Neuronal organization underlying visually elicited prey orienting in the frog--III. Evidence for the existence of an uncrossed descending tectofugal pathway

A complete transverse hemisection of the neuraxis just caudal to the optic tectum in the frog, Rana pipiens, results in a failure to orient toward stimuli in one visual hemifield [Kostyk and Grobstein (1986) Neuroscience 21, 41-55]. This finding indicates that each tectal lobe gives rise to a crossed descending pathway adequate to cause turns in a direction contralateral to that tectal lobe, and suggests that each may also give rise to an uncrossed descending pathway adequate to cause turns in the ipsilateral direction. To determine whether there is in fact such an uncrossed pathway, we have studied the orienting behavior of frogs after lesions which interrupt crossed pathways. Two groups of animals were studied. In one group we made midline lesions of the ansulate commissure, through which run the major crossed descending projections from both tectal lobes. In the other group, we combined a complete transverse hemisection with removal of the tectal lobe on the same side of the brain, leaving intact only an uncrossed pathway from one tectal lobe. A persistence of orienting turns was observed in both groups of animals. In both, the direction of the turns was that expected on the assumption that an uncrossed pathway would cause ipsilateral turns. We conclude that such a pathway exists. While both groups of animals turned in the expected directions, they did so for stimuli at unexpected locations. Increasingly eccentric stimulus locations to one side of the mid-sagittal plane were associated with increasing amplitude turns to the other. The observation suggests that tectal regions mapping areas of visual space to one side of the mid-sagittal plane are capable of triggering turns not only in that direction but in the opposite direction as well. In the case of ansulate commissure section, mirrored orienting responses were observed for tactile stimuli as well. These and other behavioral anomalies described in the preceding papers [Kostyk and Grobstein (1986) Neuroscience 21, 41-55 and 57-82] suggest that between the topographic retinotectal projection and the premotor circuitry for orienting there may exist an intermediate processing step, one in which stimulus location is represented in a generalized spatial coordinate frame.     

Neuronal organization underlying visually elicited prey orienting in the frog--II. Anatomical studies on the laterality of central projections

A complete transverse hemisection of the neuraxis just caudal to the optic tectum in the frog, Rana pipiens, results in a failure to orient toward stimuli in one visual hemifield [Kostyk and Grobstein (1986) Neuroscience 21, 41-55]. The extent of the deficit area implies disturbances in the outputs triggered by both tectal lobes. In this paper we report studies aimed at determining more precisely what damage is involved in producing the hemisection deficit, with the broader objective of identifying particular neural structures which may be important in visually elicited orienting. Small lesions at the level of the hemisection which are restricted to the ventromedial white tracts result in an orienting deficit identical to that produced by a complete hemisection. Large lesions which spare the ventromedial white tracts are without significant effect on orienting turns. The finding is consistent with the hypothesis that the hemisection deficit results from interruption of tectal outflow paths. Interestingly, partial damage of the ventromedial white tracts does not result in disconnection of any local tectal region from premotor circuitry but instead systematically alters the turns triggered from all tectal regions. Ventrolateral lesions at the same level do not produce deficits in orienting but do disturb optokinetic behavior. Introduction of horseradish peroxidase into ventromedial lesions produces retrograde labeling in a large number of structures both rostral and caudal of the lesion. Labeling patterns following introduction of horseradish peroxidase into ventrolateral lesions, which do not affect orienting turns, were qualitatively similar but differed quantitatively. The observed patterns of tectal cell labeling make it unlikely that the hemisection deficit can be accounted for in terms of interruption of direct projections deriving from complementary regions of the two tectal lobes. They also indicate that if there exists an uncrossed tectal outflow adequate to trigger orienting turns, it must be by way of an indirect projection. A more general analysis of the labeling patterns suggests that a crossed tectal projection and uncrossed projections from three midbrain tegmental nuclei (the anterodorsal tegmental nucleus, the nucleus profunds lateralis and the nucleus of the medial longitudinal fasciculus) are likely to be involved in triggering orienting turns. The three midbrain tegmental nuclei are of particular interest in that they provide possible anatomical substrates for an indirect uncrossed descending tectal outflow path.     

