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Notes: Summary Responses of neck motoneurons to electrical stimulation of the pontomedullary reticular formation were recorded intracellularly in cerebellectomized cats anesthetized with chloralose. Stimulation of nucleus reticularis (n.r.) ventralis and the dorsal part of n.r. gigantocellularis evoked short latency, monosynaptic inhibitory postsynaptic potentials (IPSPs) in the majority of motoneurons supplying the ipsilateral splenius, biventer cervicis and complexus muscles and in 25% of motoneurons projecting in the ipsilateral spinal accessory nerve. Monosynaptic IPSPs were also evoked by stimulating the medial longitudinal fasciculus (MLF) but lesion and collision experiments indicated that these IPSPs were independent of those evoked by reticular stimulation. Monosynaptic IPSPs were also occasionally observed following stimulation of the contralateral reticular formation, especially of the dorsal part of n.r. gigantocellularis. Monosynaptic excitatory postsynaptic potentials (EPSPs) were evoked in all classes of neck motoneurons studied by stimulation of n.r. pontis caudalis, gigantocellularis and ventralis. Each reticular nucleus appeared to contribute to this excitation. The excitation was bilateral but large monosynaptic EPSPs were most often seen in motoneurons ipsilateral to the stimulus site. Data indicated that pontine EPSPs were mediated by ventromedial reticulospinal fibers while medullary EPSPs were mediated by ventrolateral reticulospinal fibers. Neck motoneurons thus receive at least three distinct direct reticulospinal inputs, two excitatory and one inhibitory.

Notes: Summary Responses of motoneurons supplying muscles of the forelimbs, hindlimbs, back, and neck to stimulation of the medial pontomedullary reticular formation were studied with intracellular recording in cere-bellectomized cats under chloralose anesthesia. Stimulation of the midline or of a reticular region consisting of nucleus reticularis (n.r.) pontis caudalis and the dorsorostral part of n.r. gigantocellularis produced monosynaptic excitation of ipsilateral motoneurons supplying axial muscles and flexor and extensor muscles in both proximal and distal parts of the limbs. This widespread excitation appears to have been produced by rapidly conducting medial reticulospinal fibers. Stimulation of a second region consisting of n.r. ventralis and the ventrocaudal part of n. r. gigantocellularis produced monosynaptic excitation of ipsilateral neck and back motoneurons but only longer latency, apparently multisynaptic excitation of limb motoneurons. Collision tests indicated that this monosynaptic excitation did not involve fibers descending along the midline. It therefore appears to have been produced by lateral reticulospinal fibers. Reticular stimulation also produced short latency, monosynaptic inhibition of neck motoneurons, long latency, apparently polysynaptic inhibition of limb motoneurons and intermediate latency inhibition of back motoneurons. The latencies and properties of inhibitory responses of back motoneurons indicated that they were produced either disynaptically by fast fibers or monosynaptically by slower fibers. The data indicate that the medial pontomedullary reticular formation can be divided into a number of different zones each with a distinct pattern of connections with somatic motoneurons. These include the dorsorostrally located medial reticulospinal projection area, from which direct excitation of a wide variety of motoneurons can be evoked, the ventrocaudally located lateral reticulospinal projection area from which direct excitation of neck and back and direct inhibition of neck motoneurons can be evoked and the dorsal strip of n.r. gigantocellularis which has direct excitatory and inhibitory actions only on neck motoneurons.

