Spatio-temporal convergence (STC) in otolith neurons

It has been recently demonstrated that some primary otolith afferents and most otolith-related vestibular nuclei neurons encode two spatial dimensions that can be described by two vectors in temporal and spatial quadrature. These cells are called broadly-tuned neurons. They are characterized by a non-zero tuning ratio which is defined as the ratio of the minimum over the maximum sensitivity of the neuron. Broadly-tuned neurons exhibit response gains that do not vary according to the cosine of the angle between the stimulus direction and the cell's maximum sensitivity vector and response phase values that depend on stimulus orientation. These responses were observed during stimulation with pure linear acceleration and can be explained by spatio-temporal convergence (STC) of primary otolith afferents and/or otolith hair cells. Simulations of STC of the inputs to primary otolith afferents and vestibular nuclei neurons have revealed interesting characteristics: First, in the case of two narrowly-tuned input signals, the largest tuning ratio is achieved when the input signals are of equal gain. The smaller the phase difference between the input vectors, the larger the orientation differences that are required to produce a certain tuning ratio. Orientation and temporal phase differences of 30–40° create tuning ratios of approximately 0.10–0.15 in target neurons. Second, in the case of multiple input signals, the larger the number of converging inputs, the smaller the tuning ratio of the target neuron. The tuning ratio depends on the number of input units, as long as there are not more than about 10. For more than 10–20 input vectors, the tuning ratio becomes almost independent of the number of inputs. Further, if the inputs comprise two populations (with different gain and phase values at a given stimulus frequency), the largest tuning ratio is obtained when the larger population has a smaller gain. These findings are discussed in the context of known anatomical and physiological characteristics of innervation patterns of primary otolith afferents and their possible convergence onto vestibular nuclei neurons.     

Purkinje cells in posterior cerebellar vermis encode motion in an inertial reference frame

The ability to orient and navigate through the terrestrial environment represents a computational challenge common to all vertebrates. It arises because motion sensors in the inner ear, the otolith organs, and the semicircular canals transduce self-motion in an egocentric reference frame. As a result, vestibular afferent information reaching the brain is inappropriate for coding our own motion and orientation relative to the outside world. Here we show that cerebellar cortical neuron activity in vermal lobules 9 and 10 reflects the critical computations of transforming head-centered vestibular afferent information into earth-referenced self-motion and spatial orientation signals. Unlike vestibular and deep cerebellar nuclei neurons, where a mixture of responses was observed, Purkinje cells represent a homogeneous population that encodes inertial motion. They carry the earth-horizontal component of a spatially transformed and temporally integrated rotation signal from the semicircular canals, which is critical for computing head attitude, thus isolating inertial linear accelerations during navigation.     

Activity of premotor vestibular neurons in the alert cat

The activity of medial vestibular nucleus neurons projecting to the contralateral abducens nucleus (premotor vestibular neurons) has been recorded during spontaneous and vestibular induced eye movements in the alert cat. Recorded neurons were identified by their antidromic activation from the abducens nucleus and by the post-synaptic field potential induced in this nucleus. The activity of identified medial vestibular neurons increased significantly with horizontal eye position and velocity toward the contralateral side, and decreased abruptly during ipsilateral saccades. The activity of these neurons was also related to head velocity toward the ipsilateral side. The functional role and origin of eye position and velocity signals present in these vestibular neurons are discussed.     

Otolith and semicircular canal inputs to single vestibular neurons in cats.

Researchers studied the convergence of the vertical posterior semicircular canal (PC), saccular nerves (SAC), utricular nerves (UT), and horizontal semicircular canal nerves (HC) on single vestibular neurons. The vestibular neurons were categorized by their innervating targets. Vestibular neurons were classified as vestibulospinal proper neurons (VS), vestibulo-ocular proper neurons (VO), vestibulo-oculo-spinal neurons sending axon collaterals to the extraocular motoneuron pools and spinal cord (VOS), and vestibular nucleus neurons without axons to the oculomotor nuclei or the spinal cord (V). Results indicate that the percentage of convergence of VS neurons was higher that that of neurons sending axons to the oculomotor nuclei (VO and VOS). They conclude that the convergence of canal and otolith inputs likely contributes mainly to vestibulospinal reflexes by sending inputs to the neck and other muscles during head inclination, which creates the combined stimuli of angular and linear acceleration.     