The organization of descending tectofugal pathways underlying orienting in the frog,Rana pipiens

We have studied the visually triggered orienting behavior of frogs following complete unilateral transection of the neuraxis at the junction of the medulla and spinal cord, as well as after smaller lesions at the same level. Complete transection produces the same behavioral deficit as previously reported (Kostyk and Grobstein 1982, 1987a) for a similar lesion at the junction between midbrain and medulla. Lesioned frogs failed to turn toward stimuli at all locations in the ipsilateral visual hemifield, responding instead with forwardly directed movements in which there was a persistance of variations related to stimulus elevation and distance. Responses to stimuli in the contralateral visual hemifield were normal. Similar deficits were seen after smaller lesions restricted to a medial white tract. Partial damage to the tract resulted in turns of reduced amplitude for stimuli throughout the ipsilateral hemifield. Lesions to adjacent tissue were without effect on the behaviors studied. In all animals, we observed a strong correlation between turn amplitude for lateral stimuli and the distance at which the animals switched from snapping to hopping. These observations provide new evidence that a transformation from a retinocentric to a lateralized and parcellated form of spatial representation occurs in going from the retinotectal projection to the descending tectofugal pathway in the caudal midbrain, and that this form of representation remains stable until the spinal cord. A second transformation involved in determining the actual movement to be triggered must occur subsequently. Our findings also suggest that the signals underlying orienting turns may not descend into the spinal cord on tectospinal axons, and suggest that the lateralization of descending signals probably occurs coincidentally with a synaptic relay in the midbrain tegmentum.     

Head and body movements produced by electrical stimulation of superior colliculus in rats: effects of interruption of crossed tectoreticulospinal pathway

Stimulation of the superior colliculus in rats produces movements of the head and body that resemble either orientation and approach towards a contralateral stimulus, or avoidance of, or escape from, such a stimulus. A variety of evidence indicates that the crossed descending pathway, which runs in the contralateral predorsal bundle to the pontomedullary reticular formation and the spinal cord, is involved in orienting movements. The nature of this involvement was investigated, by assessing the effects on tectally-elicited movements of midbrain knife-cuts intended to section the pathway as it crosses midline in the dorsal tegmental decussation. As expected, ipsilateral movements resembling avoidance or escape were little affected by dorsal tegmental decussation section, whereas contralateral circling movements of the body were almost abolished. However, contralateral movements of the head in response to electrical stimulation were not eliminated, nor were orienting head movements to visual or tactile stimuli. There was some suggestion that section of the dorsal tegmental decussation increased the latency of head movements from electrical stimulation at lateral sites, and decreased the accuracy of orienting movements to sensory stimuli. These results support the view that the crossed tectoreticulospinal system is concerned with approach rather than avoidance movements. However, it appears that other, as yet unidentified, tectal efferent systems are also involved in orienting head movements. It is possible that this division of labour may reflect functional differences between various kinds of apparently similar orienting responses. One suggestion is that the tectoreticulospinal system is concerned less in open-loop orienting responses (that are initiated but not subsequently guided by sensory stimuli), than in following or pursuit movements.     

Organization of the crossed tecto-reticulo-spinal projection in rat--I. Anatomical evidence for separate output channels to the periabducens area and caudal medulla.

The superior colliculus has been used to study principles of sensorimotor transformation underlying the guidance of orienting movements by multimodal sensory stimuli. We have previously suggested that there may be two different classes of mechanism which can produce orienting-like movements towards a novel event; one that locates a stimulus on the basis of remembered position, and another which uses continuous feedback relating to target velocity. The crossed descending pathway of the superior colliculus is widely considered the projection most likely to relay signals associated with the production of orienting movements. However, if different neural mechanisms are used to produce functionally distinct types of orienting, we might expect this pathway to have separate anatomical components related to function. The purpose of the present experiment was to see if collicular fibres innervating two important pre-motor targets of the crossed descending pathway, the periabducens area and the caudal medulla-spinal cord, come from the same population of tectal cells. One of the retrogradely transported fluorescent tracers (Diamidino Yellow) was injected into the periabducens area, and another (True Blue or Fast Blue) was injected into tectospinal fibres at the level of the ventromedial caudal medulla. Under these conditions we found: (i) less than 10% of labelled cells within the superior colliculus contained both tracers; (ii) the bulk of singly labelled cells projecting to the periabducens area or the caudal medulla were concentrated at different locations within the colliculus, (iii) in regions of the superior colliculus where there was overlap of singly labelled cells, neurons projecting to the periabducens area or the caudal medulla could be distinguished morphologically. These data provide three classes of evidence which indicate that the crossed descending projection in rat can be subdivided into at least two relatively independent anatomical components. This conclusion may, in part, provide an anatomical substrate for the functional dissociations proposed for orienting movements.     

