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S M Highstein

Publications and source records attributed to S M Highstein.

At least 37 records · Page 2Linked to original sources

Examination of the cupula and stereocilia of the horizontal semicircular canal in the toadfish Opsanus tau.

We imaged the horizontal semicircular canal (HSCC) crista and cupula of toadfish, Opsanus tau, by using a) confocal light microscopy of isolated vital HSCC; b) serial sections of fixed, trichrome-stained HSCC; and c) scanning electron microscopy of fixed HSCCs. HSCC were dissections which included an ampulla and an attached canal tube (long and slender canal portion), and, in some cases, a small portion of the utricular wall. Cupulae were seen as multipartite mucus connective tissue shells rising from the crista and extending toward the ampullary roof. They were composed of several refractile bands traversing the cupulae perpendicular to longitudinal fibers extending from the cupular base to its apex. Alcian green-stained cupulae showed an asymmetric alcianphilic, dark, X-shaped structure, indicating that the pillar is rich in mucin and carbohydrate, an interpretation supported by images of trichrome-stained sections. The cupular antrum is devoid of prominent refractile fibers. No tubes or channels were observed in the cupula or antrum of vital preparations. Cupular shell fibers cover the surface of the crista, are roughly parallel, and are associated with a translucent material having a refractive index greater than the surrounding endolymph. Stereocilia were thin, 100-microm-long structures, with little longitudinal curvature, which end with no end bulb. No strands extend from stereocilia to the roof or other portions of the cupular antrum. Gross movements of stereocilia were not seen in mechanically quiescent preparations. Within the cupular antrum, stereocilia were parallel to connective tissue fibers, all embedded in an isotropic gel. This fiber-reinforced gel and cupular matrix are sensitive to N-acetlyneuraminidase and beta-N-acetyl glucosaminidase, and minimally sensitive to beta-N-acetyl hexosaminidase. Connective tissue fibers may serve to stiffen the gel, whose matrix would restrict lateral motion of embedded fibers and stereocilia thereby providing mechanical support for stereocilia.

Acetylglucosaminidase↗

Role of the flocculus of the cerebellum in motor learning of the vestibulo-ocular reflex.

Structure-function studies at the systems level are an effective method for understanding the relationship of the central nervous system to behavior. Motor learning or adaptation of the vestibulo-ocular reflex is a clear example wherein this approach has been productive. During a vestibulo-ocular reflex the brain converts a head velocity signal, transduced through the vestibular semicircular canals, into an eye movement command delivered to the extraocular muscles. If the viewed target remains on the fovea of the retina, the reflex is compensatory, and its gain, eye velocity/head velocity, is one. When the image of the viewed object slips across the retina, visual acuity decreases, and the gain of the reflex, which is no longer one, is plastically adapted or adjusted until retinal stability is restored. The anatomic substrate for this plasticity thus involves brain structures in which visual-vestibular interaction can potentially occur, as well as vestibular and visual sensory and oculomotor motor structures. Further, it has been known for many years that removal of the flocculus of the cerebellum permanently precludes further vestibulo-ocular reflex adaptation, demonstrating the involvement of the cerebellum in this behavior. Maekawa and Simpson (J Neurophysiol 1973;36: 649-66) discovered that one visual input to the flocculus involved the accessory optic system and the inferior olive. Ensuing work has demonstrated that the visual signals used to adapt the vestibulo-ocular reflex are transmitted by this accessory optic system to the flocculus and subsequently to brain stem structures involved in vestibulo-ocular reflex plasticity. Presently the inclusive list of anatomic sites involved in vestibulo-ocular reflex circuitry and its adaptive plasticity is small. Our laboratory continues to believe that this behavior should be caused by interactions within this small class of neurons. By studying each class of identified neuron and its interactions with others within the list, we hope to ultimately understand the mechanisms used by the brain in the expression of this behavior.

Adaptation, Physiological↗

Anatomy and physiology of the primate interstitial nucleus of Cajal. II. Discharge pattern of single efferent fibers.

