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Connections of cat omnipause neurons
166
Brain Research, 241 (1982) 166-170
Elsevier Biomedical Press
Connections of cat omnipause neurons CHRIS R. S. KANEKO and ALBERT F. FUCHS Department of Physiology and Biophysics, and Regional Primate Research Center, University of Washington, Seattle, WA 98195 (U.S.A.)
(Accepted February 18th, 1982) Key words: omnipause neurons - - saccades - - eye movements
Omnipause neurons (OPNs) are brainstem neurons that have been implicated in the generation of saccades. Anatomically demonstrated projections from the OPN region to the cerebellum and spinal cord originate from neighboring neurons, not from OPNs. OPNs are activated following stimulation of the optic chiasm and superior colliculus, but not following stimulation of the vestibular nerve. On the basis of single-neuron recordings and stimulation in alert monkeysS, 9, it has been suggested that the discharge in motoneurons during saccadic eye movements is the result of a burst of action potentials in brainstem 'burst neurons' (BNs). BNs are thought to be tonically inhibited during intersaccadic intervals by omnipause neurons (OPNs) which, in turn, must be inhibited to initiate saccades. We recently injected tritiated amino acids into the O P N region and found that the O P N region projects to three groups of structures: (1) all areas known to contain BNs; (2) the cerebellum, particularly the flocculus and vermis, and structures that project to the cerebellum; and (3) the spinal cord and structures that project to the spinal cord. Although projections to BN regions are consistent with our present understanding of how saccades are generated, direct projections from OPNs to the cerebellum and spinal cord are not readily incorporated into this scheme. One limitation of the orthograde tracer technique is that it does not distinguish between the efferents of OPNs and those of other neurons whose somata lie in the same region. Thus, the major purpose of these experiments was to test directly whether the observed projections from the O P N region 8 arose from OPNs per se. To do this, we recorded OPNs in ketamine-anesthetized cats 3,6 and attempted to activate them by stimulating the cerebellar vermis and cervical spinal cord. 0006-8993/82/0000-0000/$02.75 © Elsevier Biomedical Press
A secondary objective was to investigate other regions for connections with OPNs. Since we had shown that cat OPNs are activated by visual stimuli (refs. l, 2), we placed stimulating electrodes on the optic chiasm. We also placed stimulating electrodes in the superior colliculus to test whether it might be the source of the visual input or, alternatively, a source for an inhibitory input that could trigger saccades. Finally, we placed stimulating electrodes on the vestibular nerves to test for direct inhibitory input that could act as the trigger for the fast phases of nystagmus. A preliminary report of these results has appeared 3. Fifteen adult male cats were anesthetized with i.m. injections of ketamine hydrochloride (45 rag/ kg) supplemented with continuous i.v. infusion of ketamine diluted in saline (10 mg/kg/h). All wound margins were dusted with long-lasting 10 ~ benzocaine powder. The cats were mounted in a stereotaxic apparatus on which the front stabilization was modified to allow the introduction of an eye-movement transducer. The transducer, a photo-diode that detected art infrared beam from a light-emitting diode affixed to the cornea, was sensitive to less than 0.1 ° of movement and was linear ( ± 3 ~ ) within 2~ 15° of the midposition. While the cats were in the prone position, stimulating electrodes were placed in the cerebellar vermis, the optic chiasm, and/or the superior colliculus. The
