Facial input to neck motoneurons: trigemino-cervical reflexes in the conscious and anaesthetised cat.

Cutaneous facial inputs influencing head movement were examined in the conscious and anaesthetised cat. EMG recordings were made in neck muscles of conscious, unrestrained cats in which an unexpected light cutaneous stimulus was applied to the glabrous skin of the planum nasale (PN). These observations established that head aversion movements were associated with synchronised activation of both deep and superficial dorsal neck muscles. In anaesthetised cats in which activity in the motoneurons of the large dorsal neck muscles was examined, mechanical stimulation of the PN or electrical stimulation of the infraorbital nerve (ION) produced a short latency, reflex activation. The reflex could be elicited by excitation of low threshold, rapidly conducting fibres in the ION. Intracellular recording from neck motoneurons showed that there is a short latency, probably disynaptic, excitatory pathway from low threshold nerves in the ION to neck motoneurons, but discharge of neck motoneurons occurred several milliseconds later, presumably as a result of activity in a longer multisynaptic pathway.

Cat trigeminal neurons innervated from the planum nasale: their medullary location and their responses to mechanical stimulation.

Experiments were performed to determine whether the receptors of the glabrous skin of the cat planum nasale (PN) could function in tactile analysis. Trigeminal projection sites of the PN were first identified using transganglionic transport of wheat germ agglutinin-horseradish peroxidase and horseradish peroxidase. Restricted projection sites were identified in this way among the interstitial neurons of the trigeminal tract, in the dorsal horn of the medulla, in subnucleus interpolaris and to a lesser extent in subnucleus oralis. Electrophysiological recording in the trigeminal spinal nucleus confirmed the major neuroanatomical findings and confirmed the paucity of PN projections to the trigeminal system. Most neurons innervated from the PN have small receptive fields, are rapidly adapting and responsive to PN vibration at amplitudes as low as 10 micros. Neurons could be entrained at frequencies below 80 Hz. This upper limit for entrainment presumably reflects the lack of pacinian corpuscles in the PN. A limited number of slowly adapting neurons were found, but only responded to PN displacements of 400 microns and above. The data suggest that the PN can function in tactile analysis to a limited degree. The significance of these findings is considered with respect to the organization of neural systems controlling head movement.

Projections of the tectospinal tract to the upper cervical spinal cord of the cat: a study with the anterograde tracer PHA-L.

The goal of the present experiments was to re-examine the spinal projections of neurons in the superior colliculus (SC) of the cat by taking advantage of the high sensitivity of the anterograde tracer, phaseolus vulgaris leucoagglutinin (PHA-L). In seven experiments, multiple injections of PHA-L into different regions of the SC labelled a total of 172 axons in the predorsal bundle; yet only 11 tectospinal tract (TST) axons were found in the upper cervical spinal cord. Collaterals emerging from these axons were rare and arose exclusively from TST axons with a diameter of less than 1 micron. Individual collaterals had different termination zones: some terminated in the lateral part of lamina V and VI after taking a dorsolateral course through lamina VII and VIII; others terminated in the medial part of lamina VII. One collateral terminated within lamina IX and the ventral part of lamina VIII. The combined termination of all collaterals was densest in lamina VII and dorsal lamina VIII. A small number of boutons were also found in the lateral parts of laminae V and VI, and in lamina IX and immediately adjacent regions in lamina VIII. Compared to axons belonging to other spinal descending systems, individual TST axons give rise to much simpler intraspinal collaterals with relatively few boutons. This feature, together with the relative paucity of TST axons, suggests that direct connections from the SC to neurons in the upper cervical spinal cord are sparse. Furthermore, our results are consistent with electrophysiological studies that show that few, if any, neck motoneurons receive monosynaptic connections from TST neurons. Projections to neck motoneurons must therefore involve a relay, either through other descending pathways, such as the reticulospinal system, or via local segmental interneurons.

Representation of forelimb mechanoreceptors within the superior colliculus of the cat.

Forelimb mechanoreceptor representation within the superior colliculus was investigated using microelectrode recording in decerebrate or anaesthetized cats. Selective activation of different mechanoreceptive fibre classes supplying the distal forelimb revealed a poor representation of all three fibre classes (SA, PC and RA) that innervate the glabrous skin. Furthermore, there was no evidence for Pacinian (PC) input from the interosseous or wrist region. The tap stimuli which are often needed to activate the collicular neurones, may be effective, when applied to the distal limb, because of stimulus spread to more proximal sites, or as a result of the synchronous recruitment of multiple classes of afferent fibres.