Anatomy and physiology of the primate interstitial nucleus of Cajal. II. Discharge pattern of single efferent fibers. J. Neurophysiol. 80: 3100-3111, 1998. Single efferent fibers of the interstitial nucleus of Cajal (NIC) were characterized physiologically and injected with biocytin in alert behaving monkeys. Quantitative analysis demonstrated that their discharge encodes a constellation of oculomotor variables. Tonic and phasic signals were related to vertical (up or down) eye position and saccades, respectively. Depending on how they encoded eye position, saccade velocity, saccade size, saccade duration, and smooth-pursuit eye velocity, fibers were characterized as regular or irregular, bi- or unidirectionally modulated, more or less sensitive, and reliable or unreliable. Further, fibers that did not burst for saccades (tonic) and fibers the eye-position and saccade-related signals of which increased in the same (in-phase) or in the opposite (anti-phase) directions were encountered. A continuum of discharge properties was the rule. We conclude that NIC efferent fibers send a combination of eye-position, saccade-, and smooth-pursuit-related signals, mixed in proportions that differ for different fibers, to targets of the vertical neural integrator such as extraocular motoneurons.

Animals↗

Differential central projections of physiologically characterized horizontal semicircular canal vestibular nerve afferents in the toadfish, Opsanus tau.

Anatomical and neurophysiological studies were undertaken to examine the central projection pattern of physiologically characterized horizontal semicircular canal vestibular nerve afferents in the toadfish, Opsanus tau. The variations in individual response characteristics of vestibular nerve afferents to rotational stimulus provided a means of typing the afferents into descriptive classes; the afferents fell into a broad continuum across the spectrum from low-gain, velocity-sensitive to high-gain, acceleration-sensitive responses (Boyle and Highstein [1990b] J. Neurosci. 10:1557-1569; Boyle and Highstein [1990a] J. Neurosci. 10:1570-1582). In the present study, each afferent was typed as a low-gain, high-gain, or acceleration fiber during rotational or mechanical stimulation (Rabbitt et al. [1995] J. Neurophysiol. 73:2237-2260) and was then intracellularly injected with biocytin. The axons were reconstructed, and the morphology, synaptic boutons, and projection pattern of each axon were determined. The results indicated that the three descriptive classes of vestibular nerve afferents have unique as well as overlapping central projection patterns and destinations in the vestibular nuclei, with intranuclear parcellation in the anterior octavus, magnocellularis, tangentialis, posterior octavus, and descending octavus nuclei. In general, increased sensitivity and faster response dynamics were correlated with both a more extensive central projection and a progressive increase in morphological complexity. Low-gain, velocity-sensitive fibers were the simplest morphologically, with the fewest number of branches (n = 17) and shortest length (4,282 microm), and projections were confined to the middle portions of the vestibular nuclei. High-gain, velocity-sensitive fibers were morphologically more diverse than low-gain fibers, with a greater number of branches (n = 26), longer length (6,059 microm), 29% greater volume, and a more widespread projection pattern with projections to both the anterior and the middle portions of the vestibular nuclei. Acceleration fibers were morphologically distinct from low- and high-gain fibers, with more elaborate branching (n = 41), greatest overall length (17,370 microm) and volume (16% greater than high gains), and displayed the most extensive central projection pattern, innervating all vestibular nuclei except tangentialis. Thus, there are anatomically demonstrable differential central projections of canal afferents with different response dynamics within the vestibular complex of the fish.

Animals↗

Determinants of semicircular canal afferent response dynamics in fish.

