicating horizontal canal input. Thus, the cell received input from all three canal pairs. The gains of the cell's responses to horizontal roll rotation (1E, 9&) and vertical roll rotation (1D, 90°) were the same. F: relative gain (decibels) and phase (deg.) of cell 1091's responses during a sum of ten sinusoids rotation stimulus in the 0° horizontal plane (top) and 80° vertical plane (bottom).
135 The cat was positioned at one of a variety of orientations in the apparatus before applying a rotation stimulus. Rotation via the vertical servo with the cat at our 0 ° horizontal orientation angle presented a pitch stimulus. Vertical rotation with the cat in the horizontal 90 ° orientation (clockwise from zero as seen from above) presented a roll stimulus. Typically, 12 vertical rotation planes at 15° intervals were tested in non-sequential order at 0.5 Hz with response data averaged over 20--40 cycles in each plane. Horizontal or yaw rotation was done in a similar way, orienting the cat at one of several pitch or roll vertical angles (pitched yaw, rolled yaw). Extremes of pitched or rolled yaw were limited by considerations of recording stability and the cat's comfort. We tried to gather data over + 40 °. The head fixation bars pitched the head 28 ° nose down from stereotaxic horizontal plane when the cat was in the 0 ° pitched or rolled yaw position, to minimize vertical canal stimulation. The platform rotation waveform was a sinusoid or sum of 4-10 sinusoids, with amplitude generally + 15° or less. We tested for oculomotor input related to eye position by recording a neuron's activity during gaze fixation at several vertical and horizontal eccentricities, and for neck afferent input by fixing the head in space during vertical or horizontal body rotation. Small electrolytic lesions were made at some recording sites, and after 1-3 months of recording the cat was deeply anesthetized, perfused, and electrode tracks located in vestibular nuclei on Luxol blue/cresyl violet stained sections. Of 137 monosynaptically responsive neurons isolated, 79 were studied with rotation in typically 13-30 planes. A m o n g cells responsive to vertical rotation, we observed two patterns of response as a function of rotation plane orientation angle. Forty-three cells had responses indicative of semicircular canal input (C cells), 26 cells more complex properties indicative of convergent inputs that differed in their spatial orientation and dynamic properties (spatial-temporal convergence or STC cells). In addition, 3 cells had response patterns strongly suggestive of pure otolith input as described by Schor and Miller14. Seven cells responded only to horizontal rotation and were included as C cells based on horizontal rotation responses, making a total of 50 C cells. This report focuses on our analysis of C cell responses; an accom-
panying report 2 describes STC cells. The distinguishing characteristics of C cell responses were sinusoidal variation in response gain as a function of rotation plane orientation and a constant response phase of roughly 90 ° relative to position in the sinusoidal rotation cycle (velocity response), except when rotation was in a plane near the null orientation. Fig. 1A and 1D show gains and phases of responses of two C cells to vertical rotations. Least square sine fits to the gain of C cell responses as a function of rotation plane are shown by curves. Fig. 1B, C, and E show C cell responses to rolled yaw (B) and pitched yaw (C, E) horizontal rotations. Many C cells were studied with sum of sinusoids stimuli, and as shown in Fig. IF, response phase remained approximately constant at about 90 ° relative to position, and gain increased in proportion to frequency. On the assumption, discussed below, that C cell responses to rotation at 0.5 Hz were produced primarily by input from semicircular canals, we used the sinusoidal fits to gain as a function of orientation angle to find the plane of rotation in three dimensional space at which a C cell's response would be maximal. We then found the relative strengths of inputs to the cell from the three canal pairs. A vector representing the axis of a cell's maximal response plane was determined from the fitted sine function values of response gain for vertical rotation in the pitch (0 °) and roll (90 °) planes, and from a fitted or average value to horizontal rotation in the 0 ° yaw plane. Median vector magnitude (sensitivity at 0.5 Hz), was 4.39 spikes/s per degree of rotation, or 1.40 spikes/s per deg./s velocity. C cell maximal response vectors are shown from front and top views in Fig. 2A. Clustering of vectors around the canal plane vectors (shown separately) indicates that many secondary vestibular neurons received input primarily from one canal pair; the dispersion of vectors in other directions indicates that convergence of canal inputs occurred commonly among secondary cells. We found the strength of inputs to each C cell from the three canal pairs using its response vector and a matrix defining canal sensitivities to roll, pitch, and yaw rotation3.1•, calculated from data by Curthoys et alS. The normalized values or canal components for all C cells are plotted in Fig. 2B. Filled circles represent C cells with significant input from only one pair
136
LPC
A
/
/
P~%~i
LfM;~ChL,,
" "
L A(
.......
