Spatial coordination by descending vestibular signals

Electromyographic activity of dorsal neck muscles and neck torques was recorded to study vestibulocollic, cervicocollic, and combined reflexes in alert and decerebrate cats during rotations of the whole body, the body except for the head, and the head but not the rest of the body. Cats were rotated about many axes that lay in the frontal, sagittal, and horizontal planes using sinusoidal 0.25-Hz waveforms or sum-of-sinusoid waveforms. Robust electromyographic responses were recorded from six muscles, with response directionality that in most cases did not show strong dependence on the reflex tested or on other factors including exact neck angle, stimulus amplitude from 5° to 60°, and intact versus decerebrate state. Based on the strength of responses to rotations about all the tested axes, neck muscles could be characterized by maximal activation direction vectors representing the axis and direction of rotation in threedimensional space that was most excitatory during reflex responses. Responses to rotations about axes that lay in a coordinate plane were predicted by a cosine function of the angle between the axis under test and the maximally excitatory axis in the plane. All muscles were excited by the nose down phase of pitch rotation and by yaw and roll away from the side on which the muscle lay. Biventer cervicis was best activated by rotations with axes near nose-down pitch, and its axis of maximal activation also had small, approximately equal components of yaw and roll toward the contralateral side. Complexus was best excited by rotations with axes nearest roll, but with large components along all three axes. Occipitoscapularis was best excited by rotations about axes near pitch, but with a moderately large contralateral yaw component and a smaller but significant contralateral roll component. Splenius was best excited by rotations with a large component of contralateral yaw, considerable nose-down pitch, and a smaller component of contralateral roll. Rectus major was best excited by rotations near nose-down pitch, but with a substantial contralateral yaw component and smaller contralateral roll component. Obliquus inferior was best excited by rotations with a large component of contralateral yaw, but with considerable contralateral roll and nose-down pitch components. All muscles responded as though they received convergent input from all three semicircular canals. Vestibulocollic and combined reflex responses in alert cats and vestibulocollic, cervicocollic, and combined responses in decerebrate cats appeared to have the same directionality, as evidenced by insignificant shifts in maximal activation vectors. Cervicocollic responses in alert cats were inconsistent and often absent, but appeared upon decerebration, suggesting that higher centers suppress the cervicocollic reflex in intact animals. Decerebration and partial cerebellectomy had no significant effect on maximal activation directions, although electromyographic response magnitudes increased after each. The results suggest that common circuits or strategies are used by neck stretch and vestibular-neck reflexes. The reflex excitation directions do not match the mechanical actions of the neck muscles but agree fairly well with previously published predictions of a mathematical model of neck motor control.     

Spatial coordination by descending vestibular signals

Spatial response properties of medial (MVST) and lateral (LVST) vestibulospinal tract neurons were studied in alert and decerebrate cats during sinusoidal angular rotations of the whole body in the horizontal and many vertical planes. Of 220 vestibulospinal neurons with activity modulated during 0.5-Hz sinusoidal rotations, 200 neurons exhibited response gains that varied as a cosine function of stimulus orientation and phases that were near head velocity for rotation planes far from the minimum response plane. A maximum activation direction vector (MAD), which represents the axis and direction of rotation that maximally excites the neuron, was calculated for these neurons. Spatial properties of secondary MVST neurons in alert and decerebrate animals were similar. The responses of 88 of 134 neurons (66%) could be accounted for by input from one semicircular canal pair. Of these, 84 had responses consistent with excitation from the ipsilateral canal of the pair (13 horizontal, 27 anterior, 44 posterior) and 4 with excitation from the contralateral horizontal canal. The responses of the remaining 46 (34%) neurons suggested convergent inputs. The activity of 38 of these was significantly modulated by both horizontal and vertical rotations. Twelve neurons (9%) had responses that were consistent with input from both vertical canal pairs, including 9 cells with MADs near the roll axis. Thirty-two secondary MVST neurons (24%) had type II yaw and/or roll responses. The spatial response properties of 18 secondary LVST neurons, all studied in decerebrate animals, were different from those of secondary MVST neurons. Sixteen neurons (89%) had type II yaw and/or roll responses, and 12 (67%) appeared to receive convergent canal pair input. Convergent input was more common on higher-order vestibulospinal neurons than on secondary neurons. These results suggest that MVST and LVST neurons and previously reported vestibulo-ocular neurons transmit functionally different signals. LVST neurons, particularly those with MADs close to the roll axis, may be involved in the vestibular-limb reflex. The combination of vertical and ipsilateral horizontal canal input on many secondary MVST neurons suggests a contribution to the vestibulocollic reflex. However, in contrast to most neck muscles, very few neurons had maximum vertical responses near pitch.     

