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Brain stem pursuit pathways: dissociating visual, vestibular, and proprioceptive inputs during combined eye-head gaze tracking.

Eye-head (EH) neurons within the medial vestibular nuclei are thought to be the primary input to the extraocular motoneurons during smooth pursuit: they receive direct projections from the cerebellar flocculus/ventral paraflocculus, and in turn, project to the abducens motor nucleus. Here, we recorded from EH neurons during head-restrained smooth pursuit and head-unrestrained combined eye-head pursuit (gaze pursuit). During head-restrained smooth pursuit of sinusoidal and step-ramp target motion, each neuron's response was well described by a simple model that included resting discharge (bias), eye position, and velocity terms. Moreover, eye acceleration, as well as eye position, velocity, and acceleration error (error = target movement - eye movement) signals played no role in shaping neuronal discharges. During head-unrestrained gaze pursuit, EH neuron responses reflected the summation of their head-movement sensitivity during passive whole-body rotation in the dark and gaze-movement sensitivity during smooth pursuit. Indeed, EH neuron responses were well predicted by their head- and gaze-movement sensitivity during these two paradigms across conditions (e.g., combined eye-head gaze pursuit, smooth pursuit, whole-body rotation in the dark, whole-body rotation while viewing a target moving with the head (i.e., cancellation), and passive rotation of the head-on-body). Thus our results imply that vestibular inputs, but not the activation of neck proprioceptors, influence EH neuron responses during head-on-body movements. This latter proposal was confirmed by demonstrating a complete absence of modulation in the same neurons during passive rotation of the monkey's body beneath its neck. Taken together our results show that during gaze pursuit EH neurons carry vestibular- as well as gaze-related information to extraocular motoneurons. We propose that this vestibular-related modulation is offset by inputs from other premotor inputs, and that the responses of vestibuloocular reflex interneurons (i.e., position-vestibular-pause neurons) are consistent with such a proposal.

Action Potentials↗

In vivo analysis of proprioceptive coding and its antidromic modulation in the freely behaving crayfish.

Although sensory nerves in vitro are known to convey both orthodromic (sensory) and antidromic (putatively modulating) action potentials, in most cases very little is known about their bidirectional characteristics in intact animals. Here, we have investigated both the sensory coding properties and antidromic discharges that occur during real walking in the freely behaving crayfish. The activity of the sensory nerve innervating the proprioceptor CBCO, a chordotonal organ that monitors both angular movement and position of the coxo-basipodite (CB) joint, which is implicated in vertical leg movements, was recorded chronically along with the electromyographic activity of the muscles that control CB joint movements. Two wire electrodes placed on the sensory nerve were used to discriminate orthodromic from antidromic action potentials and thus allowed for analysis of both sensory coding and antidromic discharges. A distinction is proposed between 3 main classes of sensory neuron, according to their firing in relation to levator muscle activity during free walking. In parallel, we describe 2 types of antidromic activity: one produced exclusively during motor activity and a second produced both during and in the absence of motor activity. A negative correlation was found between the activity of sensory neurons in each of the 3 classes and identified antidromic discharges during walking. Finally, a state-dependent plasticity of CBCO nerve activity has been found by which the distribution of sensory orthodromic and antidromic activity changes with the physiological state of the biomechanical apparatus.

Action Potentials↗

Proprioceptive input patterns elevator activity in the locust flight system.

1. In the locust, Locusta migratoria, the roles of two groups of wing sense organs, hind wing tegulae and wing-hinge stretch receptors, in the generation of the flight motor pattern were investigated. A preparation was employed that allowed the intracellular recording of neural activity in almost intact tethered flying locusts or after selective manipulations of sensory input. The functions of the two sets of receptors were assessed 1) by studying the phases of their discharges in the wingbeat cycle (Fig. 3), 2) by the selective ablation of input from the receptors (Figs. 4-7), and 3) by the selective stimulation of the receptor afferents (Figs. 8-12). 2. Input from the tegulae was found to be responsible for the initiation of elevator activity (Figs. 9 and 10) and for the generation of a distinct initial rapid depolarization (Figs. 4, 5, and 8) characteristic of elevator motor neuron activity in intact locusts (Figs. 1 and 16). 3. Input from the wing-hinge stretch receptors was found to control the duration of elevator depolarizations by the graded suppression of a second late component of the elevator depolarizations as wingbeat frequency increased (Figs. 6, 7, 11, and 12). The characteristics of this late component of elevator activity suggested that it is generated by the same (central nervous) mechanism that produces the elevator depolarizations recorded in deafferented animals (Fig. 2). Apparently this late component contributes to the intact pattern of elevator depolarizations only at lower wingbeat frequencies and is abolished by the action of stretch-receptor input at frequencies above approximately 15 Hz (Figs. 1, 2, and 4). At these high wingbeat frequencies elevator activity is dominated by the rapid depolarizations generated as a result of tegula input. 4. The present study demonstrates 1) that the timing of elevator motor neuron activity is determined by phasic afferent input from tegulae and stretch receptors and 2) that input from the stretch receptors controls the duration of elevator activity in the wingbeat cycle following the wing movement that was responsible for the generation of the receptor discharge.

