Afferent signals from cat extraocular muscles in the medial vestibular nucleus, the nucleus praepositus hypoglossi and adjacent brainstem structures

The responses of single units in the vestibular nuclei, nucleus praepositus hypoglossi and in the brainstem, deep and posterior to the abducens nucleus, were studied in anaesthetized, paralysed cats. Natural vestibular stimulation was provided by horizontal, sinusoidal oscillation of the animal and extraocular muscle afferents of the ipsilateral eye were activated either by passive eye-movement or by electrical stimulation of the inferior oblique branch of the oculomotor nerve in the orbit. Unit responses to vestibular and/or orbital stimuli were examined in sets of peristimulus time histograms interleaved in time. Of 127 units exposed to both types of stimulus, 40 (32%) responded only to vestibular input; 46 (32%) were affected only by the orbital afferent signal and 19 (15%) received both signals; the remaining 22 units (17%) were discarded because they had polymodal (usually somaesthetic) input. Of the 93 units whose recording sites were determined histologically, 24 were in the medial vestibular nucleus, 16 in the n. praepositus hypoglossi and 45 in the magnocellular nucleus of the reticular formation posterior and deep to the abducens nucleus. In these three nuclei 19 units in total were found which carried the orbital proprioceptive afferent signal and also responded to horizontal vestibular stimulation. The input from the eye muscles proved able to modify the vestibular response by adding excitation or inhibition or both. Effects of the orbital signal were generally phasic. About half of the units which responded to passive eye-movement showed statistically significant differences between their responses to horizontal and to vertical eye-movement. We have shown previously that signals from extraocular muscle proprioceptors reach the vestibulo-oculomotor system in an amphibian and a bony fish; the present experiments show that this is the case in a mammal also. The fact that the visual and visuomotor behaviour of these three species is very different suggests that the proprioceptive signal may play some rather fundamental role in the vestibulo-ocular system. The principal interest of the present results is that they demonstrate that units in the central vestibular system of the cat, in structures which are known to be concerned in oculomotor control, and particularly in the organization of horizontal eye-movement, receive an afferent signal from the eye muscles during passive eye-movement. These brainstem nuclei are known to receive various combinations of input from the vestibular and visual systems and of signals which represent neck movement and eye position and velocity.(ABSTRACT TRUNCATED AT 400 WORDS)     

Effects of afferent signals from the extraocular muscles upon units in the cerebellum, vestibular nuclear complex and oculomotor nucleus of the trout

The responses of single units in the cerebellum, the vestibular nuclear complex and adjacent regions of the brainstem and in the oculomotor nucleus were studied in decerebrate, paralysed rainbow trout (Salmo gairdneri). Natural vestibular stimulation was provided by horizontal, sinusoidal oscillation of the fish and extraocular muscle afferents of the eye ipsilateral to the recording were activated either by passive eye-movement or by electrical stimulation of the trochlear (IV) nerve in the orbit. Unit responses to vestibular and/or orbital stimuli were examined in peristimulus-time histograms interleaved in time. In the cerebellum and brainstem, of 124 units exposed to both types of stimulus, 26 (21%) responded only to vestibular input, 26 (21%) were affected only by the orbital signal and 23 (18%) received both signals. The remaining 49 units (39%) responded to mechanical stimulation of the head or body or to vibration; they were labelled "polymodal" and discarded. The recording sites of 56 units were verified by histology; 30 were in the cerebellum and 26 in the brainstem. Input from the eye muscles had excitatory or inhibitory effects upon the vestibular responses. The effects of the orbital signal were usually phasic but rare tonic responses also occurred. About half (15 of 34) of the units which responded to passive eye-movement showed statistically significant differences in the magnitude of their responses to horizontal and to vertical eye-movement. More units preferred horizontal movement (11) than preferred vertical passive eye-movement (four). Note that the plane of vestibular stimulation was always horizontal. In the region of the oculomotor nucleus, of 19 units, five (26%) gave vestibular responses only and three (16%) were affected only by the orbital signal; three units (16%) with polymodal responses were discarded. Of the eight units carrying both signals, histological confirmation that the recording site lay in the column of cells forming the oculomotor/trochlear nuclei was obtained in four. The responses and interactions were similar to those found in the brainstem. The results present two principal points of interest. 1. They reinforce the accumulating body of evidence that, in species with widely different oculomotor and visual behaviour, signals from extraocular muscle proprioceptors reach the vestibulo-ocular system; this, in turn, suggests that these signals may play some rather fundamental role in the oculomotor system.(ABSTRACT TRUNCATED AT 400 WORDS)     