167 tungsten microelectrodes and conventional extracellular recording techniques. Following each experiment, the cat was killed with an overdose of Nembutal and perfused with saline followed by 10~o formalin. Marking lesions were made by the stimulating electrodes, and the locations of recording and stimulating electrodes were confirmed histologically. Sixty-nine OPNs were identified on the basis of their discharge patterns in relation to eye movements and their anatomical location. The upper portion of Fig. 1 illustrates the similarity of discharge patterns in alert (left) and ketamine-anesthetized (right) cats. Note that in both records the tonic discharge is unrelated to eye position but ceases abruptly for each saccadic eye movement. The lower half of Fig. 1 shows parasagittal sections of the reconstructed locations of the recording sites of the neurons pictured above and, in addition, illustrates the region over which OPNs could be recorded in the two paradigms. The two regions are very similar in rostro-caudal and dorso-ventral extent, although
vermal electrodes were placed visually in lobules 5 and 6 and positioned to evoke eye movements to electrical stimulation. The chiasm electrode was positioned to record the maximum flash-evoked potential. The bilateral collicular electrodes were placed to record either the flash- or chiasm-evoked responses and then fine-adjusted to produce eye movements when stimulating currents were applied. The cats were then rotated to the supine position to expose the ventral surface of the spinal cord and ponto-medullary brainstem. Bipolar stimulating electrodes were placed bilaterally in the ventral quadrants of the spinal cord at the C2 level to allow activation of tracts previously labeled in our autoradiographic material. Electrodes also were placed on both vestibular nerves via a ventral approach through the bullae. All electrodes were pairs of A g AgCI electrodes that could be positioned independently exce'l~t for the collicular electrodes, which had a concentr{c bipolar configuration. O P N discharge was recorded near the midline at the level of the exit of the abducens nerve using insulated iron-tipped
Im
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,~!',c',,~ ~5;,~i,~i~i~,,~ ~LL,~i;
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Fig. 1. Identification of omnipause neurons (OPNs). Upper: activity of OPNs recorded in an alert, trained cat (left) and in a ketamine-anesthetized cat (right) shows their similar discharge characteristics. Note that the anesthetized cat makes smaller spontaneous saccades and does not hold fixation. Lower: location of OPNs shown on parasagittal standard sections. Three marking lesions (Ieft) show the dorso-ventral extent of OPNs recorded on a single tract in an alert animal. This area coincides with the region where we recorded OPNs (right, hatched) in anesthetized cats. The black line is a lesion caused by an electrode in another experiment; the black dot is the site of the OPN recording above.
168 D
A
.
.
.
.
E 1 ms
B
F
Optic chiasm stimuiotion lOq Mean latency = 9.07 ± 141(sd) /
C
--r?
z
,
Q
2
,
4 6 8 10 12 LQtency (reset)
5 ms
Fig. 2. OPN responses to stimulation of the spinal cord (A) and optic chiasm (B-E). Three superimposed traces (A) show a consistent field response (first arrow) following stimulation (dot) of the spinal cord at the C2 level at current intensities just below threshold for limb twitches. The spontaneous action potential during one of the 3 trials (second arrow) shows that any response to cord stimulation would be easily distinguished. The response to optic chiasm stimulation is shown in 4 (D and E) or 5 (B and C) superimposed traces. Increasing current strength from threshold (B) to 1.5 × threshold (C) slightly reduced the latency of the response but did not make the response more secure; further increases in current strength did not alter the response. Using double (E) versus single (D) shock at maximal current intensities did not make the response more stable. F: latency histogram of the first action potential in the OPN following threshold stimulation of the optic chiasm. Calibration in C applies for B-E.
the mediaMateral extent seems to be reduced in the anesthetized preparationsl,S. None of the 17 OPNs tested for antidromic activation from the spinal cord responded following even supramaximal stimulation (Fig. 2A). The stimulation was effective because it: (1) evoked prominent fields in the O P N region (Fig. 2A); (2) could elicit short-latency antidromic responses from reticulo-spinal neurons recorded at the margins of the O P N region, and (3) often resulted in twitches of the limbs at high current intensities.
