The anatomy and physiology of primate neurons that control rapid eye movements.
Explore the source record for details and available documents.
Animals↗
Biomedical subjects
S M Highstein
Publications and source records attributed to S M Highstein.
Lesions of the posterior commissure disable the vertical neural integrator of the primate oculomotor system.
1. Spontaneous saccades, vestibuloocular responses (VOR), and optokinetic nystagmus were recorded in three squirrel monkeys before and after chemical or electrolytic lesion of the posterior commissure (PC). 2. PC lesions produced abnormal vertical eye movements, in particular, 1) Postsaccadic drifts, and 2) VOR gain reduction and phase advance more pronounced at lower frequencies of sinusoidal head rotation. Horizontal eye movements were much less affected (or normal). 3. We conclude that PC fibers are necessary for conveying the output of the vertical neural integrator to vertical oculomotor-neurons.
Abducens Nerve↗
Sensory transduction of head velocity and acceleration in the toadfish horizontal semicircular canal.
1. Sinusoidal mechanical indentation of the long-and-slender limb of the horizontal semicircular canal and/or utricle was used to produce adequate stimulation of the labyrinth. Indentation of the canal increased, while indentation of the utricle decreased the afferent discharge rate. This follows because indentation of the canal and utricle produce oppositely directed mechanical stimuli as defined by endolymph flow, transcupular pressure, and cupular deflection. Simultaneous in-phase indentations of both the canal and utricle, with amplitudes adjusted to produce equal (but opposite) magnitudes of afferent response modulation, generate destructive interaction that minimizes the afferent modulation, whereas sinusoidal indentation 180 degrees out-of-phase generates constructive interaction that maximizes the afferent modulation. This observation correlates directly with analysis of the labyrinthine elasto-hydrodynamics which predicts that balanced in-phase indentations minimize macromechanical endolymph flow through the ampullary cross section and maximize the dilatational pressure within the ampulla acting equally on both sides of the cupula and across the labyrinthine wall. 2. Two groups of afferents are identified according to their response to balanced sinusoidal indentation of the canal limb and the utricle. In one group there is complete destructive interaction and the afferent response can be effectively nulled by adjusting the relative amplitude and phase of the two stimuli. In the second group a residual afferent response remains that cannot be nulled. The residual is described in the model as unit-specific sensitivity to dilatational pressure acting equally on both sides of the cupula.
Afferent Pathways↗
Properties of superior vestibular nucleus neurons projecting to the cerebellar flocculus in the squirrel monkey.
1. Properties of superior vestibular nucleus (SVN) neurons and their projection to the cerebellar flocculus were studied in alert squirrel monkeys by using chronic unit and eye movement recording and microstimulation techniques. Twenty-three cells were antidromically activated from the ipsilateral flocculus, and seventeen of these were also orthodromically activated from the ipsilateral VIIth nerve at monosynaptic latencies. Only 1 of these 23 units was also inhibited by flocculus stimulation. According to their response properties, 9 of the cells were pure vestibular, 2 were vestibular-pause, and 12 were position-vestibular cells. The mean eye position sensitivity of these position-vestibular cells was significantly lower than that of cells projecting to the oculomotor nucleus (OMN). No eye movement-only neurons were antidromically activated from the flocculus. No cells could be antidromically activated from both the oculomotor nucleus and the flocculus.
Animals↗
Anatomical organization of the brainstem octavolateralis area of the oyster toadfish, Opsanus tau.