Evidence for corrective effects of afferent signals from the extraocular muscles on single units in the pigeon vestibulo-oculomotor system

The role of extraocular muscle (EOM) afferent feedback signals in the control of eye movement is still controversial. We recorded from 106 single units in the vestibular nuclei, oculomotor nuclei and reticular formation of 80 decerebrate, paralysed pigeons. EOM afferents were stimulated by passive eye movement (PEM) during vestibular stimulation by sinusoidal oscillation in the horizontal plane. We found that EOM afferent signals profoundly modified the vestibular responses of 91 (86%) of the single units recorded. As well as using PEM to simulate eye movements similar to saccades, we moved the eye in a manner which mimicked the slow phase of the vestibulo-ocular reflex (artificial VOR, AVOR). We have found evidence that, as well as providing signals closely related to the parameters of eye movement, PEM alters the vestibular responses of cells during AVOR in a manner which suggests that EOM afferent signals may play a corrective role in the moment-to-moment control of eye movement in the vestibulo-ocular reflex.     

Directionally-specific effects of afferent signals from the extraocular muscles upon responses in the pigeon brainstem to horizontal vestibular stimulation

The responses of single units in the brainstem of the decerebrate, paralysed, pigeon were studied. Natural vestibular stimulation was provided by horizontal, sinusoidal, oscillation of the bird and extraocular muscle afferents of the ipsilateral eye were activated by passive eye-movement. Unit responses to vestibular and/or orbital stimuli were examined in sets of peristimulus time histograms interleaved in time. Of 352 units in the brainstem, in the region of the vestibular nuclei, which were exposed to the effects of both vestibular stimuli and passive eye-movement, 40 (11%) responded only to the latter; the other 312 units (89%) responded to vestibular stimulation at 0.4 Hz (amplitude +/- 8 degrees). Of these 312 units, 129 (41%) were affected only by vestibular stimuli; in the other 183 units (59%) passive eye-movement produced clear modification of the vestibular responses by adding excitation or inhibition, or both. There were phasic modifications in most units; in 77 there were longer-lasting changes in the vestibular responses, often following a phasic response. In 124 units whose responses were subjected to statistical analysis, the vestibular responses of 42 (34%) were modified only by horizontal eye-movement and eight (6%) were affected only by vertical movement. A further 18% showed larger effects from horizontal than from vertical eye-movement; in 2% vertical eye-movement was preferred. Further examination of the specificity of the effects of eye-movement in planes between the vertical and horizontal was possible in 29 units which showed various degrees of "tuning" of the effect. In some units there was additional specificity for eye-movement in (a) particular directions (towards the beak rather than towards the tail, for example); (b) in particular arcs of the orbit (centre-to-temporal rather than nasal-to-centre, for example). Note that all these effects were upon the responses of the units to horizontal vestibular stimulation. Thus, the modifications of the vestibular responses depended upon specific characteristics of the passive eye-movement. The exact recording sites of 29 units were determined histologically; some were in the medial vestibular nucleus but many were in the adjacent reticular formation. The principal interest of the results is that they provide more detailed information than was available previously on the specificity of the effects of afferent signals from the extraocular muscles upon the vestibular responses of units in regions of the brainstem known to be involved in oculomotor control. The decerebrate pigeon proves to be a particularly good preparation in which to study these effects.(ABSTRACT TRUNCATED AT 400 WORDS)     

Different neural strategies for multimodal integration: comparison of two macaque monkey species

The integration of neck proprioceptive and vestibular inputs underlies the generation of accurate postural and motor control. Recent studies have shown that central mechanisms underlying the integration of these sensory inputs differ across species. Notably, in rhesus monkey (Macaca mulata), an Old World monkey, neurons in the vestibular nuclei are insensitive to passive stimulation of neck proprioceptors. In contrast, in squirrel monkey, a New World monkey, stimulation produces robust modulation. This has led to the suggestion that there are differences in how sensory information is integrated during self-motion in Old versus New World monkeys. To test this hypothesis, we recorded from neurons in the vestibular nuclei of another species in the Macaca genus [i.e., M. fascicularis (cynomolgus monkey)]. Recordings were made from vestibular-only (VO) and position-vestibular-pause (PVP) neurons. The majority (53%) of neurons in both groups were sensitive to neck proprioceptive and vestibular stimulation during passive body-under-head and whole-body rotation, respectively. Furthermore, responses during passive rotations of the head-on-body were well predicted by the linear summation of vestibular and neck responses (which were typically antagonistic). During active head movement, the responses of VO and PVP neurons were further attenuated (relative to a model based on linear summation) for the duration of the active head movement or gaze shift, respectively. Taken together, our findings show that the brain’s strategy for the central processing of sensory information can vary even within a single genus. We suggest that similar divergence may be observed in other areas in which multimodal integration occurs. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Firing behavior of vestibular neurons during active and passive head movements: vestibulo-spinal and other non-eye-movement related neurons.