Notes: Summary 1. Interstitiospinal neurons were activated by antidromic stimulation of the ventromedial funiculus of the spinal cord at C1 and C4 in cerebellectomized cats under chloralose anesthesia. 46% of these neurons responded only at C1 (N cells) and the remaining 54% responded at C4 also (D cells). There is no topographical difference in the location of N and D cells. Conduction velocities of N cells were significantly slower than those of D cells. 2. Stimulation of the contralateral whole vestibular nerve evoked firing of 31% of both N and D cells; some responded early enough to suggest disynaptic connections, many responded late. Stimulation of the ipsilateral whole vestibular nerve evoked firing of several cells, one spontaneously discharging D cell was inhibited. 3. Stimulation of the contralateral individual semicircular canal nerves evoked firing of 33% of N cells and 13% of D cells. Most of these responses were late. N cells responded not only to the vertical canals but also to the horizontal canal, whereas D cells responded to the horizontal canal, but seldom to the vertical ones. Most canal responding neurons received specific input, only two N cells received convergent input from both the anterior and horizontal canals. Stimulation of the ipsilateral canals did not evoke excitation of any cells tested; one D cell was inhibited by stimulation of the horizontal canal nerve. 4. Stimulation of the rostral medial vestibular nucleus evoked characteristic negative field potentials centered in the contralateral interstitial nucleus of Cajal (INC). Approximately 60% of both N and D cells received excitation from the contralateral vestibular nuclei. About 17% of these responding neurons received monosynaptic excitation, most frequently from the rostral medial nucleus. Stimulation of the ipsilateral vestibular nuclei evoked firing of 12% of both N and D cells. 5. Twenty-nine neurons were fired antidromically by weak stimuli applied to the ipsilateral vestibular nuclei. Twenty-seven of the 29 were activated only from C1 and were found in the INC (10 cells) and in the reticular formation dorsal to the INC (19 cells). Measurement of the spread of the effect of stimulus current and comparison of latencies to stimulation of the vestibular nuclei and C1 indicated that these neurons have axon collaterals going to the ipsilateral vestibular nuclei. Only one of them received excitation from the contralateral posterior canal, others did not respond to the labyrinth. Some were activated by stimulation of the vestibular nuclei.

Notes: Summary 1. Maximal activation directions of vertical burst-tonic and tonic neurons in the region of the interstitial nucleus of Cajal (INC) were examined in alert cats during vertical vestibulo-ocular reflex induced by sinusoidal rotation (at 0.11 Hz±10 deg, or 0.31 Hz±5 deg) in a variety of vertical planes using a null point analysis. The results were compared with the angles of anatomical and functional planes of vertical canals reported by Blanks et al. (1972) and Robinson (1982), and with the angles of vertical eye muscles measured in this study and by Ezure and Graf (1984). 2. Maximal activation directions of 23 cells (21 burst-tonic and 2 tonic neurons) were determined from their responses during rotation in 4 or more different vertical planes. All cells showed sinusoidal gain curves and virtually constant phase values except near the null regions, suggesting that their responses were evoked primarily by canal inputs. Phase values of 5 cells near the null regions depended on the rotation plane, suggesting additional otolith inputs. We used a measurement error range of ±10 deg for calculating the maximal activation directions from the null regions of individual cells and the values of error ranges of null calculation. Of the 23, the maximal activation directions of 7 cells were outside the measurement error ranges of vertical eye muscle angles and within the ranges of vertical canal angles (class A), those of 5 cells were within the ranges of eye muscle angles and outside the ranges of vertical canal angles (class B), and those of the remaining 11 cells were in the overlapping ranges for both angles (class C). Even if only the cells in which 5 or more measurement points were taken to determine maximal activation directions (n = 15), the results were similar. During vertical rotation with the head orientation +60 deg off the pitch plane, dissociation of cell activity and vertical compensatory eye movement was observed in 5 cells in class A or C that had null angles near +45 deg. These results suggest that the cells in class A and B carried individual vertical canal and oculomotor signals, respectively, although it is difficult to tell for the majority of cells (class C) which signals they reflected. Some cells in class A and C were antidromically activated from the medial longitudinal fasciculus at the level of abducens nucleus, suggesting that the signals carried by these cells may be sent to the lower brainstem. 3. Most burst-tonic neurons did not respond to horizontal rotation; significant responses were obtained in only 3 of 10 cells tested for which the gain was only 14–17% of their maximal vertical gain. There was no clear difference in gain or phase values of the responses to vertical rotation, or in eye position sensitivity (during spontaneous saccades) between cells whose responses coincided with individual vertical canal angles and those matching the angles of vertical recti muscles. The values of phase lag (re head acceleration during pitch rotation) and eye position sensitivity of these cells are still smaller compared to those of extraocular motoneurons reported by Delgado-Garcia et al. (1986), although they were larger than those of secondary vestibulo-ocular neurons (Perlmutter et al. 1988). All these results suggest that the signals carried by burst-tonic and tonic neurons in the INC region are different from oculomotor signals. 4. Similar analysis was done for comparison for 19 other cells that did not show close correlation with spontaneous eye movement but whose activity was clearly modulated by pitch rotation (pitch cells). More than a half (10/19) had maximal activation directions outside the measurement error ranges of individual vertical canal angles, and many shifted towards roll. Horizontal rotation produced responses with higher gain than burst-tonic neurons, suggesting a difference in the spatial response properties of burst-tonic and tonic neurons on one hand and pitch cells on the other.