Anatomical studies were undertaken to analyze the brainstem organization of the auditory, vestibular, and lateral line nuclei in a teleost, the oyster toadfish, Opsanus tau. Neuronal cytoarchitectonics and horseradish peroxidase label of cranial nerves were utilized to delineate the borders of the five octavus and two lateralis brainstem nuclei. Each of the eight octavolateralis nerves were labeled individually to compare and contrast their central projections. Projections of the three semicircular canals were found to be largely overlapping. Terminal fields were observed within the eminentia granularis and in each of the octavus nuclei. The nucleus anterior octavus was reciprocally innervated by the semicircular canals and the saccule. The canals terminated heavily in the ventral portions of the anterior octavus, whereas the saccule terminated extensively in the dorsal nuclear portions. The saccule also distributed terminals throughout the octavus cell column, including a light terminal field within the dorsal, medial, and anterior portions of the descending octavus nucleus, a region densely innervated by this end-organ in other species. These results suggest that the anterior octavus nucleus may have a dual function. The dorsal portions may be an auditory relay nucleus, whereas the ventral portions may subserve vestibular function. Utriclar and lagenar afferents also terminated throughout the octavus cell column. Afferents of the anterior and posterior lateral lines ended within the eminentia granularis and the lateral line nuclei. Semicircular canal afferents and lateral line afferents appeared completely segregated within the eminentia. The above results are useful as an aid in the understanding of an ongoing, comprehensive functional analysis of auditory and vestibular mechanisms in toadfish and complement previous work on the efferent vestibular and sound-producing motor systems. Examination of toadfish contributes to a more general and complete overview of the octavolateralis area of teleosts and the eventual identification of primitive and derived patterns of octaval organization. Additionally, this work may permit the further demonstration of species-typical characters that may indicate adaptations to particular behavioral repertoires.
Animals↗
The efferent control of the organs of balance and equilibrium in the toadfish, Opsanus tau.
All vertebrates are endowed with a vestibular efferent system (EVS) consisting of somata within the central nervous system with long axons exiting the brain to innervate the labyrinth. Behaviorally relevant stimuli related to feeding and/or aggressive behaviors and conditions leading to enhanced attentional states or alerting activate the EVS. Increased EVS activity modifies the resting rate and response dynamics to motion of vestibular afferents. This modification is nonuniform across the fiber spectrum of the semicircular canals, for example, affecting the more-sensitive, low-spontaneous-activity cells more profoundly than their less-sensitive counterparts. The cellular bases for EVS effects are excitatory axoaxonic synapses upon primary afferents and axosomatic inhibitory synapses upon hair cells.
Afferent Pathways↗
Inputs from regularly and irregularly discharging vestibular nerve afferents to secondary neurons in squirrel monkey vestibular nuclei. III. Correlation with vestibulospinal and vestibuloocular output pathways.
1. A previous study measured the relative contributions made by regularly and irregularly discharging afferents to the monosynaptic vestibular nerve (Vi) input of individual secondary neurons located in and around the superior vestibular nucleus of barbiturate-anesthetized squirrel monkeys. Here, the analysis is extended to more caudal regions of the vestibular nuclei, which are a major source of both vestibuloocular and vestibulospinal pathways. As in the previous study, antidromic stimulation techniques are used to classify secondary neurons as oculomotor or spinal projecting. In addition, spinal-projecting neurons are distinguished by their descending pathways, their termination levels in the spinal cord, and their collateral projections to the IIIrd nucleus. 2. Monosynaptic excitatory postsynaptic potentials (EPSPs) were recorded intracellularly from secondary neurons as shocks of increasing strength were applied to Vi. Shocks were normalized in terms of the threshold (T) required to evoke field potentials in the vestibular nuclei. As shown previously, the relative contribution of irregular afferents to the total monosynaptic Vi input of each secondary neuron can be expressed as a %I index, the ratio (x100) of the relative sizes of the EPSPs evoked by shocks of 4 x T and 16 x T. 3. Antidromic stimulation was used to type secondary neurons as 1) medial vestibulospinal tract (MVST) cells projecting to spinal segments C1 or C6; 2) lateral vestibulospinal tract (LVST) cells projecting to C1, C6; or L1; 3) vestibulooculo-collic (VOC) cells projecting both to the IIIrd nucleus and by way of the MVST to C1 or C6; and 4) vestibuloocular (VOR) neurons projecting to the IIIrd nucleus but not to the spinal cord. Most of the neurons were located in the lateral vestibular nucleus (LV), including its dorsal (dLV) and ventral (vLV) divisions, and adjacent parts of the medial (MV) and descending nuclei (DV). Cells receiving quite different proportions of their direct inputs from regular and irregular afferents were intermingled in all regions explored. 4. LVST neurons are restricted to LV and DV and show a somatotopic organization. Those destined for the cervical and thoracic cord come from vLV, from a transition zone between vLV and DV, and to a lesser extent from dLV. Lumbar-projecting neurons are located more dorsally in dLV and more caudally in DV. MVST neurons reside in MV and in the vLV-DV transition zone.(ABSTRACT TRUNCATED AT 400 WORDS)
Animals↗
Morphophysiology of synaptic transmission between type I hair cells and vestibular primary afferents. An intracellular study employing horseradish peroxidase in the lizard, Calotes versicolor.