Bilateral distribution of vagal motor and sensory nerve fibers in the rat's lungs and airways

This study combined single and transneuronal labeling to define the origin of midline-crossing vagal fibers projecting to the rat's lungs. Injections of the beta-subunit of cholera toxin (CT-beta) into the lungs labeled similar numbers of neuronal somata in the nucleus ambiguus and dorsal motor nucleus of the vagus on both sides of the medulla, even though vagal stimulation increased lung resistance 50% less in the contralateral than in the ipsilateral lung. Unilateral cervical vagotomy prevented CT-beta labeling of ipsilateral neuronal somata and sensory fibers, indicating that lung-bound vagal fibers undergo decussation only inside the thorax. Injections of CT-beta and FluoroGold into opposite main stem bronchi double labeled 30% and 11% of all neuronal somata immunoreactive for CT-beta and FluoroGold, respectively, showing that one single vagal motoneuron can innervate airways on both sides. Injections of pseudorabies virus into the right lung revealed a bilateral network of infected neurons, even after unilateral vagotomy. The latter did not prevent infection of the ipsilateral vagal nuclei. These findings demonstrate that vagal motoneurons that project to the lungs receive contralateral inputs from the airway premotor network and vagal bronchomotor centers.     

Chromatin changes in frog neurons after eighth nerve transection

Fourteen days after unilateral eighth nerve transection in the frog, Purkinje neurons of the lobus vestibulolateralis and corpus of the cerebellum and medium-sized neurons of the vestibular nuclear complex showed changes in metabolic activity. In the ipsilateral parts, and to a lesser extent in the contralateral parts, of operated frogs, the Feulgen-DNA values were higher and the nuclear areas larger, associated with decondensation of chromatin. The cytoplasmic basophilia was also less. These changes could be due to anabolic responses of the neuronal populations during regeneration. The anabolic reaction of the corpus cerebelli and contralateral vestibular nuclear complex is only partially non-specific and ascribable to the surgical trauma (comparison between sham-operated and unoperated frogs). The results indicate clear patterns of connection between the ipsilateral and contralateral parts and between the cerebellar and vestibular nuclear complex neurons.     

Canal and otolith inputs to single vestibular neurons in cats

Convergence of both afferents from the PC and saccular macula, and those from the PC and utricular macula on single vestibular neurons was noted by use of intercellular recording from vestibular neurons. Vestibular neurons were classified VO neurons (vestibulo-ocular proper neurons), VOS (Vestibulo-oculo-spinal neurons sending axon collaterals both to the extraocular motoneuron pools and to the spinal cord), VS neurons (vestibulospinal proper neurons) and V neurons (vestibular neurons without axons to the oculomotor nuclei or the spinal cord) on the basis of whether or not they responded antidromically to stimulation of the oculomotor nuclei and the spinal cord. Of the total 143 vestibular neurons recorded in the series of experiments on convergence of the PC and saccular afferents, 47 neurons (33%) were received inputs from both the PC and saccular nerves. Twenty-six of the 47 convergent neurons were identified as having the nature of VS neurons. Half (13/26) of those were activated monosynaptically from both the PC and saccular nerves. Only one saccular-activated neuron without PC inputs sent an axon to the oculomotor nuclei. In the other series of experiments on the convergence of the PC and utricular afferents, 41 (37%) of 111 vestibular neurons were proved to converge on inputs from both nerves. The majority (35/41) of the neurons received monosynaptic inputs from the PC nerve and polysynaptic EPSP-IPSP sequences from the utricular nerve, or vice versa. The ratio of PC-otolith convergent neurons among utricular-activated neurons (41/54, 76%) was higher than that among saccular activated neurons (47/88, 53%). The percentage of utricular alone neurons without PC inputs (13/111, 12%) was less than that of the saccular alone without PC inputs (41/145, 28%). In conclusion, the convergence of canal and otolith inputs likely contribute mainly to vestibulospinal reflexes including the vestibulocollic reflex, by sending inputs to the neck and other muscles during head inclination which creates the combined stimuli of angular and linear acceleration.     