The firing behavior of 51 non-eye movement related central vestibular neurons that were sensitive to passive head rotation in the plane of the horizontal semicircular canal was studied in three squirrel monkeys whose heads were free to move in the horizontal plane. Unit sensitivity to active head movements during spontaneous gaze saccades was compared with sensitivity to passive head rotation. Most units (29/35 tested) were activated at monosynaptic latencies following electrical stimulation of the ipsilateral vestibular nerve. Nine were vestibulo-spinal units that were antidromically activated following electrical stimulation of the ventromedial funiculi of the spinal cord at C1. All of the units were less sensitive to active head movements than to passive whole body rotation. In the majority of cells (37/51, 73%), including all nine identified vestibulo-spinal units, the vestibular signals related to active head movements were canceled. The remaining units (n = 14, 27%) were sensitive to active head movements, but their responses were attenuated by 20-75%. Most units were nearly as sensitive to passive head-on-trunk rotation as they were to whole body rotation; this suggests that vestibular signals related to active head movements were cancelled primarily by subtraction of a head movement efference copy signal. The sensitivity of most units to passive whole body rotation was unchanged during gaze saccades. A fundamental feature of sensory processing is the ability to distinguish between self-generated and externally induced sensory events. Our observations suggest that the distinction is made at an early stage of processing in the vestibular system.     

Vestibular,auditory, and somatic input to the posterior thalamus of the cat

Summary The responses of 157 neural units in the magnocellular (mc) and parvocellular (pc) components of the medial geniculate nucleus (MG) and other nuclei of the posterior (PO) thalamic group were recorded and analyzed. Units were tested for a response to electrical stimulation of the vestibular nerve, natural auditory and electrical cochlear nerve stimulation, and natural stimulation of joint, muscle, and cutaneous receptors of the limbs, trunk, and neck (somatic stimulation). Only 45% of the units responded to these stimuli. Twenty-four percent of the responsive units were multimodal, responding to more than one stimulus. All multimodal units were activated by auditory stimuli. More units responding to vestibular stimulation were found in mcMG than in pcMG or other components of the PO group. Potentials evoked by vestibular nerve stimulation were recorded in all 3 regions with latencies of 5–25 msec. No evidence was found for a thalamic relay from vestibular nerve to cortex in the area investigated, since the recorded latency for activity from vestibular nerve stimulation was longer than the latency of responses recorded in the cortex. This region of the thalamus appears to be important for reception of auditory information and integration with vestibular and somatic modalities.This investigation was supported in part by USPHS Grant NS 11307     

Nystagmus induced by electrical stimulation of the vestibular and prepositus hypoglossi nuclei in the monkey: evidence for site of induction of velocity storage