Stimulation of the vermis did not activate the 12 OPNs tested. Similarly, no response was elicited in 25 OPNs following ipsi- or contralateral vestibular stimulation, even at stimulus currents that were several times threshold for evoking a vestibular field potential and were often sufficient to produce movement of the globe. In contrast, stimulation of either the optic chiasm or the superior colliculus evoked a consistent response in OPNs. The response of 41/46 OPNs to chiasm stimulation is illustrated in Fig. 2B-E. To make the response to stimulation more clear, stimulation was triggered so that the response occurred during the interspike interval. The superimposed traces (Fig. 2B-E) show that stimulation produced a variable, long-latency excitation. Because both the occurrence of the response and its latency were variable, we could not tell whether there was, in addition, an initial inhibition and/or an inhibition following the excitation. The response efficacy was not improved either by increasing current strength from threshold (B) to 1.5 × threshold (C) (although the minimal latency was slightly reduced) or by using double (E) versus single (D) shock. A histogram of the latency from the threshold stimulus to the first extracellularly recorded action potential is shown in F. Fig. 3 shows the response of OPNs following stimulation of the superior colliculus. The response consists of an initial short-latency excitation followed by a longer-duration inhibition of the tonic discharge (Fig. 3B). The excitation has a variable latency (Fig. 3A; 3 superimposed trials, evoked action potentials indicated by downward arrows) at threshold stimulating currents and the duration of the inhibition is proportional to the number of stimuli (Fig. 3B). Effective collicular stimulation sites were always in the intermediate and deep layers (Fig. 3C). Collicular stimulation activated only 23 of 35 OPNs; the remaining 12 OPNs did not respond even at stimulating currents of 1 mA or more, which should have activated most of the superior colliculusl0. This study showed that OPNs do not project directly to the spinal cord or to the cerebellar vermis, nor do they receive direct afferents from those structures. This conclusion is consistent with the results of our control injections of tritiated
169
A
vestibular nerve stimulation resulted in strong, short-latency inhibition of O P N discharge as might be expected if these structures were the source of an inhibitory trigger to OPNs that initiates saccades. The initial response to collicular stimulation was excitatory rather than inhibitory, while there was no response at all to VN stimulation (cf. King et al.6,7). Although the excitatory response could not trigger saccades, it might have relayed a portion of the visual excitation of OPNs seen in alert cats1, 2 and confirmed by chiasm stimulation (Fig. 2) in this and other7, s studies. King et al. 7 have suggested, on the basis of lesion studies, that the visually induced excitation of OPNs 1,2 reaches them via both the cortex and the colliculus. Our own data 1 suggest that whatever the pathway, the excitation is not obviously important in oculomotor function. On the other hand, the inhibition of OPNs evoked by stimulation of the superior colliculus may be important in the generation of saccades. Longduration inhibition following collicular stimulation has been reported in alert monkeys ~2, but only when the stimulus also elicited a saccade. It was therefore impossible to determine whether the inhibition was caused by direct activation from the colliculus or was due merely to the concomitant occurrence of a saccade. However, in both the present study and in alert cats (Kaneko, Grarttyn and Fuchs, unpublished observations), we have produced OPN inhibition following cotlicular stimulation at stimulus intensities too small to elicit a saccade, suggesting that the superior colliculus has direct access to
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Fig. 3. Activation of OPNs following stimulation of superior colliculus (dots in B). A: 3 superimposed sweeps showing short-latency (1-2 ms) excitation (the positive peak of each action potential is indicated by a downward arrow). B: superimposed trials showing prolonged inhibition of lhe same OPN's tonic discharge following (top to bottom) two, three and four shocks to the colliculus. C: transverse section of the brainstem showing a marking lesion made at the end of the experiment. amino acids around, but not in, the OPN region, which suggested that cerebellar and cord projections were not from OPNs per se4,8. Another study 11, employing stimulation of the flocculus, showed that OPNs did not send axons to or receive afferents from the flocculus. We conclude that since OPNs project directly to areas that contain BNs but only indirectly to the cerebellum and spinal cord, OPNs probably subserve a strictly oculomotor function. This study also showed that neither collicular nor
1 Evinger, C., Kaneko, C. R. S. and Fuchs, A. F., The activity of omnipause neurons in alert cats during saccadic eye movements and visual stimuli, J. NeurophysioL, 47 (1982) 827-844. 2 Evinger, C., Kaneko, C. R. S., Johanson, G. W. and Fuchs, A. F., Omnipauser cells in the cat. In R. Baker and A. Berthoz (Eds.), Control of Gaze by Brain Stem Neurons,
OPNs. We gratefully acknowledge L. Pfeiffer for secretarial help, K. Schmitt for editorial assistance, P. Roberts and T. Nguyen for photography, and C. Ganders for care of the animals. This study was supported by Grants EY00096, EY00745, RR00166 from the National Institutes of Health.