Notes: Summary (1) Discharge characteristics of neurons in the region of the interstitial nucleus of Cajal (INC) were studied in alert cats during spontaneous or visually induced eye movement and sinusoidal vertical (pitch) rotation. Activity of a majority of cells (n = 68) was closely related to vertical eye position with or without bursting activity during on-direction saccades. They were called vertical burst-tonic (n = 62) and tonic (n = 6) neurons. Mean discharge rates for individual cells when the eye was near the primary position ranged from 35 to 133 (mean 75) spikes/s with a coefficient of variation (CV) ranging from 0.04 to 0.29 (mean 0.15). Average rate position curves were linear for the great majority of these cells with a mean slope of 3.9 ± 1.2 SD spikes/s/deg. (2) The burst index was defined as the difference in discharge rate between maximal rate during an on-direction saccade and the tonic rate after the saccade. The values of mean burst index for individual cells ranged from 8 to 352 (mean 135) spikes/s. Tonic neurons had a burst index lower than 60 spikes/s and were distributed in the lower end of the continuous histogram, suggesting that burst-tonic and tonic neurons may be a continuous group with varying degrees of burst components. During off-direction saccades, a pause was not always observed, although discharge rate consistently decreased and pauses were seen when saccades were made further in the off-direction toward recruitment thresholds. Significant positive correlation was observed between average discharge rate during off- as well as on-direction saccades and tonic discharge rate after saccades for individual cells, which was not due to cats making saccades mainly from the primary position. (3) During pitch rotation at 0.11 Hz (±10 deg), burst-tonic and tonic neurons had mean phase lag and gain of 128 (±13 SD) deg and 4.2 (±1.7 SD) spikes/s/deg/s2 relative to head acceleration. During pitch rotation of a wide frequency range (0.044–0.495 Hz), the values of phase lag were mostly constant (120–140 deg), while simultaneously recorded vertical VOR showed the mean phase lag of 178 deg. Vertical eye position sensitivity and pitch gain (re head position) showed significant positive correlation. (4) Comparison of the discharge characteristics of vertical burst-tonic and tonic neurons with those of secondary vestibulo-ocular neurons (Perlmutter et al. 1988) and extraocular motoneurons (Delgado-Garcia et al. 1986) in alert cats suggests that signals carried by burst-tonic and tonic neurons are partially processed signals in vertical VOR and saccades, and different from oculomotor signals. (5) The INC region also contained many cells that did not belong to the above groups but whose activity was clearly modulated by pitch rotation (called pitch cells for the present study, n = 44). Many (n = 23) showed some correlation with vestibular quick phases, and some (n = 12) with visually elicited eye movement, although they showed significantly lower and more irregular discharge rates than burst-tonic and tonic neurons (mean discharge rate when the eye was near the primary position 34, range 3–91, spikes/s; mean CV 0.61, range 0.15–1.7). During pitch rotation they showed the mean phase lag and gain of 119(±26 SD) deg and 3.2(±2.1 SD) spikes/s/deg/s2. Some cells showed a much lower phase lag of about 90 deg. (6) More than half the burst-tonic, tonic and pitch cells tested were antidromically activated by stimuli applied to the ponto-medullary medial longitudinal fasciculus at the level of abducens nucleus, while none of them were activated from the inferior olive, suggesting that vertical eye position signals carried by some burst-tonic and tonic neurons are carried to the lower brainstem.