Both striate cortex and superior colliculus contribute to visual properties of neurons in superior temporal polysensory area of macaque monkey

Although the tectofugal system projects to the primate cerebral cortex by way of the pulvinar, previous studies have failed to find any physiological evidence that the superior colliculus influences visual activity in the cortex. We studied the relative contributions of the tectofugal and geniculostriate systems to the visual properties of neurons in the superior temporal polysensory area (STP) by comparing the effects of unilateral removal of striate cortex, the superior colliculus, or of both structures. In the intact monkey, STP neurons have large, bilateral receptive fields. Complete unilateral removal of striate cortex did not eliminate visual responses of STP neurons in the contralateral visual hemifield; rather, nearly half the cells still responded to visual stimuli in the hemifield contralateral to the lesion. Thus the visual properties of STP neurons are not completely dependent on the geniculostriate system. Unilateral striate lesions did affect the response properties of STP neurons in three ways. Whereas most STP neurons in the intact monkey respond similarly to stimuli in the two visual hemifields, responses to stimuli in the hemifield contralateral to the striate lesion were usually weaker than responses in the ipsilateral hemifield. Whereas the responses of many STP neurons in the intact monkey were selective for the direction of stimulus motion or for stimulus form, responses in the hemifield contralateral to the striate lesion were not selective for either motion or form. Whereas the median receptive field in the intact monkey extended 80 degrees into the contralateral visual field, the receptive fields of cells with responses in the contralateral field that survived the striate lesions had a median border that extended only 50 degrees into the contralateral visual field. Removal of both striate cortex and the superior colliculus in the same hemisphere abolished the responses of STP neurons to visual stimuli in the hemifield contralateral to the combined lesion. Nearly 80% of the cells still responded to visual stimuli in the hemifield ipsilateral to the lesion. Unilateral removal of the superior colliculus alone had only small effects on visual responses in STP. Receptive-field size and visual response strength were slightly reduced in the hemifield contralateral to the collicular lesion. As in the intact monkey, selectivity for stimulus motion or form were similar in the two visual hemifields. We conclude that both striate cortex and the superior colliculus contribute to the visual responses of STP neurons. Striate cortex is crucial for the movement and stimulus specificity of neurons in STP.(ABSTRACT TRUNCATED AT 400 WORDS)     

Restoration of acoustic orienting into a cortically deaf hemifield by reversible deactivation of the contralesional superior colliculus: the acoustic "Sprague Effect"