Developments in Neuroseienee, VoL 1, Elsevier/North-
Holland, Amsterdam, 1977, pp. 337-348. 3 Kaneko, C. R. S. and Fuchs, A. F., Connections of feline omnipause neurons, Neurosci. Abstr., 4 (1978) 164. 4 Kaneko, C. R. S., Langer, T. P. and Graybiel, A. M., Efferent projections of the pontine oculomotor pauser region in the cat, Neurosci. Abstr., 5 (1979) 374.
170 5 Keller, E. L,, Participation of medial pontine reticular formation in eye movement generation in monkey, J. Neurophysiol., 37 (1974) 316-332. 6 King, W. M., Precht, W. and Dieringer, N., Connections of behaviorally identified cat omnipause neurons, Exp. Brain Res., 31 (1978) 435438. 7 King, W. M., Precht, W. and Dieringer, N., Afferent and efferent connections of cat omnipause neurons, Exp. Brain Res., 38 (1980) 395-403. 8 Langer, T. P. and Kaneko, C. R. S., Efferent projections of eat omnipause neurons, J. eomp. Neurol., submitted. 9 Luschei, E. S. and Fuchs, A. F., Activity of brain stem
neurons during eye movements of alert monkeys, aT. Neurophysiol., 35 (1972) 445M61. 10 McIlwain, J. T., Lateral spread of neural excitation during microstimulation in the intermediate gray layer of the cat's superior colliculus, J. Neurophysiol., 47 (1982) 167-178. 11 Nakao, S., Curthoys, I. S. and Markham, C. H., Eye movement related neurons in the cat pontine reticular formation: projection to the flocculus, Brain Research, 183 (1980) 291-299. 12 Raybourn, M. S. and Keller, E. L., Colliculoreticular organization in primate oculomotor system, J. Neurophysiol., 40 (1977) 861-878.
Brain Research, 241 (1982) 166-170
Elsevier Biomedical Press
Connections of cat omnipause neurons CHRIS R. S. KANEKO and ALBERT F. FUCHS Department of Physiology and Biophysics, and Regional Primate Research Center, University of Washington, Seattle, WA 98195 (U.S.A.)
(Accepted February 18th, 1982) Key words: omnipause neurons - - saccades - - eye movements
Omnipause neurons (OPNs) are brainstem neurons that have been implicated in the generation of saccades. Anatomically demonstrated projections from the OPN region to the cerebellum and spinal cord originate from neighboring neurons, not from OPNs. OPNs are activated following stimulation of the optic chiasm and superior colliculus, but not following stimulation of the vestibular nerve. On the basis of single-neuron recordings and stimulation in alert monkeysS, 9, it has been suggested that the discharge in motoneurons during saccadic eye movements is the result of a burst of action potentials in brainstem 'burst neurons' (BNs). BNs are thought to be tonically inhibited during intersaccadic intervals by omnipause neurons (OPNs) which, in turn, must be inhibited to initiate saccades. We recently injected tritiated amino acids into the O P N region and found that the O P N region projects to three groups of structures: (1) all areas known to contain BNs; (2) the cerebellum, particularly the flocculus and vermis, and structures that project to the cerebellum; and (3) the spinal cord and structures that project to the spinal cord. Although projections to BN regions are consistent with our present understanding of how saccades are generated, direct projections from OPNs to the cerebellum and spinal cord are not readily incorporated into this scheme. One limitation of the orthograde tracer technique is that it does not distinguish between the efferents of OPNs and those of other neurons whose somata lie in the same region. Thus, the major purpose of these experiments was to test directly whether the observed projections from the O P N region 8 arose from OPNs per se. To do this, we recorded OPNs in ketamine-anesthetized cats 3,6 and attempted to activate them by stimulating the cerebellar vermis and cervical spinal cord. 0006-8993/82/0000-0000/$02.75 © Elsevier Biomedical Press