Somatosensory projections to the superior colliculus of the anaesthetized cat.

1. Experiments in anaesthetized cats have shown that the superior colliculus receives deep afferent input from the forelimb and hindlimb, but not from the large superficial neck muscles. 2. Neuronal activity in the superior colliculus is readily elicited by electrical stimulation of C2 and C3 cutaneous nerves. A significant proportion of neurones so activated have multiple receptive fields and some with no identifiable receptive fields in regions innervated by C2 and C3 nerves have receptive fields elsewhere on the body surface. Many collicular neurones activated by C2 and C3 stimulation had no identifiable receptive fields. 3. Natural stimuli to the limbs, hitherto believed to activate only cutaneous receptors, are sufficient to activate deep receptors which contribute to the neuronal responses in the superior colliculus elicited by the natural stimulus. These same natural stimuli set up transmitted vibration adequate to excite receptors some distance from the applied stimulus. 4. No evidence was found for a rigorous somatotopy in the superior colliculus. The great majority of neurones received trigeminal input which is widely distributed throughout the superior colliculus. 5. Tactile stimuli to the face are most effective in eliciting unit activity in the superior colliculus and many neurones activated by these stimuli were shown to be tectospinal neurones. In particular, the specialized receptors of the face, including the glabrous skin of the snout (the planum nasale) and the vibrissae, are major sources of input to collicular neurones including tectospinal neurones. 6. It is suggested that a major role of the superior colliculus is in the organization of head movements associated with the use of the specialized receptor organs of the face in exploratory behaviours. The superior colliculus may also be involved in the organization of aversion movements of the head.

Organization of segmental input from neck muscles to the external cuneate nucleus of the cat.

The musculotopic organisation of projections to the external cuneate nucleus (ECN) from the neck muscles splenius (SP) and biventer cervicis (BC) was examined electrophysiologically. These muscles are divided into a number of serially arranged compartments and are supplied by nerves from different cervical segments. About one-third of ECN neurons receive input from a single nerve. The majority of ECN neurons, however, receive input from more than one nerve in each muscle. ECN neurons are also limited in their ability to follow high frequency nerve stimulation and they frequently exhibit non-linear following. The connections and characteristics of ECN neurons suggest that a minority of neurons in the nucleus have the potential for the faithful transmission of afferent signals, but the majority have the potential to transform incoming patterns of muscle receptor discharge.

Morphology, distribution, and density of sensory receptors in the glabrous skin of the cat rhinarium.

The sensory organization of the cat rhinarium has been investigated. Individual rete pegs were found to contain a triad of receptors comprising free nerve endings ascending in the peg to terminate in close proximity to the skin surface, a basally situated layer of Merkel corpuscles, and an abundance of encapsulated receptors lying at the base and to one side of the rete peg. Neither the Merkel corpuscles nor the encapsulated receptors were evenly distributed. Merkel corpuscles were more abundant dorsally; ventrally they were fewer and asymmetrically arranged within individual rete pegs. The encapsulated corpuscles were more evenly distributed, but dorsally they were consistently present as encapsulated clusters of up to nine corpuscles.

The pattern of spinal and medullary projections from a cutaneous nerve and a muscle nerve of the forelimb of the cat: a study using the transganglionic transport of HRP.

The transport of HRP into the spinal cord and medulla in the cat has been examined from a forelimb cutaneous nerve, the lateral superficial radial nerve (LSR), and from the muscle nerves supplying both heads of the forelimb muscle, extensor carpi radialis (ECR). HRP transported by the LSR was widely distributed in the spinal cord throughout laminae I-IV in the vicinity of the root entry zone and from spinal segments T1 to C5. HRP was also transported from the LSR to the medulla where there was intense patchy, discontinuous labelling in the main cuneate nucleus. The pattern of labelling in the cuneate nucleus did not follow any simple somatotopic plan. Exposure of the muscle nerve to HRP led to labelling in the spinal dorsal horn in lamina I, in the deep dorsal horn on the lamina V/VI border, and in lateral and medial lamina VI at sites that contain cells of origin of spinocerebellar tracts. The medial lamina VI label was contiguous with a deposit that extended medially to the central canal. The label in lateral lamina VI was patchy and formed a discontinuous column from T1 to C5. HRP transported by the muscle nerve also produced label in the more ventral regions of the cuneate nucleus where it had a lacy appearance, in part due to its extensive distribution around dendrites. A relatively dense, patchy, and discontinuous deposit of reaction product was also present in the external cuneate nucleus after muscle nerve exposure. This deposit was most intense on the dorsomedial surface of this nucleus, but another, less intense, deposit was also present ventrally.