Functional organization of the vestibular input to the anterior and posterior cerebellar vermis of cat

1. Responses evoked by electrical stimulation (auditory division of the VIIIth nerve sectioned chronically) and natural stimulation of the vestibular apparatus were recorded in the anterior and posterior cerebellar vermis of cats anesthetized with Ketamine or Nembutal. Under Ketamine the functional state of the cerebellar cortex was similar to that of the decerebrate or encéphale isolé preparation. 2. Vestibular-evoked responses were found bilaterally throughout the vermis (lob. I-X) and parts of pars intermedia and were, for the most part, mediated via the mossy fiber-granule cell pathway although natural stimulation occasionally evoked climbing fiber responses in Purkinje cells. 3. Lesion and stimulation experiments suggested that the polysynaptic potentials recorded in the dorsal folia of the anterior and parts of posterior vermis were mediated, at least in part, by the lateral reticular nucleus. Potentials recorded in the deeper folia often had shorter latencies and were probably mediated by primary and/or secondary vestibular fibers. Studies with horseradish peroxidase (injections in lob. V and VI) supported these notions. 4. An analysis of Purkinje cell responses to sinusoidal rotation and steps of angular acceleration or velocity indicated that P-cells in these regions signalled angular head velocity in the mid-frequency range. Single canal responses as well as multi-canal convergent P-cell responses were found. Purkinje cells also responded to static head displacement.     

Postsynaptic influences on the vestibular non-deiters nuclei from primary vestibular nerve

Summary Neurones in the descending, medial and superior vestibular nuclei of the cats were explored with intracellular microelectrodes. Cerebellar- and spinal-projecting neurones were identified by their antidromic invasion from the region of fastigial nuclei and from the second cervical segment, respectively, and the others by their location. The central actions of the primary vestibular impulses upon these non-Deiters vestibular nuclei neurones were investigated by using electric stimulation of the ipsilateral vestibular nerve. Many of these cells received excitatory postsynaptic potentials (EPSPs) monosynaptically, similar to those evoked in the ventral Deiters neurones, as described elsewhere, except that the unitary EPSPs are often larger. Some cells received only polysynaptic EPSPs or IPSPs and a few cells were not influenced at all.     

Functional organization of vestibular and visual inputs to neck and forelimb motoneurons in the frog.

1. Intracellular responses in neck and forelimb motoneurons to electrical stimulation of the vestibular nerve, the optic tectum, and the optic nerve were studied in frog. 2. Stimulation of the anterior branch of the vestibular nerve typically produced EPSPs, bilaterally, in neck, shoulder (DOR), and forelimb extensor (TRI, RAD) motoneurons, and bilateral IPSPs in forelimb adductor (PED) and flexor (ULN, COR) motoneurons. 3. Latencies of PSPs recorded in neck, shoulder, and proximal extensor motoneurons (TRI) were mostly in the disynaptic range, whereas many of those recorded in distal extensor (RAD) and in adductor and flexor motoneurons involved three synapses. 4. Lesion of the vestibulospinal fibers greatly reduced the vestibular nerve-evoked field potentials in the spinal cord and the occurrence of PSPs in forelimb motoneurons. These results as well as the latency measurements suggest that the pathway linking vestibular nerve and forelimb motoneurons mainly consists of vestibulospinal fibers, though involvement of other structures for production of later PSPs could not be completely ruled out. Hemisection of the brain stem at its most caudal level showed that the pathway to the contralateral motoneurons crosses at the level of brain stem as well as in the spinal cord. 5. Stimulation of the optic tectum produced EPSPs, IPSPs, and a mixture of EPSPs and IPSPs in neck, shoulder, and forelimb motoneurons, bilaterally. Most frequently, a combination of an excitation and inhibition was observed. The pathway from the optic tectum to neck and limb motoneurons is at least dysnaptic in nature. 6. Stimulation of the optic nerve produced IPSPs and a mixture of EPSPs and IPSPs in neck and forelimb motoneurons. Impulses originating from the optic nerve descend as far as to lumbar motoneurons producing EPSP-IPSP sequences bilaterally. 7. Interaction studies suggested that the vestibular and optic pathways to neck and forelimb motoneurons are separate from each other so that the site of integration of vestibular and visual input occurs at the level of motoneurons. 8. Evidence for electronic coupling among forelimb motoneurons and electrical synaptic transmission in th pathway linking vestibular nerve and forelimb motoneurons is presented.     