~ i ~
¸
I P(:
'\\
', \'\
i
.j
il
] (
Fig. 2. A: normalized C cell vectors representing optimal axes of rotation, as seen in our coordinate system from front (left) andabove (right), Shorter vectors are those not in the plane of the graph. The axes of the 3 canal pairs 5 are superimposed on cat drawings shown above for comparison. B: relative contributions of the three canal pairs to each C cell's responses. Positive values correspond to type I responses. Cells that met our criterion for canal convergence (see text) are plotted with X's. The figure shows that canal convergence could occur regardless of whether a neuron received its strongest input from the left horizontal-right horizontal (LHC-RHC), left anterior-right posterior (LAC-RPC), or left posterior-right anterior (LPC-RAC) canal pair. A chi-square test did not reveal any difference in likelihood of convergence when neurons were grouped by their strongest input.
of canals, as defined by an optimal plane at an angle of > 75 ° from the planes of the other canal pairs. This +_ 15 ° error allowance exceeds the uncertainty in the canal orientations 5 and our measurements. All single canal pair input cells were type I of Duensing and Schaeffer 21, except for two horizontal canal cells. By the 75 ° criterion, 22 C cells received input from one canal pair, 20 from two, and 8 from 3 canal pairs. Ten of 18 C cells tested quantitatively showed horizontal or vertical eye position sensitivity of > 0.5 spikes/s per degree (6/9 one canal pair cells, 4/9 convergent cells). Unit activity during saccades was excluded from eye position sensitivity analysis, although obvious sensitivity to saccades was rare. Eleven of 20 C cells responded to horizontal or vertical neck rotation with the head fixed in space (median sensitivity 0.42 spikes/s per degree). It is possible that cutaneous as well as muscle afferents mediated neck rotation responses, as some cells were quite sensitive to light touch around the face and upper neck (often bilaterally). We conclude that C cells are secondary neurons with vestibular input predominantly from semicircular canals, for 3 reasons: (1) the gain and phase of C cell and semicircular canal afferent responses are
quite similar over the range of frequencies we studied 7, (2) the constant phase and sinusoidal variation in gain of C cell responses as a function of rotation plane orientation are predicted from linearly summed canal inputs, and (3) C cell responses to vertical rotations were closely predicted from their responses to rotations in earth horizontal planes. Our results are in strong agreement with M a r k h a m and Curthoys' findings of canal convergence in vestibular nuclei 6, and extend results on natural stimulation to secondary neurons in awake cats. Previous studies of convergence in identified second order vestibular neurons have employed electrical rather than natural stimulation, and have concluded that these neurons rarely receive monosynaptic input from more than one canallJ0,t3J 9. Those results suggest that the neurons on which we observed convergent inputs may have received monosynaptic input from only one canal, coupled with polysynaptic input from others. Why does extensive convergence occur at the first central vestibular relay? The organization of vestibular reflexes requires convergence of vestibular inputs at some point on the pathway to muscles. For example, the spatial orientations of the semicircular canals
137
a n d t h e eye m u s c l e s d i c t a t e t h a t to p r o d u c e p r o p e r l y
essary in 3 n e u r o n v e s t i b u l o - o c u l a r a n d vestibuloospi-
compensatory
each
nal reflex arcs, w h e r e o n l y t w o s y n a p t i c relays are
eye m u s c l e m u s t r e c e i v e i n p u t f r o m all 3 p a i r s of ca-
a v a i l a b l e to t r a n s f o r m s e n s o r y i n f o r m a t i o n i n t o ap-
nals 15,17. O u r d a t a s u g g e s t t h a t s p a t i a l t r a n s f o r m a t i o n
propriate motor commands.
vestibulo-occular
movements,
of h e a d r o t a t i o n signals f r o m t h e s e m i c i r c u l a r c a n a l c o o r d i n a t e s y s t e m to m o t o r c o o r d i n a t e s y s t e m s be-
S u p p o r t e d by E Y 0 4 0 5 8 , E Y 0 0 2 3 1 .