Intracellular records with glass microelectrodes filled with horseradish peroxidase (HRP) were taken from primary afferents of the horizontal semicircular canal in the lizard, Calotes versicolor. A coefficient of variation (CV) of the interspike intervals of spontaneous action potentials (APs) was calculated and correlated with the terminal morphologies of afferents within the canal crista. Irregular fibers with CV greater than 0.4 always correlated with a nerve chalice or calyx afferent terminal expansion surrounding one or more type I hair cells; more regular fibers with CV less than 0.4 always correlated with a dimorphic or bouton only terminal expansion of afferents. Afferents with a CV greater than 0.4 demonstrated miniature excitatory postsynaptic potentials (mEPSPs) that summated to initiate APs. APs were blocked by tetrodotoxin and mEPSP frequency was modulated by caloric stimulation. Cobalt application reversibly blocked mEPSPs. Electron microscopic examination of physiologically studied afferents with CV greater than 0.4 revealed synaptic profiles consisting of typical synaptic bodies and synaptic vesicles in the type I hair cell presynaptic to the nerve chalice. Examples of the interspike baseline in regular and irregular afferents suggest differential modes of impulse initiation in these two fiber types.
Action Potentials↗
Action of the octavolateralis efferent system upon the lateral line of free-swimming toadfish, Opsanus tau.
The activation and action of the octavolateralis efferent system was studied by chronic recordings of discharge patterns from putative efferent and single primary afferent neurons in alert, free-swimming toadfish. Efferent axons isolated in the anterior lateral line nerve showed phasic discharges following touch stimuli applied to the head or trunk and demonstrated sustained discharges to visual stimuli. Resting discharge patterns of primary afferents were categorized into irregular, burster, regular, and silent classes. Afferent discharges were often modulated by low frequency (less than 1 Hz) water movement around the head generated during respiratory movements. When fish with recording electrodes implanted in the lateral line nerve were visually stimulated, modulated peak discharges and average (DC) firing rates were inhibited in irregular-type units only. Inhibition of irregular-type afferent neurons also followed visual presentation of natural prey and persisted long after prey stimuli were removed from view. The inhibitory action upon lateralis afferents when activated by biologically significant visual stimuli leads to the hypothesis that the octavolateralis efferent system functions in the peripheral processing of information carried by the lateral line in natural settings.
Animals↗
The squirrel monkey vestibulo-ocular reflex and adaptive plasticity in yaw, pitch, and roll.