Summary Electrical stimulation of the vestibular nuclei (VN) and prepositus hypoglossi nuclei (PPH) of alert cynomolgus monkeys evoked nystagmus and eye deviation while they were in darkness. At some sites in VN, nystagmus and after-nystagmus were induced with characteristics suggesting that velocity storage had been excited. We analyzed these responses and compared them to the slow component of optokinetic nystagmus (OKN) and to optokinetic after-nystagmus (OKAN). We then recorded unit activity in VN and determined which types of nystagmus would be evoked from the sites of recording. Nystagmus and eye deviations were also elicited by electrical stimulation of PPH, and we characterized the responses where unit activity was recorded in PPH. Horizontal slow phase velocity of the VN storage responses was contralateral to the side of stimulation. The rising time constants and peak steady-state velocities were similar to those of OKN, and the falling time constants of the after-nystagmus and of OKAN were approximately equal. Both the induced after-nystagmus and OKAN were habituated by stimulation of the VN. When horizontal after-nystagmus was evoked with animals on their sides, it developed yaw and pitch components that tended to shift the vector of the slow phase velocity toward the spatial vertical. Similar cross-coupling occurs for horizontal OKAN or for vestibular post-rotatory nystagmus elicited in tilted positions. Thus, the storage component of nystagmus induced by VN stimulation had the same characteristics as the slow component of OKN and the VOR. Positive stimulus sites for inducing nystagmus with typical storage components were located in rostral portions of VN. They lay in caudal ventral superior vestibular nucleus (SVN), dorsal portions of central medial vestibular nucleus (MVN) caudal to the abducens nuclei and in adjacent lateral vestibular nucleus (LVN). More complex stimulus responses, but with contralateral after-nystagmus, were induced from surrounding regions of ventral MVN and LVN, rostral descending vestibular nucleus and the marginal zone between MVN and PPH. Vestibular-only (VO), vestibular plus saccade (VPS) and tonic vestibular pause (TVP) units were identified by extracellular recording. Stimulation near type I lateral and vertical canalrelated VO units elicited typical storage responses with after-nystagmus in 23 of 29 tracks (79%). Stimulus responses were more complex from the region of neurons with oculomotor-related signals, i.e., TVP or VPS cells, although after-nystagmus was also elicited from these sites. Effects of vestibular nerve and nucleus stimulation were compared. Nerve stimulation evoked nystagmus with both a rapid and slow component and after-nystagmus. There was a more prominent rapid rise in slow phase velocity, higher peak velocities, shorter latencies and a shorter falling time constant from nerve than from nucleus stimulation. This indicates more prominent activation of rapid pathways from nerve stimulation. From a comparison of nerve- and nucleus-induced nystagmus, we infer that there was predominant activation of the network responsible for velocity storage by electrical stimulation at many sites in the VN. Microstimulation at sites in PPH elicited nystagmus with ipsilateral slow phases or ipsilateral eye deviations. Slow phase eye velocity changed rapidly at the onset of nystagmus, and peak eye velocities were about 10–15°/s lower than from VN stimulation. The nystagmus had no slow component, and it was not followed by after-nystagmus. Only burst or burst-tonic neurons were recorded in PPH. Stimulation at sites of recording of these units induced either nystagmus with a rapid component or ipsilateral eye deviation. We conclude that the slow component of optokinetic and vestibular nystagmus, attributable to velocity storage is produced in the VN, not in the PPH. We postulate that VO neurons lying in caudal ventral portions of SVN, dorsal portions of MVN and adjacent LVN are part of the network that generates velocity storage.     

Response of vestibular-nerve afferents to active and passive rotations under normal conditions and after unilateral labyrinthectomy

We investigated the possible contribution of signals carried by vestibular-nerve afferents to long-term processes of vestibular compensation after unilateral labyrinthectomy. Semicircular canal afferents were recorded from the contralesional nerve in three macaque monkeys before [horizontal (HC) = 67, anterior (AC) = 66, posterior (PC) = 50] and 1-12 mo after (HC = 192, AC = 86, PC = 57) lesion. Vestibular responses were evaluated using passive sinusoidal rotations with frequencies of 0.5-15 Hz (20-80 degrees /s) and fast whole-body rotations reaching velocities of 500 degrees /s. Sensitivities to nonvestibular inputs were tested by: 1) comparing responses during active and passive head movements, 2) rotating the body with the head held stationary to activate neck proprioceptors, and 3) encouraging head-restrained animals to attempt to make head movements that resulted in the production of neck torques of < or =2 Nm. Mean resting discharge rate before and after the lesion did not differ for the regular, D (dimorphic)-irregular, or C (calyx)-irregular afferents. In response to passive rotations, afferents showed no change in sensitivity and phase, inhibitory cutoff, and excitatory saturation after unilateral labyrinthectomy. Moreover, head sensitivities were similar during voluntary and passive head rotations and responses were not altered by neck proprioceptive or efference copy signals before or after the lesion. The only significant change was an increase in the proportion of C-irregular units postlesion, accompanied by a decrease in the proportion of regular afferents. Taken together, our findings show that changes in response properties of the vestibular afferent population are not likely to play a major role in the long-term changes associated with compensation after unilateral labyrinthectomy.     

Directional selectivity in the responses of units in cat primary visual cortex to passive eye movement