Group III and IV receptors of skeletal muscle.

The single largest group of sensory fibres leaving skeletal muscles are small myelinated or unmyelinated (groups III and IV) fibres. The receptors served by these small fibres have not been subjected to the same intensive study that receptors served by group I and II fibres have received. The evidence so far available suggests that receptors with group III and IV axons play a particular role in nociception and also subserve a wide range of sensory modalities. Despite their role in nociception, the primary afferent fibres from these receptors do not project to the substantia gelatinosa. A significant percentage of group III receptors are sensitive to stretch and have been thought to be the receptor source that initiates the clasp-knife reflex. Other group III receptors respond to chemical change within the muscle and have been implicated in the initiation of cardiovascular reflexes and the changes in muscle blood flow that accompany exercise. Group IV receptors also include high threshold mechanoreceptors and nociceptors. It is well known that encapsulated receptors are quite unevenly distributed within skeletal muscles and in different skeletal muscles. Preliminary evidence suggests that the variation in receptor content is not confined to encapsulated receptors, but that the receptors served by group III and IV afferents may have receptive properties that vary from muscle to muscle.

Patterns of primary afferent termination in the external cuneate nucleus from cervical axial muscles in the cat.

Using the method of transganglionic transport of horseradish peroxidase (HRP), the distribution of primary afferent projections was examined in the external cuneate nucleus (ECN) from different muscle groups in the forequarter of the cat. The terminal zones of afferent fibers from three shoulder muscles--clavotrapezius, acromiotrapezius, and spinotrapezius--were compared to projections from suboccipital muscles, dorsal neck extensors, and muscles of the proximal forelimb. Each muscle group had a labelled terminal zone that occupied a different subvolume of the ECN. The zone labelled from trapezius muscles formed a continuous column in the ECN running from the caudal pole of the nucleus to a level 3.0 mm rostral to the obex. Terminal zones of suboccipital muscles and dorsal neck extensors formed longer columns that extended into the most rostral tip of the ECN, while those of proximal forelimb muscles formed shorter columns confined to the caudal two-thirds of the ECN. At comparable cross-sectional levels in the caudal and middle portions of the ECN, terminal zones from proximal limb muscles were located most dorsomedially, while those from shoulder muscles, dorsal neck muscles, and suboccipital muscles were located in progressively more ventral and lateral regions. The subvolume of the ECN occupied by projections from cervical axial muscles was estimated to be more than 40% of the volume of the nucleus, suggesting that the ECN has a major role in the transmission of sensory information from axial musculature to the cerebellum. Following exposure of all muscle nerves to tracer, a second labelled zone was also identified close to the ECN in the descending vestibular nucleus at transverse levels 2.0-3.0 mm rostral to the obex. Here, reaction product was concentrated around a circumscribed collection of medium-sized, multipolar cells.

Projections from C2 and C3 nerves supplying muscles and skin of the cat neck: a study using transganglionic transport of horseradish peroxidase.

Transganglionic transport of HRP has been used to trace the pathways and termination sites of cutaneous and muscle afferent axons entering from the C2 and C3 dorsal rami. The muscle afferent projection in the spinal cord is restricted and (apart from the ventral horn) largely confined to the intermediate gray matter. There is a muscle afferent projection to the ventrolateral main cuneate nucleus and a complex pattern of projection through the extent of the external cuneate nucleus. In contrast, the cutaneous spinal projection is abundant with extensive filling of axons in the tract of Lissauer and many termination sites in the lateral substantia gelatinosa. Axons enter the lateral gray matter of the cervical spinal cord from the dorsal columns and the dorsolateral funiculus and terminate in the lateral one-third of the dorsal horn as far rostral as the spinomedullary junction. Axons of the tract of Lissauer form a complex web around the dorsal horn and many penetrate rostrally to the region of the spinomedullary junction, where they terminate among clusters of interstitial cells on and close to the dorsal medullary surface. Cutaneous afferent axons from the dorsal columns turn into the main cuneate nucleus and enter a dense mass of HRP-reaction product which occupies the most ventrolateral part of the nucleus for its entire length.

Central projections from cat suboccipital muscles: a study using transganglionic transport of horseradish peroxidase.