Spatial transformation of semicircular canal signals into abducens motor signals. A comparison between grass frogs and water frogs

The spatial transformation of semicircular canal signals to extraocular motor signals was studied by recording abducens nerve responses in grass and water frogs. Both species have similar vestibular canal coordinates but dissimilar orientations of their optic axes. Before sinusoidal oscillation in darkness the static head position was systematically altered to determine the planes of head oscillation in pitch and roll associated with minimal abducens nerve responses. Measured data and known canal plane vectors were used to calculate the abducens response vector in canal coordinates. The abducens vector deviated from the horizontal canal plane vector in grass frogs by 15° and in water frogs by 34° but was aligned with the pulling direction of the lateral rectus muscle in each of the two species. Lesion experiments demonstrated the importance of convergent inputs from the contralateral horizontal and anterior semicircular canals for the orientation of the abducens response vector. Thus, the orientation of the optic axis and the pulling directions of extraocular muscles are taken into account by the central organization of vestibulo-ocular reflexes. Horizontal and vertical canal signals are combined species-specifically to transform the spatial coordinates of sensory signals into appropriate extraocular motor signals. Accepted: 16 November 1997     

Bilateral collicular interaction: modulation of auditory signal processing in amplitude domain

In the ascending auditory pathway, the inferior colliculus (IC) receives and integrates excitatory and inhibitory inputs from many lower auditory nuclei, intrinsic projections within the IC, contralateral IC through the commissure of the IC and from the auditory cortex. All these connections make the IC a major center for subcortical temporal and spectral integration of auditory information. In this study, we examine bilateral collicular interaction in modulating amplitude-domain signal processing using electrophysiological recording, acoustic and focal electrical stimulation. Focal electrical stimulation of one (ipsilateral) IC produces widespread inhibition (61.6%) and focused facilitation (9.1%) of responses of neurons in the other (contralateral) IC, while 29.3% of the neurons were not affected. Bilateral collicular interaction produces a decrease in the response magnitude and an increase in the response latency of inhibited IC neurons but produces opposite effects on the response of facilitated IC neurons. These two groups of neurons are not separately located and are tonotopically organized within the IC. The modulation effect is most effective at low sound level and is dependent upon the interval between the acoustic and electric stimuli. The focal electrical stimulation of the ipsilateral IC compresses or expands the rate-level functions of contralateral IC neurons. The focal electrical stimulation also produces a shift in the minimum threshold and dynamic range of contralateral IC neurons for as long as 150 minutes. The degree of bilateral collicular interaction is dependent upon the difference in the best frequency between the electrically stimulated IC neurons and modulated IC neurons. These data suggest that bilateral collicular interaction mainly changes the ratio between excitation and inhibition during signal processing so as to sharpen the amplitude sensitivity of IC neurons. Bilateral interaction may be also involved in acoustic-experience-dependent plasticity in the IC. Three possible neural pathways underlying the bilateral collicular interaction are discussed.     