The responses of single units in the primary visual cortex (Area 17) of anaesthetized, paralysed cats, to passive movement of the ipsilateral eye were studied. Responses to passive eye movement were found in about one-third of the cortical units isolated. Appropriate control experiments excluded visual, auditory and cutaneous inputs as the source of the effective signal during passive eye movement. The magnitudes of the responses to a number (usually four) of radial directions of passive eye movement were estimated from sets of peristimulus time histograms "interleaved" in time. Units were defined as "radially selective" if the responses to movement along one radius (e.g. vertically upwards) exceeded that along at least one other orthogonal radius (e.g. horizontal-temporal). Of 60 units tested, 53 (88%) were "radially selective" according to this definition. Some of the "radially selective" units showed an additional type of specificity to passive eye movement: (a) Some units responded preferentially to movement along one of the arcs of passive eye movement which were tested (e.g. vertical movement above the equator of the orbit). These units we have called "arc selective". (b) Other units were sensitive to the direction of movement and preferred movement in a particular direction over more than one arc (e.g. horizontal movement towards the temporal side in both nasal and temporal halves of the orbit). These we have called "direction selective". Twenty-one "radially selective" units showed one of these additional properties, nine were arc selective and twelve were direction selective. The implications of these results for the understanding of the function of orbital proprioceptive signals in the cortex are discussed briefly. Responses to passive eye movement were found in all of layers II-VI in Area 17 and the implications of this for the understanding of the pathway by which orbital proprioceptive signals reach the primary visual cortex are discussed. The experiments have shown that many units in cat visual cortex respond to passive eye movement and that most of these units have some specificity for particular radial directions of movement while some have additional specific properties. We believe that these properties of radial, directional and arc sensitivity are likely to be important in understanding the function of the orbital proprioceptive signal which arises during eye movement and they are particularly interesting in relation to the findings of others that this proprioceptive signal appears to be concerned in the normal development of visual properties in the cortex and in the control of visually guided movement in adult cats.     

Neck proprioceptive inputs to primate vestibular nucleus neurons

The contribution of neck proprioceptive signals to signal processing in the vestibular nucleus was studied by recording responses of secondary horizontal canal-related neurons to neck rotation in the squirrel monkey. Responses evoked by passive neck rotation while the head was held stationary in space were compared with responses evoked by passive whole body rotation and by forced rotation of the head on the trunk. Most neurons (76%; 45/59) were sensitive to neck rotation. The nature and strength of neck proprioceptive inputs varied and usually combined linearly with vestibular inputs. In most cases (94%), the direction of the neck proprioceptive input was "antagonistic" or "reciprocal" with respect to vestibular sensitivity and, consequently, reduced the vestibular response during head-on-trunk rotation. Different types of vestibular neurons received different types of proprioceptive input. Neurons whose firing behavior was related to eye position (position-vestibular-pause neurons and position-vestibular neurons) were often sensitive to the position of the head with respect to the trunk. The sensitivity to head position was usually in the same direction as the neuron's eye position sensitivity. Non-eye-movement related neurons and eye-head-velocity neurons exhibited the strongest sensitivity to passive neck rotation and had signals that were best related to neck velocity. The results suggest that neck proprioceptive inputs play an important role in shaping the output of the primate vestibular nucleus and its contribution to posture, gaze and perception.     

Excitation of units in the lateral geniculate and contiguous nuclei of the cat by stretch of extrinsic ocular muscles

Summary In cats, anaesthetized with chloralose and paralysed, the responses of units in the right lateral thalamus were recorded while the extrinsic ocular muscles (EOM) of the right eye were stretched in the dark. Phasic responses were found in all layers of the dorsal lateral geniculate nucleus (LGNd) and in the perigeniculate nucleus (PGN). A given unit usually responded to stretch of more than one EOM and thus to more than one direction of rotation of the eye in the orbit. LGNd. Of a sample of 76 units in LGNd, 55 (72%) gave visual but no muscle responses and 21 (28%) responded to EOM stretch. In all, 40 units with EOM responses were examined and 25 of the 27 tested (93%) also had visual responses. Of the 40 units, 32 could be allocated to layers, thus: layer A, 8 (25%); layer A1, 20 (63%); layer B, 3 (9%); central interlaminar nucleus, 1 (3%). It is interesting that most of the EOM responses were found in layer A1 which receives the excitatory visual input from the eye whose EOM were stretched. Muscle responsive units occurred with ON- and OFF-centre visual responses of sustained and transient types. PGN. In PGN, 21 units gave EOM responses and most of them were also excited by visual input.The conclusion is that the LGNd and PGN recieve an extraretinal proprioceptive signal which should be present during at least large saccadic eye movements. The anatomical pathways which may be involved and the significance of the signal are discussed briefly.     