Afferent Pathways↗

Binocular immobilization induced by paralysis of the extraocular muscles of one eye: evidence for an interocular proprioceptive mechanism.

1. Spontaneous changes in the positions of both eyes were measured in anesthetized cats before and after infusion of paralytic or anesthetic agents directly into the extraocular muscle capsule behind one eye. 2. Before retrobulbar injection, large changes in eye position were observed in both eyes. The position changes of each eye were independent of each other and often in opposite directions. 3. Application of a paralytic agent into the orbit of one eye reduced the spontaneous position changes in that eye to a very low level. Unexpectedly, the changes in the position of the other, untreated eye were also greatly reduced. 4. Control experiments demonstrated that the binocular immobilization observed after monocular paralysis was not due to 1) leakage of the paralytic agent from the orbit of the treated eye to the orbit of the untreated eye or 2) systemic vascular transport of the paralytic agent. 5. Passive movement of the paralyzed eye did not induce movement of the untreated eye. 6. Application of a local anesthetic agent rather than a paralytic agent to one eye resulted in reversible reduction of movement only in the treated eye, but not in the untreated eye. 7. The results suggest that the reduction of movement in one eye produced by application of a paralytic agent to the other eye is mediated by an afferent neural signal derived from extraocular muscle proprioceptors possibly gated by a central motor control signal.

Anesthetics, Local↗

Cholinergic synaptic transmission between proprioceptive afferents and a hind leg motor neuron in the locust.

1. The physiology and pharmacology of the connections made by stress-sensitive campaniform sensilla on the proximal dorsal tibia of a locust hind leg with a fast extensor tibiae motor neuron (FETi) have been examined. 2. Mechanical stimulation of a campaniform sensillum on the anterior surface of the tibia elicited bursts of spikes in its afferent and a depolarization in FETi. Each afferent spike was followed at short and constant latency by an excitatory postsynaptic potential (EPSP) in FETi, even at high-frequency stimulation. Electrical stimulation of the extensor tibiae muscle with the tibia fixed elicited an antidromic spike in FETi followed by a compound potential which resulted from the activation of the campaniform sensillum afferent. The connections between the campaniform sensillum and FETi was monosynaptic and chemically mediated. 3. Ionophoresis of ACh into the neuropil depolarized FETi, as did the application of the cholinesterase inhibitor physostigmine. Bath application of the cholinergic agonists, nicotine and muscarine, also depolarized FETi, with nicotine causing a reduction in input resistance, while muscarine caused no detectable change in input resistance. Muscarine and the muscarinic agonist oxotremorine also caused rhythmic depolarizations and bursts of spikes in FETi. These effects were seen in low calcium/high magnesium saline to block synaptic transmission and are therefore due to direct effects on FETi. FETi therefore appears to have both nicotinic and muscarinic receptors. 4. The compound potential in FETi, caused by activation of the campaniform sensillum, was reduced by bath application of nicotinic cholinergic antagonists. However, the muscarinic antagonist scopolamine increased the amplitude of the compound potential.(ABSTRACT TRUNCATED AT 250 WORDS)

Animals↗

Hysteresis reduction in proprioception using presynaptic shunting inhibition.