Present results separate the relative contributions of semicircular canal biomechanics from hair cell/afferent biophysics in determining the amplitude and phase of afferent responses to sinusoidal motion of the head. Separation was achieved by combining electrical polarization of the endolymph with mechanical indentation of the canal limb to modulate the instantaneous firing rate of horizontal semicircular canal afferents. The electrical stimulus drives hair cell transduction currents via modulation of the Nernst-Planck potential, whereas the mechanical stimulus mimics head rotation and modulates the open probability of the transduction channels. Responses for electrical polarization therefore reflect post-transduction-current (PTC) mechanisms, and responses for mechanical stimulation include the additional influence of canal mechanics. Linear transfer functions defining individual afferent response dynamics were obtained for low levels of each stimuli and are reported in Bode form providing gain (spikes/s per micron or mV) and phase (deg re: peak stim) over the frequency range from 0.02 to 40 Hz. Combined results for electrical and mechanical stimuli distinguish the component of sensory signal processing carried out by canal mechanics from that carried out by the hair cell/afferent complexes. Individual afferents were categorized according to their response to the mechanical stimuli as low-gain velocity (LG), high-gain velocity (HG) or acceleration (A) sensitive, groups as originally defined by Boyle and Highstein to describe interafferent diversity present within the population. In contrast to the results for mechanical stimuli, all afferent groups exhibit nearly equal increases in gain and phase for increasing frequencies of electrical stimulation. Comparison of individual afferent responses for the two stimuli leads to the conclusion that the LG, HG, and A groups are distinguished primarily by diversity in the mechanical activation of associated hair cells and not by PTC mechanisms. Even though PTC processing does not contribute significantly to determining these groups, it is the primary determinant underlying high-frequency gain and phase enhancements observed in the population average. Comparison of mechanical and electrical responses also reveals the mechanical lower-corner responsible for phase enhancements and gain decreases in all afferents at low frequencies of mechanical stimulation (< 0.05 Hz). Results imply that LG afferents encode angular head velocity by canceling a phase lag and gain attenuation due to the mechanics with a phase lead and gain enhancement due to PTC mechanisms above approximately 0.2 Hz. In contrast, A group afferents encode angular head acceleration by combining high-frequency phase leads and gain enhancements present in both the mechanics and PTC mechanisms across the physiological frequency spectrum. HG afferents fall between these two extremes, and, other than the influence of the mechanical lower-corner, their response primarily reflects PTC processing.

Action Potentials↗

The microscopic anatomy and physiology of the mammalian saccadic system.

A central goal of the Neurosciences is to provide an account of how the brain works in terms of cell groups organised into pattern generating networks. This review focuses on the neural network that generates the rapid movements of the eyes that are called saccades. A brief description of the metrical and dynamical properties of saccades is provided first. Data obtained from lesion and electrical stimulation experiments are then described; these indicate that the relevant neural machinery spreads over at least 10 distinct cortical and subcortical regions of the brain. Each one of these regions harbors several distinct classes of saccade related cells (i.e. cells whose discharge encodes the metrical and often dynamical properties of saccades). The morphological and physiological properties of about 30 saccade related cell classes are described. To generate the signals they carry, and therefore saccades, distinct classes of cells influence each other in a non-random manner. Anatomical evidence is provided that indicates the existence of about 100 distinct connections established between saccade related neurons. The overall picture of the saccadic system that emerges from these studies is one of intricate complexity. In part this is due to the presence of at least 3, multiply interconnected negative feedback loops. Several computational models of the saccadic system have been proposed in an attempt to understand the functional significance of the simultaneous operation of these loops. An evaluation of these models demonstrates that besides providing a coherent summary of the data that concern it, successful models of the saccadic system generate realistic saccades (in precise quantitative psychophysical terms) when their elements are stimulated, produce abnormal saccades, reminiscent of those encountered in the clinic, when their elements are disabled, while their constituent units display realistic discharge patterns and are connected in a manner that respects anatomy.

Animals↗

Determinants of semicircular canal afferent response dynamics in the toadfish, Opsanus tau.