gins at s e c o n d o r d e r n e u r o n s . P e r h a p s this is nec-
1 Abend, W. K , Functional organization of the superior vestibular nucleus of the squirrel monkey, Brain Research, 132 (1977) 65-84. 2 Baker, J., Goldberg, J., Hermann, G. and Peterson, B., Spatial and temporal response properties of secondary neurons receiving convergent input in vestibular nuclei of alert cats, Brain Research, this issue. 3 Baker, J., Goldberg, J., Peterson, B. and Schor, R., Oculomotor reflexes after semicircular canal plugging in cats, Brain Research, 252 (1982) 151-155. 4 Bilotto, G., Goldberg, J., Peterson, B. W. and Wilson, V. J., Dynamic properties of vestibular reflexes in the decerebrate cat, Exp. Brain Res., 47 (1982) 343--352. 5 Curthoys, I. S., Blanks, R. H. I. and Markham, C. H., Semicircular canal functional anatomy in cat guinea pig and man, Acta otolaryng., 83 (1977) 258-265. 6 Curthoys, I. S. and Markham, C. H., Convergence of labyrinthine influences on units in the vestibular nuclei of the cat. I. Natural stimulation, Brain Research. 35 (197I) 469-490. 7 Fernandez, C. and Goldberg, J. M., Physiology of peripheral neurons innervating semicircular canals of the squirrel monkey. I1. Response to sinusoidal stimulation and dynamics of peripheral vestibular system, J. Neurophysiol.. 34 (1971) 661-675. 8 Fuchs, A. and Kimm, J., Unit activity in vestibular nucleus of the alert monkey during horizontal angular acceleration and eye movement, J. Neurophysiol., 38 (1975) 1140-1161. 9 Ito, M., Nisimaru, N. and Yamamoto, M., Specific patterns of neural connections involved in the control of the rabbit's vestibulo-ocular reflexes by the cerebellar flocculus, J. Physiol. (Lond.), 265 11977) 833--854. 10 Kasahara, M. and Uchino, Y., Bilateral semicircular canal inputs to neurons in cat vestibular nuclei, Exp. Brain Res.. 20 (1974) 285-296. ll Keller, E. L. and Kamath, B. Y., Characteristics of head
rotation and eye movement related neurons in alert monkey vestibular nucleus, Brain Research. l(ll) (1975) 182-187. 12 Keller, E, L. and Precht, W., Visual-vestibular responses in vestibular nuclear neurons in the intact and cerebellectomized, alert cat, Neuroscience, 4 (1979) 1599-1613. 13 Markham, C. H. and Curthoys, I. S., Convergence of labyrinthine influences on units in the vestibular nuclei of the cat. If. Electrical stimulation, Brain Research, 43 (1972) 383--397. 14 Schor, R. H. and Miller, A. D., Relationship of cat vestibular neurons to otolith-spinal reflexes. Exp. Brain Res., 47 (1982) 137-144. 15 Schultheis, L. W. and Robinson, D. A., The brainstem matrix of the vestibulo-ocular reflex. In A. Roucoux and M. Crommelinck (Eds.), Physiological and Patholo~,ical Aspects of Eve Movements, W. Junk, The Hague, 1982. pp. 121-125. 16 Shimazu, H. and Precht, W., Inhibition of central vestibular neurons from the contralateral labyrinth and its mediating pathway, J. Neurophysiol.. 29 (1966) 467-492. 17 Simpson, J. I. and Graf, W., Eye-muscle geometry and compensatory eye movements in lateral-eyed and frontaleyed animals, Ann. N. Y. Acad. Sci.. 374 ( 1981 ) 20-30. 18 Waespe, W. and Henn, V., Conflicting visual-vestibular stimulation and vestibular nucleus activity in alert monkeys, Exp. Brain Res., 33 11978) 203-211. 19 Wilson, V. J. and Felpel, L. P., Specificity of semicircular canal input to neurons in the pigeon vestibular nuclei, J. Neurophysiol., 35 (1972) 253-264. 20 Wilson, V. J,, Kato, M.. Thomas, R. C. and Peterson. B. W., Excitation of lateral vestibular neurons by peripheral afferent fibers, J. Neurophysiol., 29 (1966) 508-529. 21 Wilson, V. J. and Melvill Jones, G., Mammalian Vestibular Physiology. Plenum, New York, 1979.