Interaction between symmetrical cortical descending influences in lumbar motoneurons

Postsynaptic potentials (PSPs) of cat motoneurons were investigated by intracellular recording of unit activity during stimulation of the motor cortex unilaterally or bilaterally. Synaptic activation of motoneurons by ipsilateral cortical influences requires stronger stimulation than by contralateral and the PSPs thus produced differ from the contralateral in their longer latent period and segmental delay time. Stimulation of the ipsilateral cortex inhibits EPSPs and IPSPs of motoneurons evoked by contralateral cortical stimulation. Global activity recorded on the dorsal surface of the spinal cord is simultaneously depressed. It is concluded from the analysis of the data that inhibitory interaction between two descending cortical activities takes place with the participation of the segmental inhibitory interneuronal apparatus and is brought about at the level of interneurons and (or) through hyperpolarization changes in the membrane potential of the motoneurons themselves.Translated from Fiziologicheskii Zhurnal SSSR imeni I. M. Sechenova, Vol. 62, No. 1, pp. 47–55, January, 1976.     

Functional organization of premotor neurons in the cat medial vestibular nucleus related to slow and fast phases of nystagmus

Summary Extracellular spikes were recorded from secondary vestibular neurons in the cat medial vestibular nucleus (MVN) and were identified as type I or II neurons by horizontal rotation. Type I neurons were further classified as excitatory or inhibitory premotor neurons on the basis of their axonal termination in the contralateral or ipsilateral abducens nucleus, demonstrated by spike-triggered averaging of abducens nerve discharges, or by antidromic activation using systematic microstimulation within the abducens nucleus.Both excitatory and inhibitory premotor type I MVN neurons exhibited a rhythmic modulation of their firing rate in association with nystagmus elicited by rotation or electrical stimulation of the vestibular nerve. Their tonic activity during the slow phase was suppressed at the quick phase directed to the ipsilateral side.Excitatory type I MVN neurons terminating in the contralateral abducens nucleus sent collateral axons to the contralateral MVN. These commissural neurons also showed a nystagmus-related discharge pattern.Type II MVN neurons activated at short latency by stimulation of the contralateral vestibular nerve exhibited burst discharges when the activity of ipsilateral type I neurons was suppressed at the quick phase. These type II neurons made monosynaptic inhibitory connections with type I neurons as shown by the post-spike average of the membrane potential of secondary MVN neurons triggered from spikes of single type II neurons. Thus, the inhibitory action originating from burst activity of type II MVN neurons contributes to suppression of type I premotor MVN neurons during fast eye movements.Supported by Grant-in-Aid for Scientific Research No. 248106 from Japan Ministry of Education, Science and Culture. Dr. Schor was supported by the Research Fellowship of Japan Society for the Promotion of Science (JSPS)     