1. Present results determine the relative contributions of the biomechanical and the posttransduction-current (PTC) mechanisms to the sensory process carried out by the horizontal semicircular canal (HC) in the oyster toadfish, Opsanus tau. The role of each element was estimated using in vivo measurements of hair cell receptor potentials and afferent responses elicited by electrical stimuli and mechanical HC indentation. Individual afferent response dynamics are defined here using first-harmonic transfer functions presented in the form of response gain and phase for sinusoidal stimuli from approximately 0.02-30 Hz. Comparison of the response dynamics for the two types of stimuli distinguishes the mechanical and the PTC transfer functions leading to the neural response. The results show that both mechanisms contribute significantly to the overall signal processing performed by the semicircular canals. 2. Endolymphatic polarization and HC indentation. Modulation of the endolymphatic potential by current injection induces a differential voltage across the apical face of the hair cells that drives the transduction current directly via the Nernst-Planck potential. Results show that the electrical impedance of the apical tight junctions is much larger than the basal impedance to ground in O. tau, such that leakage current to the basolateral space is negligible and the voltage-sensitive basolateral currents remain fully functional during polarization of the endolymph (in the frequency range tested). Extracellular afferent responses to endolymphatic polarization were combined with responses to HC indentation to separate the relative contributions of the mechanical and the PTC mechanisms to the overall afferent response dynamics. Data show that more than one-half of the overall signal processing, as defined by the first-harmonic transfer function, persists even when canal mechanics is bypassed. 3. Hair-cell receptor potential modulation during HC indentation. Sharp microelectrodes were used to record the modulation of hair-cell receptor potentials (intracellular voltages) in vivo during physiological levels of sinusoidal HC indentation. Receptor potentials exhibit modulations dominated by the first harmonic and centered about the resting potential. The average gain of the receptor-potential modulation for HC indentation is approximately 0.88 mV/microns indent, corresponding to a value of 0.22 mV/deg/s head velocity, centered near zero phase over the range tested from 0.1-10 Hz. The present receptor potential data fall well short of spanning the full range of gain and phase present in the afferent population. Rather, intracellular hair-cell responses are consistent with the frequency-dependent mechanical activation of the transduction current as determined above. 4. Origins of individual afferent responses. The population of afferent responses forms a continuous distribution that is discussed here in terms of three groups as defined by Boyle and Highstein: velocity-sensitive low gain (LG) afferents, velocity/acceleration-sensitive high gain (HG) afferents, and acceleration-sensitive (A) afferents. The response dynamics of individual afferents were found to be determined by a mix of biomechanical and biophysical factors that vary systematically between these afferent groups. All afferents show low-frequency phase advancement and gain decrease during HC indentation associated with the mechanical lower-corner frequency and high-frequency phase and gain enhancements associated with the PTC processing. In highly phase-advanced afferents (A type), the mechanical response is additive with the PTC processing to achieve broad-band acceleration sensitive neural responses.(ABSTRACT TRUNCATED AT 250 WORDS)

Animals↗

Anatomy and physiology of the primate interstitial nucleus of Cajal I. efferent projections.

1. The efferent projections of the interstitial nucleus of Cajal (NIC) were studied in the squirrel monkey after iontophoretic injections of biocytin and Phaseolus Vulgaris leucoagglutinin into the NIC. To ensure the proper placement of the tracer, the same pipettes were used to extracellularly record the discharge pattern of NIC neurons. 2. Three projection systems of the NIC were distinguished: commissural (through the posterior commissure), descending, and ascending. 3. The posterior commissure system gave rise to dense terminal fields in the contralateral NIC, the oculomotor nucleus, and the trochlear nucleus. 4. The descending system of NIC projections deployed dense terminal fields in the ipsilateral gigantocellular reticular formation and the paramedian reticular formation of the pons, as well as in the ventromedial and commissural nuclei of the first two spinal cervical segments. It also gave rise to moderate or weak terminal fields in the vestibular complex, the nucleus prepositus hypoglossi, the inferior olive, and the magnocellular reticular formation, as well as cell groups scattered along the paramedian tracts in the pons and the pontine and medullary raphe. 5. The ascending system of NIC projections gave rise to dense terminal fields in the ipsilateral mesencephalic reticular formation and the zona incerta as well as moderate or weak terminal fields in the ipsilateral centromedian and parafascicular thalamic nuclei. It also provided dense bilateral labeling of the rostral interstitial nucleus of the medial longitudinal fasciculus and the fields of Forel, and moderate or weak bilateral labeling of the mediodorsal, central medial, and central lateral nuclei of the thalamus. 6. Models of saccade generation that rely on feedback from the velocity-to-position integrators and include the superior colliculus in their local feedback loop are contradicted because no fibers originating from the NIC traveled to the superior colliculus to deploy terminal fields. 7. Consistent with its morphological and functional diversity, these data indicate that the primate NIC sends signals to a multitude of targets implicated in the control of eye and head movements.