The vestibulo-ocular reflex (VOR) was studied in adult squirrel monkeys before and after adaptation to magnifying and minifying viewing conditions. Monkeys were subjected to broadband (0.05-0.71 Hz) conditioning rotation for six hours in head yaw, pitch, and roll on separate occasions, and the VORs in these three planes were studied in darkness to assess adaptive plasticity in the reflexes. The gain of the horizontal VOR (H-VOR) averaged 0.8 across the frequency bandwidth studied (0.025-4 Hz). Phase was near 0 degrees from 4 to around 0.1 Hz, but developed a progressive lead as frequency declined further. Normal vertical VOR (V-VOR) gain climbed from 0.6 at 0.025 Hz to near 1 as frequency increased to 4 Hz. Phase lead was more pronounced at low frequencies than in the H-VOR. The normal torsional VOR (T-VOR) qualitatively resembled the V-VOR, showing similar phase but lower gains (0.3-0.7) across the frequency bandwidth. These findings suggest that the dynamics of the V-VOR and T-VOR resemble canal characteristics more closely than does the H-VOR. After adaptation to visual minification and conditioning rotation (0.5X for yaw and pitch, 0X for roll), gain decreased in each of the planes of conditioning. Similarly, gain increased in the plane of conditioning after adaptation to visual magnification (2X). The adaptive changes were greater at low (0.025-1 Hz) than at high (2.5-4 Hz) frequencies, and were more robust when gain was driven downward than upward. However, control (sham) adaptation experiments showed that VOR gain tended to drop slightly over 6 h in the absence of adaptive drive to do so, suggesting that the gain modifications may be more symmetric when referenced to the control. Adaptive VOR gain enhancement or decrement in the plane of conditioning did not result in systematic and parallel changes in orthogonal VOR planes.
Acclimatization↗
The central nervous system efferent control of the organs of balance and equilibrium.
The vestibular labyrinth is innervated by both primary afferent nerves and efferent axons with cell bodies located in the central nervous system. Efferent terminals are found on both hair cells and on primary afferent axons. Acetylcholine is the major efferent transmitter, but enkephalin and calcitonin gene-related peptide (CGRP) have also been localized to efferent terminals and somata. The efferent vestibular nuclei are bilaterally organized in the majority of species. Semicircular canal primary afferents have been classified by their sensitivity and phase in response to rotation. Electrical activation of efferents in monkey and fish increases afferent resting discharge and reduces afferent gain to adequate stimulation. Effects are most profound on high-gain, phase-advanced (re. velocity) afferents. Experiments in alert animals indicate that multiple sensory modalities can activate the efferent system.
Animals↗
Structure of the primate oculomotor burst generator. I. Medium-lead burst neurons with upward on-directions.
1. To investigate the structure of the primate burst generator for vertical saccades, we obtained intra-axonal records from vertical medium-lead burst neurons with upward on-directions (UMLBs) in alert, behaving squirrel monkeys, while monitoring their spontaneous eye movements. After physiological characterization, these UMLBs were injected with horseradish peroxidase. 2. UMLBs (n = 14) had no spontaneous activity and emitted bursts of action potentials that preceded rapid eye movements by approximately 6 ms. Parameters of the burst (duration and number of spikes) were highly correlated with parameters of the rapid eye movement (duration and amplitude of the upward displacement of the eyes). 3. The axons of six UMLBs projected to the oculomotor complex. Their somata (4 were recovered) were all in the rostral interstitial nucleus of the medial longitudinal fasciculus (riMLF). Their axons traveled caudally in the medial longitudinal fasciculus (MLF) and ramified in the interstitial nucleus of Cajal (NIC) before entering the oculomotor nucleus. Five axons terminated bilaterally in the subdivisions innervating the superior rectus and inferior oblique muscles and therefore were presumed to be excitatory. One axon terminated in the ipsilateral inferior rectus and superior oblique subdivisions of the oculomotor complex and was presumed to be inhibitory. 4. Additionally, our data demonstrate that the nucleus of the posterior commissure (nPC) may also contain UMLBs. The axon of one such neuron crossed the midline within the posterior commissure and provided terminal fields to the contralateral nPC, riMLF, NIC, and the mesencephalic reticular formation but not to the oculomotor complex. 5. In conclusion, our data demonstrate that the rostral mesencephalon of the monkey contains neurons that have both the activity and the connections that are necessary either to provide motoneurons innervating extraocular muscles of both eyes with the pulse of activity they display during upward saccades or to inhibit their antagonists. Furthermore, our data demonstrate that some UMLBs are better suited for closing the feedback path of the local feedback loop rather than for providing direct input to extraocular motoneurons.