Binocular depth perception mechanisms in tongue-projecting salamanders

Tongue-projecting salamanders (Bolitoglossini) combine extreme speed and high precision in prey capture. They possess all requirements for stereoscopic depth perception: frontally oriented eyes, a substantial amount of direct ipsilateral projection in addition to the contralateral one, and binocularly driven neurons. Extracellular recordings were made from retinal afferents in the tectum as well as from the somata of tectal neurons. RF-sizes of afferents and tectal neurons were determined, and the response properties of tectal neurons were tested under monocular and binocular conditions with stimuli of different size and velocity. While RF-sizes and response properties of binocular neurons during binocular and contralateral stimulation were similar, ipsilaterally stimulated neurons exhibited much smaller RFs, lower spike rates and different size preferences.Furthermore, the contralateral retinotectal projection from one eye and the ipsilateral from the other are in register. While retinal afferents are distributed linearly over the tectal surface, most tectal neurons are activated by a retinal area corresponding to the frontal visual field; this results in a magnification of this region. The two monocular receptive fields of binocular neurons exhibit zero disparities (horopter) at distances that coincide with the maximum reach of the tongue. We hypothesize that bolitoglossine salamanders (as well as amphibians in general) make use of two kinds of disparities: (1) between the maps in the left and right tectal hemisphere, coding for the lateral eccentricity of an object, and (2) between the ipsilateral and contralateral retinotectal map, coding for the distance. The presence of substantial direct ipsilateral afferents in bolitoglossine salamanders appears to be the basis for a fast computation of object distance, which is characteristic of these animals.Abbreviations Ax/Ay coordinates of a recorded afference - Nx/Ny coordinates of a recorded neuron - RF receptive field - RFc contralateral receptive field - RFi ipsilateral receptive field - RFx/RFy coordinates of a receptive field center - RGC retinal ganglion cell     

Normal gait is differentially influenced by the otoliths

Postural control depends on the integration of vestibular, somatosensory and visual orientation signals. The otolith contribution to postural control is achieved by the integration of otolith inputs and peripheral afferent inputs involved in crossed reflex pathways. This study shows that a functional linkage between otolith signals and activity in lower limb muscles is detectable in normal human gait. The otolith input appears to dominate particularly the neck proprioceptive and gaze motor influences during normal gait. This is demonstrated by an increase of tibialis anterior muscle activity during retroflexion of the head/neck, leading to an increased stability and counteracting possible perturbations. It is also shown by decrease of coordination during the movement caused by larger displacement of the centre of gravity demonstrated in vector diagrams.     

Auditory centre projection of the lower brainstem to the dorsal cochlear nucleus in the rabbit

Afferent projection to dCN from SOC and the periolivary regions was studied in the rabbit by retrograde transport of WGA-HRP. The projection originates primarily from the bilateral TrV and TrL with a very clear contralateral and ipsilateral predominance, respectively. A clear-cut topographical relationship was disclosed between location of neurons in these nuclei and projection sites in dCN. Thus, the medial region of dCN is target of projection arising from the medial regions of TrV and TrL, whereas the lateral region of dCN is supplied by projection from their lateral regions. Although participation in the projection of the ipsilateral TrV is smaller and the contralateral TrL is very weak, the pattern of these preferential connections is also apparent. Minute connections were traced from the other principal olivary nuclei, i.e. MSO, LSO and TrM, mainly from neurons located in their peripheral regions. In the periolivary region the cells of origin of the projection were found in VLPO and VMPO, and in lesser extent in DPO, DMPO, DLPO, RPO and CPO. The present results are discussed in comparison with those of earlier studies and with reference to other inputs to CN.     

Probing the human vestibular system with galvanic stimulation.

Galvanic vestibular stimulation (GVS) is a simple, safe, and specific way to elicit vestibular reflexes. Yet, despite a long history, it has only recently found popularity as a research tool and is rarely used clinically. The obstacle to advancing and exploiting GVS is that we cannot interpret the evoked responses with certainty because we do not understand how the stimulus acts as an input to the system. This paper examines the electrophysiology and anatomy of the vestibular organs and the effects of GVS on human balance control and develops a model that explains the observed balance responses. These responses are large and highly organized over all body segments and adapt to postural and balance requirements. To achieve this, neurons in the vestibular nuclei receive convergent signals from all vestibular receptors and somatosensory and cortical inputs. GVS sway responses are affected by other sources of information about balance but can appear as the sum of otolithic and semicircular canal responses. Electrophysiological studies showing similar activation of primary afferents from the otolith organs and canals and their convergence in the vestibular nuclei support this. On the basis of the morphology of the cristae and the alignment of the semicircular canals in the skull, rotational vectors calculated for every mode of GVS agree with the observed sway. However, vector summation of signals from all utricular afferents does not explain the observed sway. Thus we propose the hypothesis that the otolithic component of the balance response originates from only the pars medialis of the utricular macula.     