Afferent Pathways↗

Anatomy and physiology of saccadic long-lead burst neurons recorded in the alert squirrel monkey. I. Descending projections from the mesencephalon.

1. The intra-axonal recording and horseradish peroxidase injection technique together with spontaneous eye movement monitoring has been employed in alert behaving monkeys to study the discharge pattern and axonal projections of mesencephalic saccade-related long-lead burst neurons (LLBNs). 2. Most of the recovered axons (N = 21) belonged to two classes of neurons. The majority (N = 13) were identified as efferents of the superior colliculus and had circumscribed movement fields typical of collicular saccade-related burst neurons. This discharge pattern, their responses to electrical stimulation of one or both superior colliculi, and their morphological appearance identified them as members of the T class of tectal efferent neurons. 3. Axons of these T cells deployed terminal fields within several saccade-related brain stem areas including the nucleus reticularis tegmenti pontis, which projects to the cerebellum; the nucleus reticularis pontis oralis and caudalis, which contains excitatory premotor burst neurons; the nucleus raphe interpositus, which contains omnipause neurons; the nucleus paragigantocellularis, which contains inhibitory premotor burst neurons, as well as other less differentiated parts of the brain stem reticular formation. 4. The other class of LLBNs (N = 4) had their somata in the medullary reticular formation just lateral to the interstitial nucleus of Cajal. They projected primarily to the raphe nuclei, the medullary reticular formation, and the paramedian reticular nucleus. Discharges were of the directional type with up ON directions (N = 3) and down ON directions (N = 1). 5. Other fibers, which project to pontine and medullary oculomotor structures but whose somata were not recovered (N = 4), illustrate that there are also other types of LLBNs that contribute to the generation and control of saccadic eye movements. 6. Our findings complement previous data about the axonal trajectories of T-type superior colliculus efferents. They also demonstrate the existence of LLBNs located in the mesencephalic reticular formation and their target areas in the brain stem. Implications of these findings for current concepts of oculomotor control are discussed.

Animals↗

Anatomy and physiology of saccadic long-lead burst neurons recorded in the alert squirrel monkey. II. Pontine neurons.

1. The discharge patterns and axonal projections of saccadic long-lead burst neurons (LLBNs) with somata in the pontine reticular formation were studied in alert squirrel monkeys with the use of the method of intraaxonal recording and horseradish peroxidase injection. 2. The largest population of stained neurons were afferents to the cerebellum. They originated in the dorsomedial nucleus reticularis tegmenti pontis (NRTP) including its dorsal cell group (N = 5), the preabducens intrafascicular nucleus (N = 5), and the raphe pontis (N = 1). Axons of all neurons coursed under NRTP and entered brachium pontis without having synapsed in the brain stem. Three axons sent collaterals to the floccular lobe, but other more distant targets of these and the other cerebellar afferents could not be determined. Movement fields of these neurons were intermediate between vectorial and directional types. 3. Four neurons had their somata in nucleus reticularis pontis oralis and terminations in the brain stem reticular formation. Each neuron was different, but all terminated in the region containing excitatory burst neurons, and most terminated in the region containing inhibitory burst neurons. Other targets include nucleus reticularis pontis oralis and caudalis, NRTP, raphe interpositus, and the spinal cord. Discharge patterns included both vectorial and directional types. 4. Two reticulospinal neurons had large multipolar somata either just rostral or ventral to the abducens nucleus. These neurons also projected to the medullary reticular formation, caudal nucleus prepositus hypoglossi, and dorsal and ventral paramedian reticular nucleus. 5. The functional implications of the connections of these LLBNs and those reported in the companion paper are extensively discussed. The fact that the efferents of the superior colliculus target the regions containing medium-lead saccadic burst neurons confirms the role of the colliculus in saccade generation. However, the finding that many other neurons project to these regions and the finding that superior colliculus efferents project more heavily to areas containing reticulospinal neurons argue for a diminished role of the superior colliculus in saccade generation but an augmented role in head movement control.