Action Potentials↗
Structure of the primate oculomotor burst generator. II. Medium-lead burst neurons with downward on-directions.
1. To investigate the morphology and physiology of vertical medium-lead burst neurons with downward on-directions (DMLBs), we impaled midbrain axons and recorded their discharge patterns in relation to spontaneous saccades of alert, behaving squirrel monkeys. Selected axons were injected with horseradish peroxidase and morphologically characterized. 2. DMLBs emitted bursts of impulses that preceded rapid eye movements by approximately 5 ms. Parameters of the burst (duration and number of spikes) were highly correlated with parameters of the saccadic eye movement (duration and amplitude of the downward displacement of the eyes). 3. Somata of DMLBs were recovered in the rostral interstitial nucleus of the medial longitudinal fasciculus (riMLF, n = 14), and in the interstitial nucleus of Cajal (NIC, n = 2). Fibers originating from riMLF DMLBs projected, usually ipsilaterally, to the NIC as well as in the inferior rectus and the superior oblique subdivisions of the oculomotor complex. The axons of NIC DMLBs projected to the ipsilateral riMLF, NIC, and the mesencephalic reticular formation but not to the oculomotor complex. 4. Our data demonstrate that some DMLBs can provide extraocular motoneurons of both eyes with the pulse of activity they display during downward saccades. In addition, such neurons can supply the NIC with one of the signals that this nucleus is thought to integrate to extract an estimate of the vertical eye position. Finally, our data demonstrate the existence of DMLBs that do not establish direct connections with oculomotoneurons.
Action Potentials↗
Morphological correlates of response dynamics and efferent stimulation in horizontal semicircular canal afferents of the toadfish, Opsanus tau.
1. We used the intraaxonal labeling technique to study correlations between the terminal dendritic morphology of horizontal semicircular canal primary afferents and their response dynamics to sinusoidal head rotation and combined electrical stimulation of central efferent vestibular neurons. Thirty-eight canal afferents were identified by their sensitivity and phase of response to rotation between 0.1 and 1.0 Hz (+/- 10 degrees/s) and were subsequently labeled with horseradish peroxidase or biocytin. The afferent's dendritic field and synaptic specializations in the neuroepithelium of the crista were examined under light microscopy. 2. Rate and regularity of background discharge of the afferent were not correlated with its axon diameter or relative location of its dendritic field in the crista. 3. Response sensitivity of the afferent to rotation was correlated both with the relative location of its dendritic field in the crista and with the number of terminal endings it possesses. Afferents having low sensitivities, slow dynamics, and few terminal endings supply the peripheral portions of the crista; afferents with higher sensitivities, faster dynamics, and greater number of terminal endings supply the more central portions. It is suggested that the differences in sensitivity among the afferents reflect principally the variations in both the cupular dynamics along the crista and the number of possible hair cell contact sites in the neuroepithelium. 4. Response phase of the afferent was correlated only with the extent of its dendritic processes along the transverse axis of the crista. Afferents having transversely oriented dendritic fields had less phase lags relative to acceleration than did those having a more longitudinally oriented dendritic field. 5. Efferent stimulation produced a change in both the afferent's discharge rate and its response sensitivity to rotation. Afferents discharge rate and its response sensitivity to rotation. Afferents having a centrally located dendritic field and acceleration afferents, defined by their response to rotation, were the most affected by efferent stimulation. These results suggest that efferent innervation is either directed toward, or most efficacious in, the central regions of the crista and that it may select specific hair cell-afferent complexes.
Animals↗
A structural basis for Hering's law: projections to extraocular motoneurons.