Second-order vestibular neurons form separate populations with different membrane and discharge properties

Membrane and discharge properties were determined in second-order vestibular neurons (2 degrees VN) in the isolated brain of grass frogs. 2 degrees VN were identified by monosynaptic excitatory postsynaptic potentials after separate electrical stimulation of the utricular nerve, the lagenar nerve, or individual semicircular canal nerves. 2 degrees VN were classified as vestibulo-ocular or -spinal neurons by the presence of antidromic spikes evoked by electrical stimulation of the spinal cord or the oculomotor nuclei. Differences in passive membrane properties, spike shape, and discharge pattern in response to current steps and ramp-like currents allowed a differentiation of frog 2 degrees VN into two separate, nonoverlapping types of vestibular neurons. A larger subgroup of 2 degrees VN (78%) was characterized by brief, high-frequency bursts of up to five spikes and the absence of a subsequent continuous discharge in response to positive current steps. In contrast, the smaller subgroup of 2 degrees VN (22%) exhibited a continuous discharge with moderate adaptation in response to positive current steps. The differences in the evoked spike discharge pattern were paralleled by differences in passive membrane properties and spike shapes. Despite these differences in membrane properties, both types, i.e., phasic and tonic 2 degrees VN, occupied similar anatomical locations and displayed similar afferent and efferent connectivities. Differences in response dynamics of the two types of 2 degrees VN match those of their pre- and postsynaptic neurons. The existence of distinct populations of 2 degrees VN that differ in response dynamics but not in the spatial organization of their afferent inputs and efferent connectivity to motor targets suggests that frog 2 degrees VN form one part of parallel vestibulomotor pathways.     

Behavior of horizontal semicircular canal afferents in alert monkey during vestibular and optokinetic stimulation

Summary The behavior of single vestibular nerve fibers from the lateral semicircular canal was recorded during sinusoidal oscillations of the head, during optokinetic stimulation with the head stationary, and during spontaneous oculomotor behavior in the alert monkey. The response of similar fibers to adequate vestibular stimulation was also studied in some of the animals under deeply anesthetized conditions. In the alert animals all units were spontaneously active and their discharge was modulated only by adequate vestibular stimulation. Ipsilateral horizontal rotations of the head were excitatory for all units. No modification of this basic vestibular response by visual stimulation including full-field striped drum rotation was observed. Furthermore no correlation of unit activity with oculomotor function including voluntary saccadic and pursuit eye movements was found in any of the units. The regularity of spontaneous discharge was the most consistent characteristic that differentiated the unit response into types. Most units were very regular in discharge, but a few were very irregular. The averaging of unit discharge over several cycles of oscillatory head rotation showed that the irregular type units were also consistently modulated by adequate vestibular stimulation. Both regular and irregular type units were found in the anesthetized animals. Unimodal distributions of the quantitative values for unit resting discharge rate, sensitivity, and phase relationship were found. The distributions for these three parameters were similar in the units recorded in the anesthetized animals. Thus at least these characteristics of semicircular canal response seem not to be affected by the vestibular efferent system which should be altered or eliminated in the case of the anesthetized animals.Research supported by NIH Grant EY0995-04.     

Neck proprioception compensates for age-related deterioration of vestibular self-motion perception

Vestibular functions are known to show some deterioration with age. Vestibular deterioration is often thought to be compensated for by an increase in neck proprioceptive gain. We studied this presumed compensatory mechanism by measuring psychophysical responses to vestibular (horizontal canal), neck and combined stimuli in 50 healthy human subjects as a function of age (range 15–76 years). After passive horizontal rotations of head and/or trunk (torso) in complete darkness (dominant frequencies 0.05, 0.1, and 0.4 Hz), subjects readjusted a visual target to its remembered prerotational location in space. (1) Vestibular-only stimulus (whole-body rotation); subjects' responses were shifted towards postrotatory body position, this only slightly at 0.4 Hz and pronounced at 0.1 and 0.05 Hz. These errors reflect the known physiological drop of vestibular gain at low rotational frequency. They exhibited a slight but significant increase with age. (2) Neck-only stimulus (trunk rotated, head stationary); the responses showed errors similar to those upon vestibular stimulation (with offset towards postrotatory trunk position) and this again slightly more with increasing age. (3) Vestibular-neck stimulus combination during head rotation on stationary trunk; the errors were close to zero, independent of stimulus frequency and the subjects' age. (4) Opposite stimulus combination (trunk rotated in the same direction as the head, but with double amplitude); the errors were clearly enhanced, essentially reflecting the sum of those with vestibular-only and neck-only stimulation. Taken together, we find a parallel increase in neck- and vestibular-related errors with age, in seeming contrast to previous studies. We explain our and the previous findings by a vestibular-neck interaction model in which two different neck signals are involved. One neck signal is used, in combination with the vestibular signal, for estimating trunk-in-space rotation. It is internally shaped to always match the vestibular signal, so that these two signals cancel each other out when summed during head rotation on stationary trunk. Because of this matching, perceived trunk stationariness during head rotation on the stationary trunk is independent of vestibular deterioration (related to stimulus frequency, age, ototoxic medication, etc.). The other neck proprioceptive signal, coding head-on-trunk rotation, is superimposed on the estimate of trunk-in-space rotation, thereby yielding a notion of head-in-space. This neck signal remains essentially unchanged with vestibular deterioration. Generally, we hold that the transformation of the vestibular signal from the head down to the trunk proceeds further to include the hip and the legs as well as the haptically perceived body support surface; by this, subjects yield a notion of support kinematics in space. As a consequence, spatial orientation is impaired by chronic vestibular deterioration only to the extent that the body support is moving in space, while it is unimpaired (determined by proprioception alone) during body motion with respect to a stationary support. Electronic Publication     