Animals↗

Dorsal Y group in the squirrel monkey. I. Neuronal responses during rapid and long-term modifications of the vertical VOR.

1. The activity of 113 Y group neurons was recorded extracellularly in 5 alert squirrel monkeys. Sixty-two cells were recorded in naive animals, and 51 cells were recorded after adaptation of the vestibuloocular reflex (VOR) with the use of telescopic lenses. The animals were lying on their right side, so that head rotation was in the vertical (pitch) plane and optokinetic stimulation elicited vertical eye movement. The responses of most cells, as well as the concurrent eye movement, were studied during 1) the VOR, elicited in darkness or in light by sinusoidal head rotation, 2) visual following, elicited by sinusoidal rotation of a full-field optokinetic drum around the stationary animal, and 3) paradigms of visual-vestibular interaction, elicited by combined sinusoidal vestibular and optokinetic stimulation. Stimulation parameters for both head and drum velocity were usually 0.5 Hz, 35 degrees/s peak velocity. 2. Y group cells respond vigorously during visual following and during suppression of the VOR (produced by in-phase rotation of the head and the optokinetic drum); the response is approximately in-phase with eye velocity during visual following, and approximately in-phase with head velocity during suppression of the VOR. During the VOR in darkness, Y cells usually exhibit only slight modulation. The results suggest a linear interaction of visual following and vestibular signals on Y cells during vertical visual-vestibular interaction. Taking into account the excitatory projection of Y cells to superior rectus and inferior oblique motoneurons, a causal role of the Y group in rapid modification of VOR gain during visual-vestibular interaction is suggested. 3. Nine Y neurons from two animals were recorded continuously, for periods ranging from 30 min to 5 h, while the VOR was being adapted to higher or lower gain. Progressive changes of the gain of the VOR in darkness were evident after approximately 30 min from the initiation of head rotation under visual-vestibular mismatch. Consistent changes of the gain and/or phase of the neuronal response during the VOR in darkness were noted in all cases. The phase of the neuronal response gradually approximated head velocity phase during adaptation of the VOR to low gain, increases in the neuronal gain thereafter ensued; the opposite changes were observed during adaptation of the VOR to high gain. 4. Sixteen Y cells were recorded from 1 animal chronically adapted to high VOR gain with the use of magnifying lenses, and 35 cells were recorded from 2 animals chronically adapted to low VOR gain with the use of miniaturizing lenses.(ABSTRACT TRUNCATED AT 400 WORDS)

Adaptation, Physiological↗

Dorsal Y group in the squirrel monkey. II. Contribution of the cerebellar flocculus to neuronal responses in normal and adapted animals.

1. The effects of electrical pulse stimulation and temporary pharmacological inactivation of the ipsilateral cerebellar flocculus on the activity of single Y group cells were studied in three alert squirrel monkeys. The extent of the flocculus was mapped by multiunit recording and by electrical pulse train stimulation, which elicited slow eye movement. 2. Single electrical pulse stimulation of the flocculus (0.1-ms constant current, 25-400 microA) resulted in inhibition of all 24 Y cells examined. The inhibition was evidenced as a cessation of cell firing for varying periods [8.8 +/- 2.4 (SD) ms] after the stimulus. The latency of inhibition (0.71 +/- 0.34 ms) suggests that the effect was due to direct activation of Purkinje cells monosynaptically projecting to the Y group. 3. The gamma-aminobutyric acid (GABA) agonist muscimol was used to temporarily inactivate the flocculus while recording from single Y neurons. After control responses of cells under various behavioral paradigms were collected, muscimol (total volume of 3-4 microliters of 2.0% muscimol in saline) was injected in the flocculus through a pair of fine syringes. With this technique, the contribution of the flocculus to the signal content of Y group cells was examined, both in the animals with normal vestibuloocular reflex (VOR) gain (5 cells in 3 animals) and after adaptation of the VOR to either high (5 cells in 1 animal) or low gain (7 cells in 2 animals). 4. In the normal animal, pharmacological floccular inactivation resulted in increased dc firing and in the loss of normal modulation with eye velocity. Modulation during visual-vestibular interactions was also lost, so cell responses did not differ from those during the VOR in darkness. Only minor changes (usually gain increases) in the latter response were noted after flocculus inactivation. The results suggests an extrafloccular input source to the Y group, conveying head velocity information. We believe that this input originates in the brain stem, probably in the superior vestibular nucleus. 5. To examine whether the adapted responses of Y cells during the VOR in darkness are due to their floccular input, single cells were studied before and after pharmacological floccular inactivation, in animals whose VOR had been adapted.(ABSTRACT TRUNCATED AT 400 WORDS)