Removal of all contiguous visual cortical areas of one hemisphere results in a contralateral hemianopia. Subsequent deactivation of the contralesional superior colliculus (SC) nullifies the effects of the visual cortex ablation and restores visual orienting responses into the cortically blind hemifield. This deficit nullification has become known as the "Sprague Effect." Similarly, in the auditory system, unilateral ablation of auditory cortex results in severe sound localization deficits, as assessed by acoustic orienting, to stimuli in the contralateral hemifield. The purpose of this study was to examine whether auditory orienting responses can be restored into the impaired hemifield during deactivation of the contralesional SC. Three mature cats were trained to orient toward and approach an acoustic stimulus (broadband, white noise burst) that was presented centrally, or at one of 12 peripheral loci, spaced at 15 degrees intervals. After training, a cryoloop was chronically implanted over the dorsal surface of the right SC. During cooling of the cooling loop to temperatures sufficient to deactivate the superficial and intermediate layers (SZ, SGS, SO, SGI), auditory orienting responses were eliminated into the left (contracooled) hemifield while leaving acoustic orienting into the right (ipsicooled) hemifield unimpaired. This deficit was temperature-dependently graded from periphery to center. After the effectiveness of the SC cooling loop was verified, auditory cortex of the middle and posterior ectosylvian and anterior and posterior sylvian gyri was removed from the left hemisphere. As expected, the auditory cortex ablation resulted in a profound deficit in orienting to acoustic stimuli presented at any position in the right (contralesional) hemifield, while leaving acoustic orienting into the left (ipsilesional) hemifield unimpaired. The ablations of auditory cortex did not have any impact on a visual detection and orienting task. The additional deactivation of the contralesional SC to temperatures sufficient to cool the superficial and intermediate layers nullified the deficit caused by the auditory cortex ablation and acoustic orienting responses were restored into the right hemifield. This restoration was temperature-dependently graded from center to periphery. The deactivations were localized and confirmed with reduced uptake of radiolabeled 2-deoxyglucose. Therefore deactivation of the right superior colliculus after the ablation of the left auditory cortex yields a fundamentally different result from that identified during deactivation of the right superior colliculus before the removal of left auditory cortex in the same animal. Thus the "Sprague Effect" is not unique to a particular sensory system and deactivation of the contralesional SC can restore either visual or acoustic orienting responses into an impaired hemifield after cortical damage.     

Tail and eye movements evoked by electrical microstimulation of the optic tectum in goldfish

This work studies the tail and eye co-ordinated movements evoked by the focal electrical stimulation of the tectum in goldfish. The aim of the study is to understand better those tectal sites and mechanisms that either remain functionally unaltered or are adaptively modified across vertebrates. Stimulation was applied in various tectal zones, and the characteristics of evoked tail and eye movements were examined as a function of the stimulation site over tectal surface and the stimulus parameters. Two types of response were electrically evoked: the former turned the body and the eyes contraversively towards the source of natural stimulus; the second produced initial ipsiversive turning of the body and eyes, followed by several tail beats. Evoking one or other response depended on both the site and parameters of stimulation, and responses were interpreted as orienting- and escape-like, respectively. Depending on the stimulation site, four different zones in the tectum were distinguished: in the medial zone the stimulus elicited eye and tail movements whose size increased with the distance to the rostral pole. The stimulation of the antero-medial zone evoked contraversive or ipsiversive eye saccades but tail movements were similar, irrespective of eye movements. Stimulation within the extreme antero-medial zone evoked convergent eye movements, and tail displacements turning the body either ipsiversively or contraversively. Stimulation of the posterior zone often evoked complex tail movements and pure horizontal eye saccades. Both orienting- and escape-like responses were also dependent on the stimulus parameters. The relationships between stimulus parameters and tail- and eye-orienting movement characteristics suggest that the velocity and duration might be encoded in different aspects of the tectal activity. Current strength also modified the number of tail beats that appeared during escape-like response. In conclusion, the present data suggest the involvement of the optic tectum not only in orienting but also in escape responses and that movements of eye and tail mediating such responses depend on the tectal active locus together with its level of activity. Received: 24 September 1997 / Accepted: 4 December 1997     

Role of extraocular proprioception in the orienting behaviour of cats

Summary We investigated the effects of unilateral deafferentation of extraocular proprioception on the orienting behaviour of cats. The ophthalmic branch of the Vth cranial nerve, in which most of the extraocular proprioceptive fibers are known to run, was cut unilaterally in adult cats. The animals had been previously trained to jump from a start box to a luminous target at various possible locations in the right or left visual hemifield. The postsurgical orienting performance of the animals, evaluated from the difference between landing position and position of the target, differed from the presurgical performance. The postsurgical errors were typically: (1) ipsiversive to the side of the section, (2) usually of a larger magnitude in the hemifield contralateral to the section, (3) present in binocular as well as in monocular viewing conditions and approximately of the same magnitude for jumps guided by either eye. These findings indicate that extraocular proprioception plays a role in the orienting behaviour of cats.Supported by a fellowship from Scuola Normale Superiore, Pisa     

Nucleus isthmi: its contribution to tectal acetylcholinesterase and choline acetyltransferase in the frog Rana pipiens