Patterns of canal and otolith afferent input convergence in frog second-order vestibular neurons

Second-order vestibular neurons (2 degrees VN) were identified in the isolated frog brain by the presence of monosynaptic excitatory postsynaptic potentials (EPSPs) after separate electrical stimulation of individual vestibular nerve branches. Combinations of one macular and the three semicircular canal nerve branches or combinations of two macular nerve branches were stimulated separately in different sets of experiments. Monosynaptic EPSPs evoked from the utricle or from the lagena converged with monosynaptic EPSPs from one of the three semicircular canal organs in ~30% of 2 degrees VN. Utricular afferent signals converged predominantly with horizontal canal afferent signals (74%), and lagenar afferent signals converged with anterior vertical (63%) or posterior vertical (37%) but not with horizontal canal afferent signals. This convergence pattern correlates with the coactivation of particular combinations of canal and otolith organs during natural head movements. A convergence of afferent saccular and canal signals was restricted to very few 2 degrees VN (3%). In contrast to the considerable number of 2 degrees VN that received an afferent input from the utricle or the lagena as well as from one of the three canal nerves (~30%), smaller numbers of 2 degrees VN (14% of each type of 2 degrees otolith or 2 degrees canal neuron) received an afferent input from only one particular otolith organ or from only one particular semicircular canal organ. Even fewer 2 degrees VN received an afferent input from more than one semicircular canal or from more than one otolith nerve (~7% each). Among 2 degrees VN with afferent inputs from more than one otolith nerve, an afferent saccular nerve input was particularly rare (4-5%). The restricted convergence of afferent saccular inputs with other afferent otolith or canal inputs as well as the termination pattern of saccular afferent fibers are compatible with a substrate vibration sensitivity of this otolith organ in frog. The ascending and/or descending projections of identified 2 degrees VN were determined by the presence of antidromic spikes. 2 degrees VN mediating afferent utricular and/or semicircular canal nerve signals had ascending and/or descending axons. 2 degrees VN mediating afferent lagenar or saccular nerve signals had descending but no ascending axons. The latter result is consistent with the absence of short-latency macular signals on extraocular motoneurons during vertical linear acceleration. Comparison of data from frog and cat demonstrated the presence of a similar organization pattern of maculo- and canal-ocular reflexes in both species.     

Integration of vestibular and head movement signals in the vestibular nuclei during whole-body rotation.

Single-unit recordings were obtained from 107 horizontal semicircular canal-related central vestibular neurons in three alert squirrel monkeys during passive sinusoidal whole-body rotation (WBR) while the head was free to move in the yaw plane (2.3 Hz, 20 degrees /s). Most of the units were identified as secondary vestibular neurons by electrical stimulation of the ipsilateral vestibular nerve (61/80 tested). Both non-eye-movement (n = 52) and eye-movement-related (n = 55) units were studied. Unit responses recorded when the head was free to move were compared with responses recorded when the head was restrained from moving. WBR in the absence of a visual target evoked a compensatory vestibulocollic reflex (VCR) that effectively reduced the head velocity in space by an average of 33 +/- 14%. In 73 units, the compensatory head movements were sufficiently large to permit the effect of the VCR on vestibular signal processing to be assessed quantitatively. The VCR affected the rotational responses of different vestibular neurons in different ways. Approximately one-half of the units (34/73, 47%) had responses that decreased as head velocity decreased. However, the responses of many other units (24/73) showed little change. These cells had signals that were better correlated with trunk velocity than with head velocity. The remaining units had responses that were significantly larger (15/73, 21%) when the VCR produced a decrease in head velocity. Eye-movement-related units tended to have rotational responses that were correlated with head velocity. On the other hand, non-eye-movement units tended to have rotational responses that were better correlated with trunk velocity. We conclude that sensory vestibular signals are transformed from head-in-space coordinates to trunk-in-space coordinates on many secondary vestibular neurons in the vestibular nuclei by the addition of inputs related to head rotation on the trunk. This coordinate transformation is presumably important for controlling postural reflexes and constructing a central percept of body orientation and movement in space.     