Conjugate eye movements are executed through the concurrent activation of several muscles in both eyes. The neural mechanisms that underlie such synergistic muscle activations have been a matter of considerable experimentation and debate. In order to investigate this issue, the projections of a class of primate premotoneuronal cells were studied, namely, the vertical medium-lead burst neurons (VMLBs), which drive vertical rapid eye movements. Axons of upward VMLBs ramify bilaterally within motoneuron pools that supply the superior rectus and inferior oblique muscles of both eyes. Axons of downward VMLBs ramify ipsilaterally in the inferior rectus portion of the oculomotor nucleus and in the trochlear nucleus. Thus, VMLBs can drive vertical motoneuron pools of both eyes during conjugate vertical rapid eye movements; these data support Hering's law.
Action Potentials↗
Visually mediated inhibition of lateral line primary afferent activity by the octavolateralis efferent system during predation in the free-swimming toadfish, Opsanus tau.
The activity of single lateral line afferent neurons was chronically recorded in free-swimming toadfish. CNS efferent neurons, known to be inhibitory upon peripheral lateral line mechanoreceptors, were activated by stroboscopic and natural visual stimuli. Discharges from irregular-type afferents caused by water movement relative to lateral line neuromasts decreased following stroboscopic stimulation of unrestrained and behaving fish. Visual presentation of natural prey also decreased mechanically evoked afferent firing rates. We show that visual stimuli can activate the efferent system and function in the peripheral processing of mechanical stimuli to the lateral line in biologically relevant contexts.
Animals↗
Resting discharge and response dynamics of horizontal semicircular canal afferents of the toadfish, Opsanus tau.
The response dynamics of 66 primary afferents of the horizontal semicircular canal were studied in the toadfish using sinusoidal, rotational stimuli from 0.001-10 Hz at amplitudes of 5-100 degrees/sec. Twelve afferents were also tested to constant velocity trapezoids. Responses to sinusoids were used to classify afferents into 3 broad groups: (1) low-gain afferents that maintain a relatively linear response re: stimulus velocity across most of the frequency and amplitude spectra tested; (2) high-gain afferents that have a velocity sensitivity but also show a high-frequency gain enhancement and phase advance; and (3) so-called acceleration afferents that have a response more in phase with stimulus acceleration than velocity across the tested bandwidth. The afferent's background discharge was examined in relation to its rotational response. Low-gain afferents have regular spacing of interspike intervals. High-gain and acceleration afferents have a widely variable discharge regularity that is apparently unrelated to their rotational responses. Input/output transfer models were fit to the response data to describe the low- and high-pass filtering properties of the 3 afferent groups.
Animals↗
Efferent vestibular system in the toadfish: action upon horizontal semicircular canal afferents.
The influence of the efferent vestibular system (EVS) upon the background discharge and response dynamics of horizontal semicircular canal afferents was examined in the toadfish. In one set of experiments the EVS was activated using a behavioral paradigm; in the second, electrical shocks were applied to the efferent vestibular nucleus in the brain stem. The afferent's background discharge and responses to rotation were recorded before and during efferent stimulation. Both EVS activation paradigms gave qualitatively similar results: a facilitation of the afferent's rate, while the animal was at rest or in motion, and a reduction in response sensitivity. Afferents were not affected uniformly: low-gain, velocity-sensitive afferents were weakly influenced, while high-gain and acceleration afferents having low rates were the most excited. The afferents' phase of response was unmodified by electrical EVS stimulation. In many afferents a prominent form of response nonlinearity is discharge silencing over large portions of the stimulus cycle. Efferent-evoked rate increase was often sufficient to produce a full-cycle bidirectional response. Caloric facilitation of afferent rate confirmed that the EVS-induced sensitivity decrease was rate independent. These results show a dual action of the efferent system: (1) facilitating the afferent's rate and (2) reducing its sensitivity to adequate stimulation that may be correlated with the dual EVS synaptic innervation of the labyrinth, namely postsynaptic efferent-afferent synapses and presynaptic efferent-hair cell synapses.
Animals↗