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P D Gamlin

Publications and source records attributed to P D Gamlin.

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Interconnections between the primate cerebellum and midbrain near-response regions.

The goal of this study was to determine the pattern of the connections between the midbrain and cerebellum that may play a role in the modulation of the near-response in the macaque. Injection of the retrograde tracer wheat germ agglutinin conjugated horseradish peroxidase (WGA-HRP) into the physiologically identified midbrain near-response region, which includes the supraoculomotor area, labelled cells throughout the deep cerebellar nuclei. However, labelled cells were particularly concentrated in the ventrolateral corner of the contralateral posterior interposed nucleus and in the contralateral and, to a lesser extent, the ipsilateral fastigial nuclei. Subsequently, injections of WGA-HRP were used to define the midbrain terminations of the deep cerebellar nuclei. Fastigial nucleus injections labelled terminals in a band along the border between the oculomotor nucleus and the supraoculomotor area that included the Edinger-Westphal nucleus. Injections of the posterior interposed nucleus labelled terminals in the portion of the supraoculomotor area dorsal to the fastigial projection and did not involve the Edinger-Westphal nucleus. In both cases, the terminal label was primarily found contralaterally. In contrast, retrogradely labelled cells were primarily found ipsilaterally within the supraoculomotor area following cerebellar injections. Retrogradely labelled cells projecting to the deep nuclei were also found bilaterally in the anteromedian nucleus, along with sparse terminal label. Taken as a whole, these results demonstrate the presence of a highly specific pattern of labelling in the supraoculomotor area, which may indicate that the posterior interposed nucleus and the fastigial nucleus play different roles in the control of the near-response. Alternatively, these projections may subserve other functions, such as modulating the pupillary light reflex. The fact that the projection from the deep nuclei is primarily contralateral, while the supraoculomotor projection to the deep nuclei is primarily ipsilateral, suggests that this may not be a simple feedback system, but may instead be involved in balancing the gains in the two eyes. In sum, physiological experiments have indicated the presence of near-response neurons in the midbrain supraoculomotor area and have indicated that the cerebellum may play a role in modulating the components of the near-response, as well as activity in the intrinsic eye muscles. The present experiments suggest a pattern of connections that might subserve this cerebellar modulation.

Animals

Dynamic properties of medial rectus motoneurons during vergence eye movements.

1. An early study by Keller reported that medial rectus motoneurons display a step change in firing rate during accommodative vergence movements. However, a later study by Mays and Porter reported gradual changes in firing rate during symmetrical vergence movements. Furthermore, subsequent inspection of the activity of individual medial rectus motoneurons during vergence movements indicated transient changes in their firing rate that had not been noted by Mays and Porter. For conjugate eye movements, in addition to a position signal, motoneurons display an eye velocity signal that compensates for the characteristics of the oculomotor plant. This suggested that the transient change in firing rate seen during vergence movements represented a velocity signal. Therefore the present study used single-unit recording techniques in alert rhesus monkeys to examine the dynamic behavior of medial rectus motoneurons during vergence eye movements. 2. The relationship between firing rate and eye velocity was first studied for vergence responses to step changes in binocular disparity and accommodative demand. Inspection of single trials showed that medial rectus motoneurons display transient changes in firing rate during vergence eye movements. To better visualize the dynamic signal during vergence movements, an expected firing rate (eye position multiplied by position sensitivity of the cell plus its baseline firing rate) was subtracted from the actual firing rate to yield a difference firing rate, which was displayed along with the eye velocity trace for individual trials. During all smooth symmetrical vergence movements, the profile of the difference firing rate very closely resembled the velocity profile. 3. To quantify the relationship between eye velocity and firing rate, two approaches were taken. In one, peak eye velocity was plotted against the difference firing rate. This plot yielded a measure of the velocity sensitivity of the cell (prv). In the other, a scatter plot was produced in which horizontal eye velocity throughout the vergence eye movement was plotted against the difference firing rate. This plot yielded a second measure of the velocity sensitivity of the cell (rv). 4. The behavior of 10 cells was studied during both sinusoidal vergence tracking and conjugate smooth pursuit over a range of frequencies from 0.125 to 1.0 Hz. This enabled the frequency sensitivity of the medial rectus motoneurons to be assessed for both types of movements. Both vergence velocity sensitivity and smooth pursuit velocity sensitivity decreased with increasing frequency. This is similar to a finding by Fuchs and co-workers for lateral rectus motoneurons during smooth pursuit eye movements.(ABSTRACT TRUNCATED AT 400 WORDS)