Adaptation, Physiological↗

Mechanical indentation of the vestibular labyrinth and its relationship to head rotation in the toadfish, Opsanus tau.

1. In the present study we examine the response of the semicircular canal of the toadfish (Opsanus tau) to head rotation and to mechanical indentation of the membranous labyrinth. The relationship between the two stimuli is described by a new elastohydrodynamic model that delineates the three-dimensional (3-D) spatiotemporal distribution of endolymph pressure and flow. In vivo electrophysiological recordings of primary afferents supplying the horizontal canal (HC) were employed to validate the model predictions. Data were collected from 213 afferents in 18 fish during independent head rotation. HC indentation, utricle (U) indentation, and paired stimuli. To quantify the afferent response and the relationship between the applied sinusoidal stimuli, the magnitude (gain) and temporal relationship (phase) of the first harmonic of modulation were calculated and compared with theoretical predictions. 2. A mathematical based extensively on the 3-D morphology of a toadfish labyrinth and the physical properties of endolymph is presented to describe the relationship between head rotation and mechanical indentation. All model parameters specifying labyrinthine morphology and physical properties of endolymph are known; the model contains no free parameters. New results are independent of the structural properties of the cupula. The analysis employs an asymptotic solution of the Navier-Stokes equations in the three toroidal ducts that includes the 3-D fluid-structure interaction taking place within the enlarged ampulla. The solution addresses the differential pressure (delta P) acting across the cupula and the dilatational pressure acting on both sides of the cupula. The analysis quantifies the hydrodynamics of the HC for mechanical indentations of the long and slender portion of the canal duct (HC indentation) and the U (U indentation). Results specifically relate the indentation stimuli to head rotation. Linear commutations of HC indentation, U indentation, and rotation stimuli are analyzed by matching delta P acting across the cupula for the three stimulus modalities. 3. HC afferents show a linear correspondence between HC indentation, U indentation, and rotation stimuli. Specific experimental results for sinusoidal stimuli at frequencies < 2 Hz show 1) +/- 1 micron-HC indentation commutates with +/- 4 degrees/s rotation, 2) + 1-micron HC indentation commutates with -/+ 15-microns U indentation, and 3) -/+ 15-microns U indentation commutates with +/- 4 degrees/s rotation. These results were obtained by adjusting the relative amplitude and phase of two stimuli presented simultaneously to achieve destructive interaction that minimizes the afferent modulation (balanced). Equivalent results were obtained using afferent responses to the stimuli applied independently.(ABSTRACT TRUNCATED AT 400 WORDS)

Afferent Pathways↗

Properties of superior vestibular nucleus flocculus target neurons in the squirrel monkey. I. General properties in comparison with flocculus projecting neurons.