Intranuclear coupling of hypothalamic magnocellular nuclei by glutamate synaptic circuits

Magnocellular neurons of the supraoptic nucleus (SON) and paraventricular nucleus (PVN) display bursting activity that is synchronized under certain conditions. They receive excitatory synaptic inputs from intrahypothalamic glutamate circuits, some of which are activated by norepinephrine. Ascending noradrenergic afferents and intrahypothalamic glutamate circuits may be responsible for the generation of synchronous bursting among oxytocin neurons and/or asynchronous bursting among vasopressin neurons located in the bilateral supraoptic and paraventricular nuclei. Here, we tested whether magnocellular neurons of the PVN receive excitatory synaptic input from the contralateral PVN and the region of the retrochiasmatic SON (SONrx) via norepinephrine-sensitive internuclear glutamate circuits. Whole cell patch-clamp recordings were performed in PVN magnocellular neurons in coronal hypothalamic slices from male rats, and the ipsilateral SONrx region and contralateral PVN were stimulated using electrical and chemical stimulation. Electrical and glutamate microdrop stimulation of the ipsilateral SONrx region or contralateral PVN elicited excitatory postsynaptic potentials/currents (EPSP/Cs) in PVN magnocellular neurons mediated by glutamate release, revealing internuclear glutamatergic circuits. Microdrop application of norepinephrine also elicited EPSP/Cs, suggesting that these circuits could be activated by activation of noradrenergic receptors. Repetitive electrical stimulation and drop application of norepinephrine, in some cases, elicited bursts of action potentials. Our data reveal glutamatergic synaptic circuits that interconnect the magnocellular nuclei and that can be activated by norepinephrine. These internuclear glutamatergic circuits may provide the functional architecture to support burst generation and/or burst synchronization in hypothalamic magnocellular neurons under conditions of activation.     

Effect of vestibular,somatic, and autonomic afferent impulsation on vestibular nuclear unit activity in cats

Single unit responses in nuclei of the vestibular complex to stimulation of the labyrinths and of proprioceptive and autonomic afferents were investigated. Different types of unit responses were obtained to stimulation, including evoked activity consisting of a group of action potentials followed by inhibition of the spike discharge. Unit activity in the vestibular nuclei was shown to depend on extralabyrinthine stimulation. In response to adequate stimulation of the labyrinths by tilting the head, the role of receptors of muscles and joints in the neck was distinguished. The question of the somatotopic organization of the vestibular nuclei and convergence of various afferent flows on neurons giving rise to the vestibulospinal tract is discussed.Institute of Medico-Biological Problems, Ministry of Health of the USSR, Moscow. Translated from Neirofiziologiya, Vol. 8, No. 5, pp. 507–513, September–October, 1976.     

Bilateral convergence of pulmonary stretch receptor inputs on I beta-neurons in the cat

Extracellular recordings were made from inspiratory beta- (I beta) neurons in the nucleus of the tractus solitarius in decerebrate cats. A reversible direct current block of myelinated fibers in the ipsilateral vagus nerve was used to evaluate the input from pulmonary stretch receptor afferents (PSR) of the contralateral vagus to individual I beta-neurons. This block served to remove all ipsilateral (which includes all monosynaptic) inputs from PSR to I beta-cells. The effect of withholding inflation on the firing rate and the time of onset of firing of I beta-neurons was determined before, during and after application of the direct current block. There was considerable variation in the strengths of the inputs from the ipsilateral and contralateral nerves; some cells received PSR inputs from only the ipsilateral vagus, but the majority were excited with varying magnitude from both vagi. Several neurons had powerful excitatory inputs from PSR of the contralateral vagus, with the ipsilateral (monosynaptic) contribution being of minor importance.     

Mechanisms of the otolith signal processing

A series of current hypotheses of mechanisms of the otolith signals processing and organization of adaptive responses of the oculomotor system to gravito-sensitive (otolith) inputs are reviewed: the "frequency segregation of the otolith signals", "gravito-inertial force resolution", "spatio-temporal transformation of the angular vestibulo-ocular reflex", "inertial processing of the vestibular signals", "asymmetry of the otolith signals", and their experimental corroboration.     