Animals

Characteristics of near response cells projecting to the oculomotor nucleus.

1. Previous work has shown neurons just dorsal and lateral to the oculomotor nucleus that increase their firing rate with increases in the angle of ocular convergence. It has been suggested that the output of these midbrain near response cells might provide the vergence command needed by the medial rectus motoneurons. However, lens accommodation ordinarily accompanies convergence, and a subsequent study showed that only about one-half of these midbrain near response cells carried a signal related exclusively to vergence. One hypothesis suggested by this finding is that this subgroup of neurons might have a unique role in providing a "pure" vergence signal to the medial rectus motoneurons. 2. In the present study extracellular recordings were made from midbrain near response cells in monkeys while eye position and lens accommodation were measured. The monkeys viewed targets through an optical system that allowed the accommodative and ocular vergence demands to be manipulated independently. This approach was used to produce a partial dissociation of accommodative and vergence responses, so that an accommodative and vergence coefficient could be determined for each cell, by the use of the following equation FR = R0 + kda x AR + kdv x CR where FR is the firing rate of the near response cell, R0 is the predicted firing rate for a distant target, kda is the (dissociated) accommodation coefficient, AR is the accommodative response, kdv is the (dissociated) vergence coefficient, and CR is the convergence response. 3. The vergence and accommodation coefficients were determined for a large number of midbrain near response cells, including a subset that could be antidromically activated from the medial rectus subdivisions of the oculomotor nucleus. Some near response neurons were found with signals related exclusively to convergence (i.e., kdv greater than 0 and kda = 0), whereas several others had signals related exclusively to lens accommodation (i.e., kda greater than 0 and kdv = 0). The majority of the near response cells had signals related to both responses (i.e., kda not equal to 0 and kdv not equal to 0). Furthermore, the vergence and accommodation coefficients of near response cells appeared to be continuously distributed. Some cells had negative accommodation or vergence coefficients. 4. The 17 near response cells that could be antidromically activated from the oculomotor nucleus presumably provide vergence signals to the medial rectus motoneurons. Although all had positive vergence coefficients, only four of these cells carried signals that were related exclusively to vergence.(ABSTRACT TRUNCATED AT 400 WORDS)

Accommodation, Ocular

The Edinger-Westphal nucleus: sources of input influencing accommodation, pupilloconstriction, and choroidal blood flow.