1. Using single-unit recording and microstimulation methods, a group of flocculus target neurons (FTNs) were identified in the superior vestibular nucleus (SVN) and were studied using visual-vestibular interaction paradigms in alert squirrel monkeys. The response properties of these FTNs were characterized and compared with those of flocculus projecting neurons (FPNs). 2. FTNs were monosynaptically inhibited by single-pulse flocculus stimulation. The mean inhibition latency was 1.0 +/- 0.57 (SD) ms (n = 40) and the mean inhibition period was 6.7 +/- 2.69 ms. FTNs were also monosynaptically activated by VIIIth nerve stimulation. The mean response latency was 1.10 +/- 0.25 ms (n = 12). This is about the same as that of the FPNs (1.14 +/- 0.16 ms, n = 17). 3. The most characteristic response property of the FTNs is their firing rate modulation during visual following eye movements induced by sinusoidal rotation of an optokinetic drum at 0.5 Hz. This modulation was mainly related to eye velocity and was therefore termed a visual following eye velocity signal. The average eye velocity gain for all FTNs is 0.79 spikes.s-1.deg-1.s-1. In contrast, the responses of FPNs were not modulated under the same conditions. 4. Even though FTNs are inhibited by the flocculus, they have a relatively higher mean firing rate (124 +/- 23 spikes/s, n = 45) than FPNs (66 +/- 28 spikes/s, n = 42). The underlying mechanism may be related to commissural facilitation of FTNs and commissural inhibition of FPNs. 5. Thirty FTNs were identified as upward eye velocity FTNs because their firing rate increased for upward eye velocity during a visual following eye movement. The mean eye velocity sensitivity was 1.09 spikes.s-1.deg-1.s-1. Most of these cells also modulated during vestibuloocular reflex (VOR) in the dark, with firing rate increasing for downward head velocity. During VOR suppression the firing rate either did not modulate or modulated in phase with head or drum velocity with a smaller amplitude in comparison with the response during visual following. For all cells (with 1 exception) the response during a visual following eye movement can be approximately predicted by a linear vectorial subtraction of the response during VOR suppression and the response during VOR in the dark [modulation response vector of FTNs during visual following of the optokinetic stimulus (OKR) approximately modulation response vector of FTNs during VOR suppression-modulation response vector of FTNs during VOR in the dark].(ABSTRACT TRUNCATED AT 400 WORDS)

Animals↗

Properties of superior vestibular nucleus flocculus target neurons in the squirrel monkey. II. Signal components revealed by reversible flocculus inactivation.

1. Seven upward eye velocity flocculus target neurons (FTNs) and two flocculus projecting neurons (FPNs) were studied before and after ipsilateral flocculus inactivation by injection of muscimol in the alert squirrel monkey. An additional seven FTNs and seven FPNs recorded from the corresponding FTN and FPN areas were recorded after injection. Response properties of FTNs and FPNs were characterized by visual-vestibular interaction paradigms and were compared before and after flocculus inactivation. 2. In FTNs the mean firing rate increased within 2-5 min after muscimol injection in the flocculus and reached a plateau level in approximately 10-20 min. The average mean firing rate for seven FTNs increased from 117 to 174 spikes/s, a net increase of 57 spikes/s (49%). Accompanying the large increase of the mean firing rate, a spontaneous nystagmus in the darkness developed with the slow phase directed upward and contralateral. 3. The firing rate modulation during visual following of a sinusoidal optokinetic drum (0.5 Hz) decreased within 2-5 min after muscimol injection in the flocculus and reached a level of 0 in approximately 10-20 min for all FTNs. After that, some cells remained unmodulated for the period of recording; other cells gradually reversed their phase and developed a modulation out of phase with drum velocity. The depletion of the visual following eye velocity signal on superior vestibular nucleus (SVN) FTNs accompanied a small but consistent decrease of visual following eye velocity amplitude. The average maximum decrease of eye velocity was 26 +/- 9% (mean +/- SD). 4. After flocculus inactivation, even though the modulation response at 0.5 Hz during visual following was abolished, a slow-component eye velocity signal with the same on direction was revealed by a constant-velocity optokinetic stimulus. It is concluded that there are at least two kinds of eye velocity signals during the optokinetic response. These signals are combined at the FTNs and are subsequently relayed to the oculomotor neurons. The source of the fast component is the flocculus, and the source of the slow component is another, as yet unidentified brain structure. 5. The effect of flocculus inactivation on the modulation amplitude during the vestibuloocular reflex (VOR) in darkness was variable: two cells did not change, two cells decreased, and three cells increased their amplitude. The response phase tended to move toward a phase lead, but the change was small. The effect on VOR suppression was more prominent.(ABSTRACT TRUNCATED AT 400 WORDS)

Animals↗