Cortical influences on the vestibular nuclei of the cat

 Our goal was to study potential substrates for cortical modulation of vestibular reflexes in the cat. In initial experiments, injections of wheat-germ-agglutinate-horseradish-peroxidase into Deiters’ nucleus and the rostral descending nucleus revealed bilateral colonies of retrogradely filled neurons in cortical areas 6, 2, and 3a (about 60 cells per colony). In cats anesthetized with chloralose-urethane, we stimulated areas 2 and 3a with trains of pulses while recording from ipsilateral vestibular-nucleus neurons, which were characterized by their responses to sinusoidal tilts and tested for the presence of antidromic responses to stimulation of the upper cervical cord. A majority of the neurons was affected by cortical stimulation, showing either facilitation, inhibition, or a mixture of the two. Stimulation in area 2 was more effective than stimulation in area 3a. Despite the anatomic presence of direct cortico-vestibular projections, properties of facilitation and inhibition suggest that both were evoked by polysynaptic pathways. Cortical effects were broadly distributed to vestibular neurons without regard to responses of these neurons to sinusoidal tilts. There was no significant difference between effects on lateral and medial vestibulospinal tract neurons, but, as a group, vestibulospinal neurons were much more likely to be affected by cortical stimulation than neurons not antidromically activated from the C2 segment. We conclude that, by their influence on vestibulospinal neurons, neurons in cortical areas 2 and 3a should be able to modulate, in behaving animals, vestibular reflexes acting on the neck and limbs. Received: 28 May 1998 / Accepted:14 October 1998     

Afferent diversity and the organization of central vestibular pathways

This review considers whether the vestibular system includes separate populations of sensory axons innervating individual organs and giving rise to distinct central pathways. There is a variability in the discharge properties of afferents supplying each organ. Discharge regularity provides a marker for this diversity since fibers which differ in this way also differ in many other properties. Postspike recovery of excitability determines the discharge regularity of an afferent and its sensitivity to depolarizing inputs. Sensitivity is small in regularly discharging afferents and large in irregularly discharging afferents. The enhanced sensitivity of irregular fibers explains their larger responses to sensory inputs, to efferent activation, and to externally applied galvanic currents, but not their distinctive response dynamics. Morphophysiological studies show that regular and irregular afferents innervate overlapping regions of the vestibular nuclei. Intracellular recordings of EPSPs reveal that some secondary vestibular neurons receive a restricted input from regular or irregular afferents, but that most such neurons receive a mixed input from both kinds of afferents. Anodal currents delivered to the labyrinth can result in a selective and reversible silencing of irregular afferents. Such a functional ablation can provide estimates of the relative contributions of regular and irregular inputs to a central neuron’s discharge. From such estimates it is concluded that secondary neurons need not resemble their afferent inputs in discharge regularity or response dynamics. Several suggestions are made as to the potentially distinctive contributions made by regular and irregular afferents: (1) Reflecting their response dynamics, regular and irregular afferents could compensate for differences in the dynamic loads of various reflexes or of individual reflexes in different parts of their frequency range; (2) The gating of irregular inputs to secondary VOR neurons could modify the operation of reflexes under varying behavioral circumstances; (3) Two-dimensional sensitivity can arise from the convergence onto secondary neurons of otolith inputs differing in their directional properties and response dynamics; (4) Calyx afferents have relatively low gains when compared with irregular dimorphic afferents. This could serve to expand the stimulus range over which the response of calyx afferents remains linear, while at the same time preserving the other features peculiar to irregular afferents. Among those features are phasic response dynamics and large responses to efferent activation; (5) Because of the convergence of several afferents onto each secondary neuron, information transmission to the latter depends on the gain of individual afferents, but not on their discharge regularity. Received: 22 March 1999 / Accepted: 21 July 1999     