This study used neuroanatomical techniques to investigate sources of afferents to the Edinger-Westphal nucleus (EW) of the pigeon. The EW contains the parasympathetic preganglionic neurons that, by way of the oculomotor nerve, project to the ciliary ganglion (Narayanan and Narayanan, '76; Lyman and Mugnaini, '80). The ciliary ganglion, in turn, innervates the internal musculature of the eye; the ciliary body, the iris sphincter muscle, and the smooth muscle of choroidal blood vessels (Marwitt et al., '71; Pilar and Tuttle, '82). In the bird, the neurons in the ciliary ganglion that innervate the iris sphincter muscle and the ciliary body receive input specifically from cells in the lateral EW (EWl), whereas those that innervate choroidal blood vessels receive input from cells in the medial EW (EWm) (Reiner et al., '83). Thus neurons in the EWl mediate pupilloconstriction and accommodation, whereas neurons in the EWm modulate choroidal blood flow. To study the afferents to EW, injections of horseradish peroxidase (HRP) were placed in this nucleus. These injections resulted in labeled cells in the area pretectalis, a retinorecipient pretectal nucleus and the suprachiasmatic nucleus, a retinorecipient hypothalamic nucleus. We have previously identified both these areas as being sources of afferents to EW (Gamlin et al., '82, '84). In addition, these HRP injections into EW resulted in labeled cells in the medial mesencephalic reticular formation (MRF) lateral and ventral to the oculomotor nucleus and in a localized area of the rostral lateral mesencephalic reticular formation (LRF) dorsolateral to nucleus subpretectalis. Injections of tritiated amino acids into the MRF labeled the entire EW, while such injections into the LRF labeled only the lateral EW. Both of these projections were predominantly contralateral. This study has identified the sources of two previously undocumented inputs to the avian EW. Both sources of input, the MRF and rostral LRF, receive afferents from visuomotor areas of the telencephalon and visual structures in the midbrain. The MRF input to EW could have either direct or modulatory influences on pupil diameter, accommodation, and choroidal blood flow. The LRF input to EW could play a role in controlling accommodation and possibly the pupillary near response.

Afferent Pathways

Antidromic identification of midbrain near response cells projecting to the oculomotor nucleus.

Medial rectus motoneurons carry both conjugate and vergence eye position signals. Abducens internuclear neurons, whose axons travel in the medial longitudinal fasciculus, provide these motoneurons with the major signal for conjugate eye movements but not for vergence eye movements. A vergence signal appropriate for these motoneurons is seen on the near response cells that are found in the mesencephalic reticular formation within 2 mm of the oculomotor nucleus. The goal of the present study was to determine if midbrain near response cells project to the medial rectus subdivision of the oculomotor nucleus. Near response cells were recorded in two trained rhesus monkeys with ocular search coils. A stimulating electrode was positioned within the medial rectus subdivision of the oculomotor nucleus. Twenty-eight near response cells were found that could be driven by single pulse microstimulation of the ipsilateral medial rectus subdivision. In all cases, antidromic activation was confirmed by collision testing. Attempts to antidromically activate midbrain near response cells from the contralateral medial rectus subdivision were unsuccessful. Most antidromically activated cells had a steady state firing rate proportional to vergence angle. One cell also showed burst activity during the vergence eye movements. Divergence cells were not antidromically activated.

Animals

Trochlear unit activity during ocular convergence.

1. Ocular convergence is usually accompanied by excyclotorsion of the eyes. Furthermore, the magnitude of cyclotorsion is dependent on the elevation of the eyes. The reason for this excyclotorsion during convergence is not understood. 2. Excyclotorsion could be produced by either increased activity in the inferior oblique muscle or decreased activity in the superior oblique muscle. An earlier study indicated that convergence may also be accompanied by a temporal (lateral) translation of the eye. This observation is more consistent with a relaxation of the superior oblique than contraction of the inferior oblique. 3. This hypothesis was tested by recording the activity of 31 neurons in the trochlear nucleus, which contains the superior oblique motoneurons. This was done in alert monkeys that were trained to make both versional and vergence eye movements. In addition, the cyclotorsion associated with convergence was measured in one of these monkeys. 4. A consistent excyclotorsion associated with convergence was observed. Trochlear unit activity decreased during convergence in all cells tested. The magnitude of this decrease was significantly greater than that seen with conjugate adduction. Furthermore, the size of the decrease varied systematically with ocular elevation in a manner that was consistent with earlier measures of cyclotorsion during convergence. 5. These results suggest that the excyclotorsion seen during convergence, and perhaps the lateral translation of the eye, are due to a relaxation of the superior oblique muscle. This relaxation during convergence is greater than that which accompanies similar conjugate movements of the eyes. We hypothesize that this peculiar pattern of muscle innervation has a motor rather than sensory function.(ABSTRACT TRUNCATED AT 250 WORDS)

Animals

Abducens internuclear neurons carry an inappropriate signal for ocular convergence.