A secondary objective was to investigate other regions for connections with OPNs. Since we had shown that cat OPNs are activated by visual stimuli (refs. l, 2), we placed stimulating electrodes on the optic chiasm. We also placed stimulating electrodes in the superior colliculus to test whether it might be the source of the visual input or, alternatively, a source for an inhibitory input that could trigger saccades. Finally, we placed stimulating electrodes on the vestibular nerves to test for direct inhibitory input that could act as the trigger for the fast phases of nystagmus. A preliminary report of these results has appeared 3. Fifteen adult male cats were anesthetized with i.m. injections of ketamine hydrochloride (45 rag/ kg) supplemented with continuous i.v. infusion of ketamine diluted in saline (10 mg/kg/h). All wound margins were dusted with long-lasting 10 ~ benzocaine powder. The cats were mounted in a stereotaxic apparatus on which the front stabilization was modified to allow the introduction of an eye-movement transducer. The transducer, a photo-diode that detected art infrared beam from a light-emitting diode affixed to the cornea, was sensitive to less than 0.1 ° of movement and was linear ( ± 3 ~ ) within 2~ 15° of the midposition. While the cats were in the prone position, stimulating electrodes were placed in the cerebellar vermis, the optic chiasm, and/or the superior colliculus. The
167 tungsten microelectrodes and conventional extracellular recording techniques. Following each experiment, the cat was killed with an overdose of Nembutal and perfused with saline followed by 10~o formalin. Marking lesions were made by the stimulating electrodes, and the locations of recording and stimulating electrodes were confirmed histologically. Sixty-nine OPNs were identified on the basis of their discharge patterns in relation to eye movements and their anatomical location. The upper portion of Fig. 1 illustrates the similarity of discharge patterns in alert (left) and ketamine-anesthetized (right) cats. Note that in both records the tonic discharge is unrelated to eye position but ceases abruptly for each saccadic eye movement. The lower half of Fig. 1 shows parasagittal sections of the reconstructed locations of the recording sites of the neurons pictured above and, in addition, illustrates the region over which OPNs could be recorded in the two paradigms. The two regions are very similar in rostro-caudal and dorso-ventral extent, although
vermal electrodes were placed visually in lobules 5 and 6 and positioned to evoke eye movements to electrical stimulation. The chiasm electrode was positioned to record the maximum flash-evoked potential. The bilateral collicular electrodes were placed to record either the flash- or chiasm-evoked responses and then fine-adjusted to produce eye movements when stimulating currents were applied. The cats were then rotated to the supine position to expose the ventral surface of the spinal cord and ponto-medullary brainstem. Bipolar stimulating electrodes were placed bilaterally in the ventral quadrants of the spinal cord at the C2 level to allow activation of tracts previously labeled in our autoradiographic material. Electrodes also were placed on both vestibular nerves via a ventral approach through the bullae. All electrodes were pairs of A g AgCI electrodes that could be positioned independently exce'l~t for the collicular electrodes, which had a concentr{c bipolar configuration. O P N discharge was recorded near the midline at the level of the exit of the abducens nerve using insulated iron-tipped
Im
iC!,m.,i n
fIN
I --,~,
": ~
Ii : I ,,... ~ -lrH ~'-
,~!',c',,~ ~5;,~i,~i~i~,,~ ~LL,~i;
i
16°11 .cls °
i
x, TB
mm
Fig. 1. Identification of omnipause neurons (OPNs). Upper: activity of OPNs recorded in an alert, trained cat (left) and in a ketamine-anesthetized cat (right) shows their similar discharge characteristics. Note that the anesthetized cat makes smaller spontaneous saccades and does not hold fixation. Lower: location of OPNs shown on parasagittal standard sections. Three marking lesions (Ieft) show the dorso-ventral extent of OPNs recorded on a single tract in an alert animal. This area coincides with the region where we recorded OPNs (right, hatched) in anesthetized cats. The black line is a lesion caused by an electrode in another experiment; the black dot is the site of the OPN recording above.
168 D
A
.
.
.
.