1. The tonic responses of angular-position-sensitive afferents in the metathoracic chordotonal organ of the locust leg exhibit much hysteresis. For a given joint angle, the ratio of an afferent's tonic firing rate after extension to its firing rate after flexion (or vice versa) is typically between 1.2:1 and 3:1 but can be as large as 10:1. Spiking local interneurons, that receive direct inputs from these afferents, can, by contrast, exhibit much less hysteresis (between 1.1:1 and 1.2:1). We tested the hypothesis that presynaptic inhibitory interactions between afferent axons reduces the hysteresis of postsynaptic interneurons by acting as an automatic gain control mechanism. 2. We used two kinds of neural models to test this hypothesis: 1) an abstract nonspiking neural model in which a multiplicative, shunting term reduced the "firing rate" of the afferent and 2) a more realistic compartmental model in which shunting inhibition presynaptically attenuated the amplitude of the action potentials reaching the afferent terminals. 3. The abstract neural model demonstrated the automatic gain control capability of a network of laterally inhibited afferent units. A postsynaptic unit, which was connected to the competitive network of afferents, coded for joint angle without saturating as the strength of the afferent input increased by two orders of magnitude. This was possible because shunting inhibition exactly balanced the increase in the excitatory input. This compensatory mechanism required the sum of the excitatory and inhibitory conductances to be much larger than the leak conductance. This requirement suggested a graded weighting scheme in which the afferent recruited first (i.e., at a small joint angle) received the largest inhibition from each of the other afferents because of the lack of active neighbors, and the afferent recruited last (i.e., at a large joint angle) received the least inhibition because all the other afferents were active. 4. The compartmental model demonstrated that presynaptic shunting inhibition between afferents could decrease the average synaptic conductance caused by the afferents onto the spiking interneuron, thereby counterbalancing the afferents' large average firing rates after movements in the preferred direction. Therefore the total postsynaptic input per unit time did not differ much between the preferred and nonpreferred directions.(ABSTRACT TRUNCATED AT 400 WORDS)

Afferent Pathways↗

Presynaptic inhibition of exteroceptive afferents by proprioceptive afferents in the terminal abdominal ganglion of the crayfish.

1. Exteroceptive hairs that are sensitive to water displacement and touch are distributed over the surface of the tailfan of crayfish. We show that the sensory neurons innervating these hairs receive a primary afferent depolarization (PAD) from sensory neurons innervating a proprioceptor that monitors movements of the endopodite and protopodite of the tailfan. This PAD occurs only during high-velocity movements of the exopodite, which are similar to those that occur during swimming. The effects that the proprioceptor mediate are widespread, so that afferents in four sensory nerve roots of the terminal abdominal ganglion, innervating hairs on the protopodite, exopodite, endopodite, and telson, receive a PAD. The PAD is unlikely to be mediated through monosynaptic pathways because there is no anatomic overlap between the central projections of chordotonal afferents and many of the exteroceptive afferents. The depolarization is associated with a conductance increase and can be increased by the injection of hyperpolarizing current or reversed (approximately 10 mV above resting potential) by injection of depolarizing current. The properties of the presynaptic input are, therefore, consistent with being mediated through chemical synapses. This is supported by the observation in the electron microscope that the exteroceptive afferents receive chemical input synapses. The depolarization is mimicked by gamma-aminobutyric acid and reduced by bath application of picrotoxin or bicuculline, suggesting that it is a depolarizing inhibitory postsynaptic potential. The PAD reduces the amplitude of exteroceptive afferent spikes, an action that is thus likely to reduce transmitter release and the efficacy of synaptic transmission.

Action Potentials↗

Role of proprioceptive signals from an insect femur-tibia joint in patterning motoneuronal activity of an adjacent leg joint.

Interjoint reflex function of the insect leg contributes to postural control at rest or to movement control during locomotor movements. In the stick insect (Carausius morosus), we investigated the role that sensory signals from the femoral chordotonal organ (fCO), the transducer of the femur-tibia (FT) joint, play in patterning motoneuronal activity in the adjacent coxa-trochanteral (CT) joint when the joint control networks are in the movement control mode of the active behavioral state. In the active behavioral state, sensory signals from the fCO induced transitions of activity between antagonistic motoneuron pools, i.e., the levator trochanteris and the depressor trochanteris motoneurons. As such, elongation of the fCO, signaling flexion of the FT joint, terminated depressor motoneuron activity and initiated activity in levator motoneurons. Relaxation of the fCO, signaling extension of the FT joint, induced the opposite transition by initiating depressor motoneuron activity and terminating levator motoneuron activity. This interjoint influence of sensory signals from the fCO was independent of the generation of the intrajoint reflex reversal in the FT joint, i.e., the "active reaction," which is released by elongation signals from the fCO. The generation of these transitions in activity of trochanteral motoneurons barely depended on position or velocity signals from the fCO. This contrasts with the situation in the resting behavioral state when interjoint reflex action markedly depends on actual fCO stimulus parameters, i.e., position and velocity signals. In the active behavioral state, movement signals from the fCO obviously trigger or release centrally generated transitions in motoneuron activity, e.g., by affecting central rhythm generating networks driving trochanteral motoneuron pools. This conclusion was tested by stimulating the fCO in "fictive rhythmic" preparations, activated by the muscarinic agonist pilocarpine in the otherwise isolated and deafferented mesothoracic ganglion. In this situation, sensory signals from the fCO did in fact reset and entrain rhythmic activity in trochanteral motoneurons. The results indicate for the first time that when the stick insect locomotor system is active, sensory signals from the proprioceptor of one leg joint, i.e., the fCO, pattern motor activity in an adjacent leg joint, i.e., the CT joint, by affecting the central rhythm generating network driving the motoneurons of the adjacent joint.