1. Single-unit recording studies in alert Rhesus monkeys characterized the vergence signal carried by abducens internuclear neurons. These cells were identified by antidromic activation and the collision of spontaneous with antidromic action potentials. The behavior of abducens internuclear neurons during vergence was compared with that of horizontal burst-tonic fibers in the medial longitudinal fasciculus (MLF) and to that of a large sample of unidentified abducens cells (presumably both motoneurons and internuclear neurons). 2. The results indicate that abducens internuclear neurons and lateral rectus motoneurons behave similarly during vergence eye movements: the majority of both groups of cells decrease their firing rate for convergence eye movements: a minority show no change for vergence. This finding is strongly supported by recordings of horizontal burst-tonic fibers in the MLF, the majority of which decrease their activity significantly for convergence eye movements. 3. These findings indicate that a net inappropriate vergence signal is sent to medial rectus motoneurons via the abducens internuclear pathway. Because medial rectus motoneurons increase their activity appropriately during symmetrical convergence, this inappropriate MLF signal must be overcome by a more potent direct vergence input. 4. Overall, both abducens internuclear neurons and lateral rectus motoneurons decrease their activity for convergence less than would be expected based on their conjugate gain. This implies that some degree of co-contraction of the lateral and medial rectus muscles occurs during convergence eye movements. 5. Some horizontal burst-tonic MLF fibers decrease their activity more for convergence than any recorded abducens neuron. These fibers may arise from cells in the nucleus prepositus hypoglossi or vestibular nuclei.

Abducens Nerve

Lidocaine-induced unilateral internuclear ophthalmoplegia: effects on convergence and conjugate eye movements.

1. To characterize the vergence signal carried by the medial longitudinal fasciculus (MLF), it was subjected to reversible blockade by small injections of 10% lidocaine hydrochloride. The effects of these blockades on both conjugate and vergence eye movements were studied. 2. With this procedure, experimentally induced internuclear ophthalmoplegia (INO) and its effects on conjugate eye movements could be studied acutely, without possible contamination from long-term oculomotor adaptation. In the eye contralateral to the MLF blockade, saccadic and horizontal smooth-pursuit eye movements were normal. Horizontal abducting nystagmus, often seen in patients with INO, was not observed in this eye. 3. As previously reported for INO, profound oculomotor deficits were seen in the eye ipsilateral to the MLF blockade. During maximal blockade, adducting saccades and horizontal smooth-pursuit movements in this eye did not cross the midline. Adducting saccades were reduced in amplitude and peak velocity and showed significantly increased durations. Abducting saccades, which were slightly hypometric, displayed a marked postsaccadic centripetal drift. 4. The eye ipsilateral to the blockade displayed a pronounced, upward, slow drift, whereas the eye contralateral to the blockade showed virtually no drift. Furthermore, although vertical saccades to visual targets remained essentially conjugate, the size of the resetting quick phases in each eye was related to the amplitude of the slow phase movement in that eye. Thus the eye on the affected side displayed large quick phases, whereas the eye on the unaffected side showed only slight movements. On occasion, unilateral downbeating nystagmus was seen. This strongly suggests that the vertical saccade generators for the two eyes can act independently. 5. The effect of MLF blockade on the vergence gain of the eye on the affected side was investigated. As a measure of open-loop vergence gain, the relationship of accommodative convergence to accommodation (AC/A) was measured before, during, and after reversible lidocaine block of the MLF. After taking conjugate deficits into account, the net vergence signal to the eye ipsilateral to the injection was found to increase significantly during the reversible blockade. 6. The most parsimonious explanation for this increased vergence signal is suggested by the accompanying single-unit study. This study showed that abducens internuclear neurons, whose axons course in the MLF, provide medial rectus motoneurons with an appropriate horizontal conjugate eye position signal but an inappropriate vergence signal. Ordinarily, this incorrect vergence signal is overcome by another, more potent, v

Animals

Retinal projections to the pretectum in the pigeon (Columba livia).