E 1 ms
B
F
Optic chiasm stimuiotion lOq Mean latency = 9.07 ± 141(sd) /
C
--r?
z
,
Q
2
,
4 6 8 10 12 LQtency (reset)
5 ms
Fig. 2. OPN responses to stimulation of the spinal cord (A) and optic chiasm (B-E). Three superimposed traces (A) show a consistent field response (first arrow) following stimulation (dot) of the spinal cord at the C2 level at current intensities just below threshold for limb twitches. The spontaneous action potential during one of the 3 trials (second arrow) shows that any response to cord stimulation would be easily distinguished. The response to optic chiasm stimulation is shown in 4 (D and E) or 5 (B and C) superimposed traces. Increasing current strength from threshold (B) to 1.5 × threshold (C) slightly reduced the latency of the response but did not make the response more secure; further increases in current strength did not alter the response. Using double (E) versus single (D) shock at maximal current intensities did not make the response more stable. F: latency histogram of the first action potential in the OPN following threshold stimulation of the optic chiasm. Calibration in C applies for B-E.
the mediaMateral extent seems to be reduced in the anesthetized preparationsl,S. None of the 17 OPNs tested for antidromic activation from the spinal cord responded following even supramaximal stimulation (Fig. 2A). The stimulation was effective because it: (1) evoked prominent fields in the O P N region (Fig. 2A); (2) could elicit short-latency antidromic responses from reticulo-spinal neurons recorded at the margins of the O P N region, and (3) often resulted in twitches of the limbs at high current intensities.
Stimulation of the vermis did not activate the 12 OPNs tested. Similarly, no response was elicited in 25 OPNs following ipsi- or contralateral vestibular stimulation, even at stimulus currents that were several times threshold for evoking a vestibular field potential and were often sufficient to produce movement of the globe. In contrast, stimulation of either the optic chiasm or the superior colliculus evoked a consistent response in OPNs. The response of 41/46 OPNs to chiasm stimulation is illustrated in Fig. 2B-E. To make the response to stimulation more clear, stimulation was triggered so that the response occurred during the interspike interval. The superimposed traces (Fig. 2B-E) show that stimulation produced a variable, long-latency excitation. Because both the occurrence of the response and its latency were variable, we could not tell whether there was, in addition, an initial inhibition and/or an inhibition following the excitation. The response efficacy was not improved either by increasing current strength from threshold (B) to 1.5 × threshold (C) (although the minimal latency was slightly reduced) or by using double (E) versus single (D) shock. A histogram of the latency from the threshold stimulus to the first extracellularly recorded action potential is shown in F. Fig. 3 shows the response of OPNs following stimulation of the superior colliculus. The response consists of an initial short-latency excitation followed by a longer-duration inhibition of the tonic discharge (Fig. 3B). The excitation has a variable latency (Fig. 3A; 3 superimposed trials, evoked action potentials indicated by downward arrows) at threshold stimulating currents and the duration of the inhibition is proportional to the number of stimuli (Fig. 3B). Effective collicular stimulation sites were always in the intermediate and deep layers (Fig. 3C). Collicular stimulation activated only 23 of 35 OPNs; the remaining 12 OPNs did not respond even at stimulating currents of 1 mA or more, which should have activated most of the superior colliculusl0. This study showed that OPNs do not project directly to the spinal cord or to the cerebellar vermis, nor do they receive direct afferents from those structures. This conclusion is consistent with the results of our control injections of tritiated
169
A