Notes: Summary Second-order vestibular nucleus neurons which were antidromically activated from the region of the oculomotor nucleus (second-order vestibuloocular relay neurons) were studied in alert cats during whole-body rotations in many horizontal and vertical planes. Sinusoidal rotation elicited sinusoidal modulation of firing rates except during rotation in a clearly defined null plane. Response gain (spikes/s/deg/s) varied as a cosine function of the orientation of the cat with respect to a horizontal rotation axis, and phases were near that of head velocity, suggesting linear summation of canal inputs. A maximum activation direction (MAD) was calculated for each cell to represent the axis of rotation in three-dimensional space for which the cell responded maximally. Second-order vestibuloocular neurons divided into 3 non-overlapping populations of MADs, indicating primary canal input from either anterior, posterior, or horizontal semicircular canal (AC, PC, HC cells). 80/84 neurons received primary canal input from ipsilateral vertical canals. Of these, at least 6 received input from more than one vertical canal, suggested by MAD azimuths which were sufficiently misaligned with their primary canal. In addition, 21/80 received convergent input from a horizontal canal, with about equal number of type I and type II yaw responses. 4/84 neurons were HC cells; all of them received convergent input from at least one vertical canal. Activity of many vertical second-order vestibuloocular neurons was also related to vertical and/or horizontal eye position. All AC and PC cells that had vertical eye position sensitivity had upward and downward on-directions, respectively. A number of PC cells had MADs centered around the MAD of the superior oblique muscle, and 2/3 AC cells recorded in the superior vestibular nucleus had MADs near that of the inferior oblique. Thus, signals with spatial properties appropriate to activate oblique eye muscles are present at the second-order vestibular neuron level. In contrast, none of the second-order vestibuloocular neurons had MADs near those of the superior or inferior rectus muscles. Signals appropriate to activate these eye muscles might be produced by combining signals from ipsilateral and contralateral AC neurons (for superior rectus) or PC neurons (for inferior rectus). Alternatively, less direct pathways such as those involving third or higher order vestibular or interstitial nucleus of Cajal neurons might play a crucial role in the spatial transformations between semicircular canals and vertical rectus eye muscles.

Notes: Summary Interstitiospinal neurons were activated by antidromic stimulation of the spinal cord ventromedial funiculus at C1 and C4 in cerebellectomized cats under chlor alose anesthesia. Neurons responding only to C1 were classified as N cells and those responding both to C1 and C4 were classified as D cells, as in previous experiments (Fukushima et al. 1980a). Vestibular branching interstitiospinal and reticulospinal neurons were also identified as in the previous experiments. Stimulation of the ipsilateral pericruciate cortex evoked firing in 31% of N cells, 41% of D cells and 35% of vestibular branching neurons, while stimulation of the contralateral cortex excited 6% of N cells, 29% of D cells and 14% of vestibular branching neurons. Response latencies ranged from 2 to 15 ms after the effective pulse. By measuring the thresholds of activation of these neurons while changing the depth of the stimulating electrodes, and by mapping the cortical areas, it was shown that the lowest threshold areas were in the frontal eye fields and the anterior sigmoid gyrus near the presylvian sulcus (Area 6). Stimulation of the latter area often evoked neck or shoulder muscle contraction. Stimulation in the deep layers of the ipsilateral superior colliculus evoked firing in about 20% of interstitiospinal neurons and about 42% of vestibular branching neurons, with typical latencies 2–3 ms after the effective pulse, while stimulation of the contralateral superior colliculus was rarely effective. N cells and D cells responded similarly. Thresholds for activation were high in the intermediate tectal layers and declined as the electrodes entered the underlying tegmentum. This suggests that the superior colliculus is not the main source of synaptic inputs to these neurons. Low threshold points were found above the deep fiber layer when stimulating electrodes were inserted into the pretectum. Stimulation of the C2 biventer cervicis nerve excited about 8% of N cells, 18% of D cells, and 15% of vestibular branching neurons bilaterally with typical latencies around 10 ms. Similar results were obtained when C2 splenius nerves were stimulated. The fibers responsible for such excitation are probably group II, since stimuli stronger than 1.8 times threshold of the lowest threshold fibers were needed to evoke excitation. Response decrement was often observed when stimuli were repeated at 1/s, while no such decrement was observed at the rate of 1/3 s. When the convergence of cortical and labyrinthine excitatory inputs was studied, 36% of interstitiospinal neurons received single inputs either from the pericruciate cortex or from the labyrinth, 22% of neurons received convergent excitation from both and the remaining 42% did not respond to either stimulus. Although vestibular branching neurons rarely received labyrinthine inputs, they frequently showed convergence of excitation to stimulation of the frontal cortex, superior colliculus and vestibular nuclei.