The retinal projection to the pretectum in the pigeon has previously been described in detail only by means of anterograde degeneration techniques (Repérant, '73). The present study reinvestigated these retinal projections by using the more sensitive anterograde autoradiographic technique. In general, our results confirm and extend those of Repérant ('73). We have found that three pretectal nuclei--the nucleus lentiformis mesencephali, tectal gray, and the area pretectalis--received heavy retinal input. A fourth pretectal nucleus, pretectalis diffusus, receives a slight retinal input. The nucleus lentiformis mesencephali can be divided into two closely apposed subnuclei that are cytoarchitecturally similar. We have termed them "lentiformis mesencephali, pars medialis" and "lentiformis mesencephali, pars lateralis." The tectal gray can be divided into a rostral, retinorecipient region and a narrow, caudal, nonretinorecipient region. The cytoarchitecture and retinal terminal field in area pretectalis have been described previously by us (Gamlin et al., '84). Pretectalis diffusus is located caudal to the retinorecipient dorsal thalamus and rostral to area pretectalis. Localized retinal injections of 3H proline delineated the number and extent of the retinal representations in the pretectum. Separate retinal representations were present in lentiformis mesencephali, pars medialis, lentiformis mesencephali, pars lateralis, the tectal gray, area pretectalis, and pretectalis diffusus. Only in the lentiformis mesencephali, pars medialis, lentiformis mesencephali, pars lateralis, and the tectal gray could the retinal representations be analyzed. Whereas the retinal representations in the lentiformis mesencephali, pars medialis and the tectal gray are comparable, the retinal representation in the lentiformis mesencephali, pars lateralis is different, being a mirror-image mediolaterally. In this study we introduce a conservative nomenclature for the retino-recipient pretectal nuclei that is consistent with earlier studies, in particular, those of Kuhlenbeck ('39), but has been modified in the light of our findings. We believe that this nomenclature, combined with the detailed cytoarchitectural descriptions provided, should facilitate future studies of the avian pretectum.

Animals

Projections of the retinorecipient pretectal nuclei in the pigeon (Columba livia).

We have used anterograde autoradiographic and retrograde HRP techniques to investigate the efferent connections of the retinorecipient pretectal nuclei in the pigeon. In the accompanying paper we identified these nuclei in the pigeon as the nucleus lentiformis mesencephali--pars lateralis and pars medialis, the tectal gray, the area pretectalis, and pretectalis diffusus. Although there are reports of a few of the projections of these nuclei, they had not previously been the subject of a detailed study. We found that different cell types in the lentiformis mesencephali, pars medialis and the lentiformis mesencephali, pars lateralis have descending projections to different targets. These targets include the inferior olive, the cerebellum, the lateral pontine nucleus, the nucleus papillioformis, the nucleus of the basal optic root, the nucleus mesencephalicus profundus, pars ventralis, the nucleus principalis precommissuralis, and the stratum cellulare externum. We found that a few cells in the lentiformis mesencephali project to the medial pontine nucleus, but that a much heavier projection arises from the nucleus laminaris precommissuralis, which is medial to the nucleus lentiformis mesencephali, pars medialis. The tectal gray has predominantly ascending projections to the diencephalon. The nuclei that it projects to are the nucleus intercalatus thalami, the nucleus of the ventral supraoptic decussation, the nucleus posteroventralis, the ventral lateral geniculate nucleus, the nucleus dorsolateralis medialis, and the nucleus dorsolateralis anterior. The tectal gray also projects topographically to layers 4 and 8-13 of the optic tectum. Area pretectalis has both ascending and descending projections. It has ipsilateral ascending projections to the nucleus dorsolateralis anterior, pars magnocellularis, the nucleus lateralis anterior, and the nucleus ventrolateralis thalami. It has ipsilateral descending projections to the central gray, the nucleus of the basal optic root, pars dorsalis, the lateral pontine nucleus, and the deep layers of the optic tectum. It has contralateral projections to the area pretectalis, the nucleus Campi Foreli, the interstitial nucleus of Cajal, the nucleus of Darkschewitsch, the cerebellum, and the Edinger-Westphal nucleus. The efferent projections of pretectalis diffusus are limited. It projects contralaterally to the pretectalis diffusus, and ipsilaterally to the nucleus of the ventral supraoptic decussation, the lateral pons, and the cerebellum.4

Animals

A second ascending visual pathway from the optic tectum to the telencephalon in the pigeon (Columba livia).