vestibular nerve stimulation resulted in strong, short-latency inhibition of O P N discharge as might be expected if these structures were the source of an inhibitory trigger to OPNs that initiates saccades. The initial response to collicular stimulation was excitatory rather than inhibitory, while there was no response at all to VN stimulation (cf. King et al.6,7). Although the excitatory response could not trigger saccades, it might have relayed a portion of the visual excitation of OPNs seen in alert cats1, 2 and confirmed by chiasm stimulation (Fig. 2) in this and other7, s studies. King et al. 7 have suggested, on the basis of lesion studies, that the visually induced excitation of OPNs 1,2 reaches them via both the cortex and the colliculus. Our own data 1 suggest that whatever the pathway, the excitation is not obviously important in oculomotor function. On the other hand, the inhibition of OPNs evoked by stimulation of the superior colliculus may be important in the generation of saccades. Longduration inhibition following collicular stimulation has been reported in alert monkeys ~2, but only when the stimulus also elicited a saccade. It was therefore impossible to determine whether the inhibition was caused by direct activation from the colliculus or was due merely to the concomitant occurrence of a saccade. However, in both the present study and in alert cats (Kaneko, Grarttyn and Fuchs, unpublished observations), we have produced OPN inhibition following cotlicular stimulation at stimulus intensities too small to elicit a saccade, suggesting that the superior colliculus has direct access to
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•••
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Fig. 3. Activation of OPNs following stimulation of superior colliculus (dots in B). A: 3 superimposed sweeps showing short-latency (1-2 ms) excitation (the positive peak of each action potential is indicated by a downward arrow). B: superimposed trials showing prolonged inhibition of lhe same OPN's tonic discharge following (top to bottom) two, three and four shocks to the colliculus. C: transverse section of the brainstem showing a marking lesion made at the end of the experiment. amino acids around, but not in, the OPN region, which suggested that cerebellar and cord projections were not from OPNs per se4,8. Another study 11, employing stimulation of the flocculus, showed that OPNs did not send axons to or receive afferents from the flocculus. We conclude that since OPNs project directly to areas that contain BNs but only indirectly to the cerebellum and spinal cord, OPNs probably subserve a strictly oculomotor function. This study also showed that neither collicular nor
1 Evinger, C., Kaneko, C. R. S. and Fuchs, A. F., The activity of omnipause neurons in alert cats during saccadic eye movements and visual stimuli, J. NeurophysioL, 47 (1982) 827-844. 2 Evinger, C., Kaneko, C. R. S., Johanson, G. W. and Fuchs, A. F., Omnipauser cells in the cat. In R. Baker and A. Berthoz (Eds.), Control of Gaze by Brain Stem Neurons,
OPNs. We gratefully acknowledge L. Pfeiffer for secretarial help, K. Schmitt for editorial assistance, P. Roberts and T. Nguyen for photography, and C. Ganders for care of the animals. This study was supported by Grants EY00096, EY00745, RR00166 from the National Institutes of Health.
Developments in Neuroseienee, VoL 1, Elsevier/North-
Holland, Amsterdam, 1977, pp. 337-348. 3 Kaneko, C. R. S. and Fuchs, A. F., Connections of feline omnipause neurons, Neurosci. Abstr., 4 (1978) 164. 4 Kaneko, C. R. S., Langer, T. P. and Graybiel, A. M., Efferent projections of the pontine oculomotor pauser region in the cat, Neurosci. Abstr., 5 (1979) 374.
170 5 Keller, E. L,, Participation of medial pontine reticular formation in eye movement generation in monkey, J. Neurophysiol., 37 (1974) 316-332. 6 King, W. M., Precht, W. and Dieringer, N., Connections of behaviorally identified cat omnipause neurons, Exp. Brain Res., 31 (1978) 435438. 7 King, W. M., Precht, W. and Dieringer, N., Afferent and efferent connections of cat omnipause neurons, Exp. Brain Res., 38 (1980) 395-403. 8 Langer, T. P. and Kaneko, C. R. S., Efferent projections of eat omnipause neurons, J. eomp. Neurol., submitted. 9 Luschei, E. S. and Fuchs, A. F., Activity of brain stem
neurons during eye movements of alert monkeys, aT. Neurophysiol., 35 (1972) 445M61. 10 McIlwain, J. T., Lateral spread of neural excitation during microstimulation in the intermediate gray layer of the cat's superior colliculus, J. Neurophysiol., 47 (1982) 167-178. 11 Nakao, S., Curthoys, I. S. and Markham, C. H., Eye movement related neurons in the cat pontine reticular formation: projection to the flocculus, Brain Research, 183 (1980) 291-299. 12 Raybourn, M. S. and Keller, E. L., Colliculoreticular organization in primate oculomotor system, J. Neurophysiol., 40 (1977) 861-878.