Propioceptive influences from eye muscle receptors on cells of the superior colliculus.
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Biomedical subjects
Publications and source records attributed to V C Abrahams.
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Unit response in the superior colliculus and underlying structures has been examined in the choralose-anaesthetized cat following passive movement of an occluded eye. One group of units was sensitive to small saccadic movements, responded regardless of the initial postion of the eye, and in most instances responded to movements in opposit directions. A second numerically smaller group also responded when they eye was moved at saccadic velocity but only when the eye passed a fixed point. Such units with fixed positional thresholds were found following movements in both nasal and temporal directions as well as to both upward and downward movement. Both types of unit response were found after transection of the optic nerve and were also recorded when individual extraocular muscles were subjected to controlled stretch. It is assumed that most unit activity seen after passive movement of the occluded eye is due to activity in extraocular muscle receptors. In the deep layers of the superior colliculus responses to small eye movements were found to be due to the activation of very low threshold receptors sensitive to vibration in the facial area.
Experiments on chloralose-anaesthetized cats have shown that low-threshold neck muscle afferents project to laminae IV and V in the dorsal horn of the upper cervical cord, to lamina VI including the region which encompasses the central cervical nucleus, as well as to extensive regions of the ventral horn. At posterior medullary levels projections also exist to laminae IV, V, and VI of the spinal nucleus of V (although those to lamina IV are circumscribed), to the deep layers and lateral margin of the cuneate nucleus, and to the inferior olive. These projections are both from low- and high-threshold afferents. Evidence of a functional relationship between the trigeminal and neck muscle afferent system was found both in the upper cervical cord and lower medulla. About 40% of units in both regions receive a convergent input and when convergence could not be demonstrated, prior stimulation of one modality in some instances affected the responsiveness of the unit to the other modality. A motor role was found for some trigeminal afferent projections to the upper cervical cord. Trigeminal afferents consistently activated antidromically identified motoneurons of splenius, biventer cervicis, and complexus.
1. Single-fiber recording was used to examine the properties of 107 spindle endings in cat biventer cervicis (BC) and complexus (CM) muscles. Responses of receptors were examined following muscle contraction and ramp and hold stretch. Twenty-two endings in splenius (SP) were also examined, but their responses could not be quantitated because the anatomy of SP prevented the application of appropriate stretches. 2. Conduction velocitites of spindle afferents ranged from 13 to 90 m/s. Endings with primary response patterns usually had faster conduction velocities than secondary endings, but there was overlap in the conduction velocity ranges of the two subgroups. 3. Most neck spindle afferents could be classified as either primary or secondary by a constellation of physiological criteria including dynamic response pattern, dynamic index, and variability of resting discharge frequency. However, 22 of 107 endings from BC and CM had responses with characteristics intermediate between primary and secondary responses. The possible sources of these characteristics are discussed. 4. Despite the similarity in properties between spindles of different neck muscles, the length sensitivities of CM spindles were high compared to those of BC spindles. CM spindles showed length-related modulation of firing frequency over a more restricted range of initial muscle lengths than did BC spindles. 5. Eight Golgi tendon organs (GTO) were identified by their characteristics responses. Conduction velocities obtained for five GTO afferent nerves ranged from 50 to 67 m/s. Recordings were also made from receptros in deep muscles surrounding the vertebrae. These receptors had properties characteristic of muscle spindles.
The distribution of motoneurones to the cat dorsal neck muscles biventer cervicis, splenius and complexus has been examined using the technique of retrograde horseradish peroxidase transport. A comparison was initially made of HRP uptake into motoneurones produced either by injecting HRP solution directly into a single neck muscle or by exposing the cut ends of motor nerves to an HRP solution. The injection of HRP into single neck muscles was found to produce widespread labelling of motoneurones presumably due to diffusion of HRP into adjacent muscles. For the examination of individual motoneurone pools the technique of cut nerve exposure was therefore used. Labelled neck muscle motoneurones ranged from 10-70 mu in diameter, but the majority of cells had diameters which were less than 40 mu. Most cells were located in the ventromedial nucleus and along the medial border of the ventral horn. In these regions there was considerable overlap between the motoneurone pools of the three neck muscles examined. In addition, some splenius motoneurones were located in the nucleus of the spinal accessory nerve. Labelled neck muscle motoneurones were also located in areas not usually considered to contain motoneurones such as the commissural and centrodorsal nuclei and in the ventral commissure.
Experiments on chloralose-anaesthetized cats have shown that cells in the superior colliculus may be antidromically activated either from the pontomedullary reticular formation or the ventral cervical spinal cord, or from both sites. In tests on 111 units this has provided a basis for differentiating between cells of origin of the tectospinal tract and the tectoreticular system within the superior colliculus. Tectospinal cells may be activated both by spinal and pontine stimulation; tectoreticular cells cannot be activated by spinal stimulation. Both tectoreticular and tectospinal cells respond to visual and muscle afferent stimulation. The afferent connections may be strongly inhibitory as afferent input to the superior colliculus ofter prevented subsequent antidromic invasion. This was more commonly seen in tectospinal cells than tectoreticular cells. The distribution of the two cell populations within the superior colliculus was also found to be dissimilar. Evidence has also been obtained to suggest that the tectoreticular system, in part, consists of collaterals of the tectospinal tract.