Two groups of secondary vestibular neurons mediating horizontal canal signals, probably to the ipsilateral medial rectus muscle, under inhibitory influences from the cerebellar flocculus in rabbits

Vestibular nuclear neurons that mediate horizontal canal signals to the ipsilateral medial rectus motoneurons were explored in anesthetized and decerebrate rabbits. These neurons were identified by four criteria: (1) they were activated monosynaptically by ipsilateral vestibular nerve stimulation and (2) antidromically from the oculomotor nucleus region, while they were inhibited by (3) direct floccular stimulation and (4) ipsilateral retinal stimulation that activated floccular Purkinje cells via a climbing fiber afferent pathway. Neurons fulfilling these criteria were found in two anatomically different regions, i.e. the rostrolateral part of the medial vestibular nucleus and in the ventral part of the lateral vestibular nucleus. In decerebrate rabbits, neurons in both loci responded to horizontal rotation of the whole body with the type I pattern (excited by ipsilateral rotation). These results suggest that horizontal canal signals are conveyed to ipsilateral medial rectus motoneurons by two separate groups of vestibular nuclear neurons which may play different roles in the vestibulo-ocular reflex.     

Differential inhibitory control of semicircular canal nerve afferent-evoked inputs in second-order vestibular neurons by glycinergic and GABAergic circuits

Labyrinthine nerve-evoked monosynaptic excitatory postsynaptic potentials (EPSPs) in second-order vestibular neurons (2°VN) sum with disynaptic inhibitory postsynaptic potentials (IPSPs) that originate from the thickest afferent fibers of the same nerve branch and are mediated by neurons in the ipsilateral vestibular nucleus. Pharmacological properties of the inhibition and the interaction with the afferent excitation were studied by recording monosynaptic responses of phasic and tonic 2°VN in an isolated frog brain after electrical stimulation of individual semicircular canal nerves. Specific transmitter antagonists revealed glycine and GABA_A receptor-mediated IPSPs with a disynaptic onset only in phasic but not in tonic 2°VN. Compared with GABAergic IPSPs, glycinergic responses in phasic 2°VN have larger amplitudes and a longer duration and reduce early and late components of the afferent nerve-evoked subthreshold activation and spike discharge. The difference in profile of the disynaptic glycinergic and GABAergic inhibition is compatible with the larger number of glycinergic as opposed to GABAergic terminal-like structures on 2°VN. The increase in monosynaptic excitation after a block of the disynaptic inhibition in phasic 2°VN is in part mediated by a N-methyl-D-aspartate receptor-activated component. Although inhibitory inputs were superimposed on monosynaptic EPSPs in tonic 2°VN as well, the much longer latency of these IPSPs excludes a control by short-latency inhibitory feed-forward side-loops as observed in phasic 2°VN. The differential synaptic organization of the inhibitory control of labyrinthine afferent signals in phasic and tonic 2°VN is consistent with the different intrinsic signal processing modes of the two neuronal types and suggests a co-adaptation of intrinsic membrane properties and emerging network properties.     

Does orbital proprioception contribute to gaze stability during translation?

Translational motion induces retinal image slip which varies with object distance. The brain must know binocular eye position in real time in order to scale eye movements so as to minimize retinal slip. Two potential sources of eye position information are orbital proprioception and an internal representation of eye position derived from central ocular motor signals. To examine the role of orbital proprioceptive information, the position of the left eye was perturbed by microstimulation of the left abducens nerve during translational motion to the right or left along the interaural axis in two rhesus macaques. Microstimulation rotated the eye laterally, activating eye muscle proprioceptors, while keeping central motor commands undisturbed. We found that microstimulation-induced eye position changes did not affect the translational VOR in the abductive (lateral rectus) direction, but it did influence the responses in the adductive (medial rectus) direction. Our findings demonstrate that proprioceptive inputs appear to be involved in the TVOR responses at least during ipsilateral head movements and proprioceptive influences on the TVOR may involve vergence-related signals to the oculomotor nucleus. However, internal representation of eye position, derived from central ocular motor signals, likely plays the dominant role in providing eye position information for scaling eye movements during translational motion, particularly in the abducent direction.