Action Potentials↗

Reference frames for spinal proprioception: kinematics based or kinetics based?

This second paper of the series deals with another issue regarding sensorimotor representations in the CNS that has received much attention, namely the relative weighting of kinematic and kinetic representations. The question we address here is the contribution of muscle tension afferent information in dorsal spinocerebellar tract (DSCT) sensory representations of foot position. In five anesthetized cats, we activated major hindlimb muscle groups using electrical stimulation of ventral root filaments while passively positioning of the left hind foot throughout its workspace. In general, as the parameters of the joint angle covariance planes indicated, muscle stimulation did not significantly change hindlimb geometry. We analyzed the effects of the muscle stimulation on DSCT neuronal activity within the framework of a kinematic-based representation of foot position. We used a multivariate regression model described in the companion paper, wherein indicators of the experimental condition were added as firing rate predictors along with the limb axis length and orientation to account for possible effects of muscle stimulation. The results indicated that the response gain of 35/59 neurons studied (59%) was not changed by the muscle activations, although most neurons showed some change in their overall firing level with stimulation of one or more muscles. Most of the neurons responded to pseudorandom stimulation of the same muscle groups with complex temporal patterns of activity. For a subpopulation of 42 neurons, we investigated the extent to which their representation of foot position was affected by a rigid constraint of the knee joint and at least one type of muscle stimulation. Although they could be divided into four subgroups based on significance level cutoffs for the constraint or stimulation effect, these effects were in fact quite distributed. However, when we examined the preferred directions of spatial tuning relative to the limb axis position, we found it was unchanged by muscle stimulation for most cells. Even in those cases in which response gain was altered by muscle stimulation, the cell's preferred direction generally was unaltered. The invariance of preferred direction with muscle stimulation lead us to the conclusion that the reference frame for DSCT coding may be based primarily on limb kinematics.

Action Potentials↗

A cortico-spinal model of reaching and proprioception under multiple task constraints.

A model of cortico-spinal trajectory generation for voluntary reaching movements is developed to functionally interpret a broad range of behavioral, physiological, and anatomical data. The model simulates how arm movements achieve their remarkable efficiency and accuracy in response to widely varying positional, speed, and force constraints. A key issue in arm movement control is how the brain copes with such a wide range of movement contexts. The model suggests how the brain may set automatic and volitional gating mechanisms to vary the balance of static and dynamic feedback information to guide the movement command and to compensate for external forces. For example, with increasing movement speed, the system shifts from a feedback position controller to a feedforward trajectory generator with superimposed dynamics compensation. Simulations of the model illustrate how it reproduces the effects of elastic loads on fast movements, endpoint errors in Coriolis fields, and several effects of muscle tendon vibration, including tonic and antagonist vibration reflexes, position and movement illusions, effects of obstructing the tonic vibration reflex, and reaching undershoots caused by antagonist vibration.

Computer Simulation↗

Proprioceptive innervation of the masticatory muscles in Pinché.

This study of the masticatory muscles of the primate showed that the temporal muscle contained 107 muscle spindles, 45 in the horizontal portion and 62 in the vertical portion; the masseter muscle contained 70, 58 in the profundus portion and 12 in the superficial portion; the medial pterygoid muscle contained 15; the lateral pterygoid muscle contained 6; and the zygomaticomandibular muscle contained 9. The muscle spindles were located around the coronoid process and mandibular ramus.

Animals↗

Influence of age on proprioceptive accuracy in two dimensions.

Slow arm movements were made over a smooth horizontal table at shoulder height. With visual cues excluded, target position was indicated by the index finger of the nonmoving arm touching the underside of the table. 134 subjects (including 26 left-handed subjects) in the age range 8.0 to 24.6 yr. were examined to see if the results were age-related. Accuracy slightly but significantly increased with age. The younger subjects showed a greater accuracy with the dominant hand--a situation which tended to be reversed in the older subjects.

Adolescent↗