Sensory processing in the vestibular nuclei during active head movements

Many secondary vestibular neurons are sensitive to head on trunk rotation during reflex-induced and voluntary head movements. During passive whole body rotation the interaction of head on trunk signals related to the vestibulo-collic reflex with vestibular signals increases the rotational gain of many secondary vestibular neurons, including many that project to the spinal cord. In some units, the sensitivity to head on trunk and vestibular input is matched and the resulting interaction produces an output that is related to the trunk velocity in space. In other units the head on trunk inputs are stronger and the resulting interaction produces an output that is larger during the reflex. During voluntary head movements, inputs related to head on trunk movement combine destructively with vestibular signals, and often cancel the sensory reafferent consequences of self-generated movements. Cancellation of sensory vestibular signals was observed in all of the antidromically identified secondary vestibulospinal units, even though many of these units were not significantly affected by reflexive head on trunk movements. The results imply that the inputs to vestibular neurons related to head on trunk rotation during reflexive and voluntary movements arise from different sources. We suggest that the relative strength of reflexive head on trunk input to different vestibular neurons might reflect the different functional roles they have in controlling the posture of the neck and body.     

Afferent connections of the cat lateral vestibular nucleus

Location within the brain of HP-labeled neurons (origins of projections to the lateral vestibular nucleus) was investigated by iontophoretic injection of this enzyme. Bilateral projections to the following midbrain structures were revealed: the field of Forel, interstitial nuclei of Cajal, oculomotor nerve nuclei, and the red nucleus — to all parts of the lateral vestibular nucleus. Bilateral projections were also shown from more caudally located structures, viz. the superior, medial and inferior (descending) vestibular nuclei, Y groups of the vestibular nuclear complex, facial nucleus and hypoglossi, nucleus prepositus nervi hypoglossi and caudal nuclei of the trigeminal tract; ipsilateral projections from crus IIa of lobulus ansiformus of the cerebellar hemisphere; contralateral projections from the bulbar lateral reticular nucleus and Deiter's nucleus. A tonic organization pattern of afferent inputs from a number of brainstem formations to the dorsal and ventral lateral vestibular nucleus is revealed and trajectories of HP-labeled fiber systems projecting to Deiter's nucleus described.L. A. Orbeli Institute of Physiology, Academy of Sciences of the Armenian SSR, Erevan. Translated from Neirofiziologiya, Vol. 20, No. 4, pp. 494–503, July–August, 1988.     

Hrp-labeled sources of descending propriospinal pathways in cats

Unilateral injections of horseradish peroxidase into the cat spinal cord at different segmental levels revealed a laminar distribution of spinal interneurons that are sources of ipsilateral and contralateral propriospinal pathways of different lengths. The majority of the long pathways connecting cervical and lumbar segments are formed by neurons located in the central quadrants (laminae VII and VIII) bilaterally; a few such neurons also are present in the marginal layer and in lateral zones at the base of the dorsal horn (ipsilaterally). The zones containing numerous propriospinal neurons forming short (extending over a few segments) connections were more extensive. In the lumbar portion neurons which were sources of short uncrossed pathways tended to be concentrated in the lateral areas of the base of the dorsal horn, intermediate zone, and ventral horn, whereas sources of crossed pathways were concentrated in the ventromedial zones of gray matter. In the cervical portion "short" propriospinal neurons forming both ipsilateral and contralateral projections were concentrated in the lateral zones of gray matter. Neurons of the marginal layer and substantia gelatinosa and neurons of intermediolateral sympathetic nuclei also were sources of descending propriospinal pathways. Some propriospinal axons were intermediate in length. The distribution of neurons with axons of this kind largely coincided with the distribution of neurons that were sources of long propriospinal pathways. The connection between the spatial distribution of different groups of propriospinal neurons and the organization of the synaptic inputs into them, and also correlation between the morphological and functional characteristics of these neurons are discussed.