Previous studies in the pigeon (Karten and Revzin: Brain Res. 2:368-377, '66; Karten and Hodos: J. Comp. Neurol. 140:35-52, '70) have described an ascending tectofugal visual pathway from the optic tectum to the ectostriatum by way of the nucleus rotundus of the thalamus. This present study used anterograde autoradiographic and retrograde horseradish peroxidase pathway-tracing techniques to investigate another ascending tectofugal pathway in the pigeon. Injections of 3H-proline/leucine confirmed a previous report that the optic tectum projects to the nucleus dorsolateralis posterior of the thalamus (DLP). This projection is predominantly ipsilateral and is confined to a large-celled caudal region of the nucleus (DLPc); the rostral region of the nucleus (DLPr) is not tectorecipient. Injections of horseradish peroxidase in DLPc labeled cells predominantly ipsilaterally in layers 8-15 of the optic tectum. Injections of 3H-proline/leucine placed in the DLPc labeled a discrete region of the ipsilateral telencephalon. Similar injections of DLPr labeled a contiguous, but more rostral, region of the neostriatum intermedium. Nissl- and silver-stained material indicated that the region in which DLP terminates is cytoarchitecturally distinct from ventromedial ectostriatal core and belt. Injections of horseradish peroxidase at various locations in the neostriatal DLP terminal field demonstrated a rostrocaudal ordering of the DLP projection upon the neostriatum intermedium. Single-unit recording demonstrated that cells in DLPc respond to whole-field illumination at the same latency as cells in the nucleus rotundus, indicating that the tecto-DLPc-neostriatal pathway transmits visual information to the telencephalon. We suggest that comparable pathways may exist in both reptiles and mammals.

Animals

Neural control of vergence eye movements: neurons encoding vergence velocity.

Single-unit recordings were made from midbrain areas in monkeys trained to make both conjugate and disjunctive (vergence) eye movements. Previous work had identified cells with a firing rate proportional to the vergence angle, without regard to the direction of conjugate gaze. The present study describes the activity of neurons that burst for disjunctive eye movements. Convergence burst cells display a discrete burst of activity just before and during convergence eye movements. For most of these cells, the profile of the burst is correlated with instantaneous vergence velocity and the number of spikes in the burst is correlated with the size of the vergence movement. Some of these cells also have a tonic firing rate that is positively correlated with vergence angle (convergence burst-tonic cells). Divergence burst cells have similar properties, except that they fire for divergent and not convergent movements. Divergence burst cells are encountered far less often than convergence burst cells. Both convergence and divergence burst cells were found in an area of the mesencephalic reticular formation just dorsal and lateral to the oculomotor nucleus. Convergence burst cells were also recorded in another more dorsal mesencephalic region, rostral to the superior colliculus. Both of the areas also contain cells that encode vergence angle. Models of the vergence system derived from psychophysical data imply the existence of a vergence integrator, the output of which is vergence angle. Some models also suggest the presence of a parallel element that improves the frequency response of the vergence system, but has no effect on the steady-state behavior of the system. Vergence burst cells would be suitable inputs to a vergence integrator. By providing a vergence velocity signal to motoneurons, they may improve the dynamic response of the vergence system. The behavior of vergence burst cells during vergence movements is similar to that of the medium-lead burst cells during saccades. The proposed roles for vergence velocity cells are analogous to those of the saccadic burst cells. In this respect, the neural organization of the vergence system resembles that of the saccadic system, despite the distinct difference in the kinematics of these two types of eye movements.

Action Potentials