Functional heterogeneity of the descending limbs of Henle's loop

Permeability properties of the descending limbs of Henle's loop were compared among rabbits, hamsters, and rats by measuring transepithelial voltage (Vt) across the isolated renal tubules perfused in vitro. From the deflection of the Vt when the composition of the bathing fluid was varied, the permeabilities of sodium and of potassium relative to chloride (Pna/PCl and PK/PCl, respectively) were determined in either the descending limbs of the short-loop nephron (SDL) or the segments of the upper protion of the long-loop nephron (LDLu). In hamsters and rats, the values of PNa/PCl of the LDLu (3.98 +/- 0.66 and 5.03 +/- 0.79) were higher than those of the SDL (0.68 +/- 0.03 and 0.61 +/- 0.00). In contrast, in rabbits the value of PNa/PCl of the LDLu (0.96 +/- 0.05) was only slightly higher than that of the SDLu (0.75 +/- 0.03). The similar tendency was also noted in the values of PK/PCl. In hamsters and rats, the PK/PCi ratios were 4.90 +/- 0.82 and 6.44 +/- 0.90, respectively, in the LDLu and 1.09 +/- 0.04 and 1.02 +/- 0.0, respectively in the SDL. When a transepithelial osmotic gradient was imposed by adding raffinose to the bath, a lumen-negative streaming voltage of about -8 mV was generated in the hamster and the rat LDLu. Taken together with the findings in the preceding paper, these observations support the view that the descending limbs of rabbits are different from those of hamsters and rats in that internephron heterogeneity is less remarkable, and that the LDLu of hamsters and rats is highly permeable to sodium and to potassium as well as to water.     

Functional heterogeneity of the descending limbs of Henle's loop

By using the in vitro microperfusion technique, were examined functions of the descending limbs of Henle's loop obtained from either the short-loop nephron (SDL) or the upper portion of the long-loop nephron of hamsters (LDLu). Morphological distinctions between these segments were confirmed by light and electron microscopic observations. Both segments were highly permeable to water. The LDLu was highly permeable to sodium and to chloride: efflux coefficients (10^–7 cm²·s^–1) for²²Na and³⁶Cl were 41.0±5.4 and 3.8±0.6, respectively. The SDL were less permeable to sodium and to chloride: efflux coefficient for²²Na and³⁶Cl were 2.9±1.4 and 0.9±0.2, respectively. In contrast, the SDL was more permeable to urea as compared to the LDL, efflux coefficients for urea being 5.1±1.4 vs 1.4±0.3, respectively. When composition of the perfusate was identical to that of the bathing fluid, no transepithelial voltage was demonstrated. The volume flux was very small or undetectable. From these observations, we propose that the internephron heterogencity must be taken into consideration for constructing a model of countercurrent system in the renal medulla.     

Segmental and descending influences on intraspinal thresholds of single C-fibers.

1. The effect was studied of various conditioning stimuli on the threshold of single C-fibers near their spinal terminals. Spikes were recorded in L6 and L7 dorsal root ganglia of cats. A stimulating electrode in the superficial dorsal horn delivered periodic pulses whose widths were adjusted automatically to near threshold for antidromic spike production. Most units were classified according to their adequate cutaneous stimuli, as C-mechanoreceptors, high-threshold mechanoreceptors, or polymodal nociceptors. 2. Orthodromic activity in all units increased their threshold for up to several minutes; the maximum and rate of decay depended on the amount of activity. This phenomenon parallels the hyperpolarizing afterpotential of C-fibers in peripheral nerve and, we suggest, is probably due to the aftereffect of impulses. 3. Cutaneous conditioning stimuli were applied for 10-20 s near the receptive fields of tested units, but without activating them. During the brushing of skin hair, all threshold changes were decreases; during pinching most changes were increases; during noxious heating the numbers of increases and decreases were similar. It will be necessary to analyze the responses of postsynaptic cells in order to know the physiological significance of these threshold changes. 4. Stimulation in the nucleus raphe magnus caused in half the units higher intraspinal thresholds. If this result is causally related to the previously reported inhibition of neuronal responses in the dorsal horn by the nucleus raphe magnus (NRM), then increased thresholds could reflect either direct presynaptic inhibition or facilitation of inhibitory connections. 5. No correlation between receptive-field classification and the response of terminals to natural cutaneous stimulation or stimulation of the NRM could be discovered. However, the terminals of all kinds of C-fibers differ from A-fibers in their reaction to noxious cutaneous and NRM stimulation, suggesting they are subject to a different system of control.