The distribution of acetylcholinesterase and the activity of choline acetyltransferase was studied in the tecta of normal frogs and frogs without retinal and/or nucleus (n.) isthmi inputs. In normal animals acetylcholinesterase activity is found primarily in three bands in the outer layers of the tectum-lamina A, laminae C-F, and lamina G. After retinal and contralateral n. isthmi deafferentation three distinct bands of tectal acetylcholinesterase activity are still present. After bilateral n. isthmi deafferentation there is loss of activity in lamina G and reduced activity in lamina A. With retinal and ipsilateral n. isthmi deafferentation, activity is seen only in lamina A. With retinal and bilateral n. isthmi deafferentation there is virtually no acetylcholinesterase activity in the outer tectal layers. Following unilateral retinal deafferentation there is no statistically significant difference in choline acetyltransferase specific activity between intact and deafferented tectal lobes after two, four and nine weeks. With unilateral nucleus isthmi lesions and survival times of between 10 and 40 days, choline acetyltransferase specific activity in the tectal lobe ipsilateral to the ablation is approximately 38% of the specific activity of the contralateral lobe. With bilateral n. isthmi lesions there is a strong correlation between amount of n. isthmi ablated and reduction of choline acetyltransferase activity. In vitro tectal acetylcholine synthesis was also determined in animals with unilateral n. isthmi ablation. On average, tectal lobes ipsilateral to the ablated n. isthmi synthesize acetylcholine at a rate which is approximately 58% of that of contralateral tecta. Collectively, these results imply that n. isthmi is the sole cholinergic input to the frog optic tectum, with ipsilaterally projecting isthmotectal fibers accounting for the greater share.     

Motor responses to localized electrical stimulation of the tectum in the freshwater perch (Perca fluviatilis)

The results of localized electrical stimulation of the teleostean tectum indicate the presence within each tectal lobe of separate motor areas mediating ipsilateral turning, contralateral turning, and rolling movements. Stimulation of caudal regions produced larger turning circles than stimulation of rostral sites. Both these sets of observations conflict with the retinotopic map. Stimulation sites connected with turning and rolling movements were mostly located in the upper layer of the tectum. Other kinds of movement including aggressive behaviour, escape movements, head dipping, and forward swimming were obtained by stimulating the deeper tectal sites and subtectal areas. These results suggest that the tectum may be differentiated into areas with specific motor functions and afferent connections. This has important consequences for studies on optic nerve regeneration and neuronal specificity.     

The lateral reticular nucleus in the cat—II. Effects of lateral reticular lesions on posture and reflex movements

Unilateral lesion of the lateral reticular nucleus produced a postural asymmetry characterized by ipsilateral hypertonia and contralateral hypotonia of the limb extensor muscles. Soon after the operation the cat was unable to stand or walk, and it laid on one side. Within 3 days, it began to walk, but it often deviated to its contralateral side, 'frequently falling in this direction. Some compensation for both postural and motor deficits occurred in chronic preparations maintained up to 154 days after the lesion. The postural asymmetry was reversed by the following operations: (1) section of the ipsilateral VIIIth nerve, (2) electrolytic lesion of the ipsilateral Deiters' nucleus, or (3) ablation of the contralateral vermal cortex of the cerebellar anterior lobe.The lateral reticular nucleus lesion also produced, in the ipsilateral limbs, a transient loss of the proprioceptive placing reaction and a persistent deficit of the tactile placing reflex. These effects on the ipsilateral side were not reversed by the procedures described above.All of these behaviors depended on selective destruction of the lateral reticular nucleus and were not due to damage to the nearby main reticular formation or ascending and descending pathways. Moreover, the postural changes did not involve mesencephalic or higher mechanisms, since they were still observed after decerebration. The forelimbs were affected primarily by lesions involving the dorsomedial, magnocellular part of the lateral reticular nucleus, whereas the hindlimbs also were affected by lesions including the ventrolateral, parvicellular part of the lateral reticular nucleus.The postural asymmetry is attributed to interruption of the crossed spinoreticulocerebellar pathway, acting on the vermal cortex of the anterior lobe and the fastigial nucleus, while the ipsilateral loss of the placing reaction is attributed to interruption of the uncrossed spinoreticulocerebellar pathway acting on the intermediate cortex of the anterior lobe and the interpositus nucleus. The lateral reticular nucleus appears, therefore, to be composed of two, more or less independent, parts, a crossed one being related to major changes in postural tone, equilibrium and locomotion of the entire body, and an uncrossed one restricted to discrete movements of the ipsilateral limbs.     