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The numbers and sizes of nerve fibres to the dorsal neck muscles, splenius, complexus and biventer cervicis have been examined in the cat. The total number of fibres is unusually high as is the content of sensory fibres (estimated as the loss of fibres after ganglionectomy). The fibre spectra of these sensory nerves has an unusually large number of fibres in the group II and III range (3-7 mum) and differs markedly in this way from other muscle nerves. The motor fibres contain a high proportion (64-99%) in the gamma fibre size range. Large motor fibres are absent in the nerves to biventer cervicis (a slow muscle). The ratio of unmyelinated to myelinated fibres in neck muscle nerves is similar to that in hind legs at about 2.5:1.
The effects of passive eye rotation on unit discharge in the superior colliculus has been examined in the chloralose anaesthetized cat. Providing that velocity exceeded 50 degrees/sec, passive eye movement led to brief-burst discharges in the superior colliculus. This discharge occurred as the eye traversed a fixed point. The displacement of this point from the primary position has been defined as the displacement threshold for that unit. Displacement thresholds range from 3 to 30 degrees and are consistent over a wide range of velocities but become larger at the velocity threshold for the unit. Conduction times to the superior colliculus ranged from 7 to 108 msec.
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1. Projections to the superior colliculus from fore and hind limb muscle nerves have been examined. 2. Hind leg nerve stimulation at strengths sufficient to excite Group II and III fibres elicited unit discharge in all layers of the superior colliculus and underlying tegmentum. 3. Forelimb nerve stimulation excited units in all layers of the superior colliculus and underlying tegmentum. Twenty per cent were activated by stimulation below Group II threshold, the remainder by stimulation above Group II threshold. 4. Most units activated by limb afferent nerve stimulation were also activated by visual stimuli. There was considerable convergence from both flexor and extensor nerves and most units were excited by stimulation of nerves in more than one limb. 5. Units fired either with a short or long latency or with a paired discharge. Short latency units were most common in deep collicular layers and the tegmentum, long latency units were most common in superficial layers. 6. The spinal pathway of the afferents is mainly in the dorsolateral quadrant contralateral to the recording site. The anatomical characteristics of the pathway are similar to the lateral funiculus climbing fibrespinocerebellar pathway.
Unit recordings were made in the superior colliculus of cats anesthetized with chloralose and with Pentothal. Electrical stimulation of extraocular muscle afferents and neck muscle afferents excited more units in the superior colliculus than did a variety of moving and stationary visual stimuli. Units responding to neck muscle afferent stimulation fell into three populations; one population firing with a short latency and following stimulus presentation up to 1/s, a second population with a long latency and following stimulus presentation at frequencies lower than 15/min, and a third population exhibiting paired firing. The latencies and firing patterns of the third population combined the characteristics of each of the first two patterns. It is suggested that these characteristics of unit discharges stem from the existence of two pathways from neck muscle afferents to the superior colliculus. The projection is predominantly bilateral. Units responding to neck muscle afferent stimulation are distributed throughout the superior colliculus on the basis of their latencies. Long-latency responses predominate in the superficial layers of the superior colliculus and short-latency responses, while more common in the intermediate and deep layers, predominate in the tegmentum. Extraocular muscle afferent projections to the superior colliculus constitute the single richest projection found in these experiments. While the response patterns and latencies are similar to those of the neck muscle afferents, long-latency responses are the most common and dominate in all collicular regions. Few units in the tegmentum could be excited by extraocular muscle afferents. Both extraocular muscle and neck muscle afferents show considerable convergence with one another and with retinal afferents within the superior colliculus. Cells of origin of the tectospinal tract were identified within the superior colliculus and tegmentum by antidromic excitation from the upper cervical cord. These cells were distributed predominantly within the intermediate and deep layers of the superior colliculus, and sparsely in the superficial layers and tegmentum. Almost 50% of the cells of origin of the tectospinal tract receive a convergent input from extraocular muscle and neck muscle afferents and from the retina. About 30% of the cells were inexcitable to the stimuli employed in these experiments. The significance of these projections is discussed with respect to superior collicular function in the cat and i
An examination has been made of the five dorsal muscles of the cat neck which insert into the lamboidal crest. The three larger muscles, splenius, biventer cervicis, and complexus, are characterized by the presence of tendinous inscriptions which serve as the insertion points of shorter muscle fibers which do not run the length of the muscle. Longer fibers are bound by the inscriptions and, thus can transmit tension developed by shorter fibers. These three muscles are multiply innervater by nerves emerging from upper cervical spinal roots. Multiple innervation is not associated with multiple end plates but with arrangement so that lower roots innervate a high proportion of short fibers and higher roots, a high proportion of long fibers. Occipitoscapularis and rectus capitis major are, by comparison, simple muscles, each with a single motor nerve. Of the muscles examined, occipitoscapularis alone does not have its origin on the vertebral column but on the scapula, and is unlikely to have any major function in head movement.
Silver-stained sections have been examined from the five dorsal neck muscles splenius, biventer, cervicis, complexus, rectus capitis major, and occipitoscapularis. Every serial section was examined for at least one muscle of each type so that a complete description of the spindle distribution and morphology could be made. With the exception of occipitoscapularis (whose prime function is probably in scapula rotation and not in head movement), neck muscles have a remarkably high spindle density. Occipitoscapularis has a spindle density similar to that of hindleg locomotor muscles (13-19 per gram), but splenius has a density of 46-66 per gram, biventer cervicis 74-96 per gram, complexus 71-107 per gram, and rectus capitis major 48-84 per gram. Such high densities have only previously been seen in small muscles whose total spindle population is not large. Because of the relatively large size of some neck muscles, individual muscles with a spindle content of up to 254 spindles have been found.
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