Central projections of suboccipital muscle nerves were examined following exposure of cut peripheral nerves to the tracer horseradish peroxidase. Labelled fibers entered the C1 and C2 dorsal roots and accumulated in the dorsolateral part of the dorsal funiculus. Many labelled fibers entered the grey matter of C1 to C3 in ventrally directed bundles which passed medially to the base of the dorsal horn. No terminal labelling was apparent in superficial layers of the dorsal horn. However, labelled fibers ramified extensively throughout medial parts of the intermediate laminae, in and around the central cervical nucleus. Labelled fibers also projected toward the ventral horn. In cats subjected to ventral root section at the time of peripheral nerve exposure, a modest distribution of reaction product was observed deep in the ventral horn. In cats which did not undergo ventral root section, anterograde projections in the ventral horn were obscured by the simultaneous retrograde filling of motoneurons both in the ventromedial nucleus and on the medial and lateral borders of the gray matter. Labelled axons also coursed rostrally into the medulla where they formed a circumscribed bundle between the main cuneate nucleus and the spinal nucleus of V. Three consistent regions of HRP deposition could be identified at medullary levels. Dense accumulations of reaction product were present in circumscribed regions of the external cuneate nucleus (ECN) throughout its rostrocaudal extent. A second zone of dense labelling occurred in the intermediate nucleus of Cajal, where it appeared to form a continuing column rostral to the central cervical nucleus in C1-C3. Sparse labelling was restricted to a third zone in the ventrolateral part of the main cuneate nucleus.

Contralateral, midline, and commissural motoneurons of neck muscles: a retrograde HRP study in the cat.

Retrograde transport of HRP has been used to examine the distribution of motoneurons supplying the dorsal neck muscles biventer cervicis, and complexus in the cat. Retrogradely filled cells were present in the expected sites in lamina IX of the ventral horn, but were not confined to that area. Retrogradely labelled cells were also found more dorsally in the ventral horn and in the white matter medial to the ventral horn. Other filled cells were found in the commissural nuclei and in laminae VII and VIII contralateral to the nerve being dipped. Cells in the ipsilateral lamina IX ranged in size from 15 to 70 microns. Cells lying outside this region were smaller with the majority having mean equivalent diameters, of 40 microns or less.

Organization and sensory properties of small myelinated fibres in the dorsal cervical rami of the cat.

A study using both anatomical dissection and electrophysiological recording has been made to analyse sensory components of the cervical dorsal rami in the cat. Particular attention has been paid to the physiological properties of Group III muscle afferents. The dorsal rami from C2 to C4 are composed of many nerve bundles that contain afferents from both muscle and skin. Bundles containing only cutaneous and only muscle afferents were identified and found to follow a relatively consistent pattern of organization within the ramus. In nerve bundles serving the biventer cervicis muscle, a population of Group III afferent fibres was identified that responded to strong localized pressure or localized stretch. Their receptive fields were generally small and situated on the muscle borders or in tendinous inscriptions. Such units comprised 73% of those with conduction velocities less than 20 m/s. Group III afferent fibres from neck muscles fired readily to intramuscular 6% sodium chloride, but were mostly not sensitive to bradykinin injected locally or intra-arterially.

Comment: unresolved questions concerning muscle afferents.

Some current questions regarding muscle afferent receptors are discussed. These include the significance of variable distribution patterns of muscle spindles in different muscles and of differences in intrinsic spindle morphology. The significance of the very large and variable population of small myelinated afferent fibres in muscle is also discussed.

The nature of afferents from the large dorsal neck muscles that project to the superior colliculus in the cat.

1. A 3.5-5 mm passive stretch of dorsal neck muscles at velocities of 50 mm/sec, a stimulus adequate to excite most neck muscle spindles, was usually ineffective in eliciting unit discharge in the superior colliculus. The sudden release of muscle tension was effective and excited fifty-seven of sixty-seven units tested. 2. When electrical stimulation of neck muscle nerves was used, a stimulus strength sufficient to excite Group III muscle afferents was usually required to elicit unit discharge in the superior colliculus. 3. It is concluded that the projection from neck muscles to the superior colliculus largely takes origin in Group III afferent whose function remains to be determined. Some contribution to the projection to the superior colliculus from proprioceptive afferents served by larger fibres cannot be ruled out.

Neck muscle and trigeminal input to the upper cervical cord and lower medulla of the cat.

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.

Unit activity in the superior colliculus of the cat following passive eye movements.

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.

Physiological properties of muscle spindles in dorsal neck muscles of the cat.

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.