Spatially precise bilateral arm movements are controlled by the contralateral hemisphere

Previous studies have reported that unilateral proximal arm movements are initiated more quickly in response to visual stimuli directed to the ispilateral hemifield than to the contralateral hemifield. This is thought to reflect differences in intrahemispheric and interhemispheric visuomotor integration. When bilateral movements are performed, this difference in reaction time (RT) is abolished owing to the involvement of bilaterally distributed motor pathways. However, these experiments typically use simple motor tasks that do not emphasise spatial precision. We investigated the hemispheric control of precise unilateral and bilateral arm movements in 12 subjects using a lateralized visual stimulus paradigm and found an ipsilateral RT advantage for both unilateral and bilateral movements. We conclude that the requirement to execute spatially precise movements restricts control to the contralateral hemisphere regardless of whether unilateral or bilateral movements are performed.     

Connectivity of the goldfish optic tectum with the mesencephalic and rhombencephalic reticular formation

The optic tectum of goldfish, as in other vertebrates, plays a major role in the generation of orienting movements, including eye saccades. To perform these movements, the optic tectum sends a motor command through the mesencephalic and rhombencephalic reticular formation, to the extraocular motoneurons. Furthermore, the tectal command is adjusted by a feedback signal arising from the reticular targets. Since the features of the motor command change with respect to the tectal site, the present work was devoted to determining, quantitatively, the particular reciprocal connectivity between the reticular regions and tectal sites having different motor properties. With this aim, the bidirectional tracer, biotin dextran amine, was injected into anteromedial tectal sites, where eye movements with small horizontal and large vertical components were evoked, or into posteromedial tectal sites, where eye movements with large horizontal and small vertical components were evoked. Labeled boutons and somas were then located and counted in the reticular formation. Both were more numerous in the mesencephalon than in the rhombencephalon, and ipsilaterally than contralaterally, with respect to the injection site. Furthermore, the somas showed a tendency to be located in the area containing the most dense labeling of synaptic endings. In addition, labeled boutons were often observed in close association with retrogradely stained neurons, suggesting the presence of a tectoreticular feedback circuit. Following the injection in the anteromedial tectum, most of the boutons and labeled neurons were found in the reticular formation rostral to the oculomotor nucleus. Conversely, following the injection in the posteromedial tectum, most of the boutons and neurons were also located in the caudal mesencephalic reticular formation. Finally, boutons and neurons were found in the rhombencephalic reticular formation surrounding the abducens nucleus. They were more numerous following the injection in the posteromedial tectum. These results demonstrate characteristic patterns of reciprocal connectivity between physiologically different tectal sites and the mesencephalic and rhombencephalic reticular formation. These patterns are discussed in the framework of the neural substratum that underlies the codification of orienting movements in goldfish. This work is dedicated to the memory of Dr. Olivier Hardy, who recently passed away. He devoted years of effort with us in previous studies aimed at elucidating the neural substratum underlying decodification of the tectal signal in goldfish. We are indebted to him for many years of friendship.     

Retrograde degeneration of myelinated axons and re-organization in the optic nerves of adult frogs (Xenopus laevis) following nerve injury or tectal ablation

Summary The optic nerve proximal to the lesion (toward the retina) was examined by light and electron microscopy in adultXenopus laevis after various types of injury to optic nerve fibres. Intraorbital resection, transection or crush of the optic nerve or ablation of the contralateral optic tectum all resulted in marked alterations in the myelinated axon population and in the overall appearance of the nerve proximal to the site of injury. Examination of the nerves from 3 days to 6 months postoperatively indicated that a progressive, retrograde degeneration of myelin and loss of large-diameter axons occurred throughout the retinal nerve stump regardless of the type of injury or distance of the injury from the retina. The retinal stump of nerves receiving resection or transection showed a nearly complete loss of myelin and large-diameter axons while the degree of degeneration was subtotal in nerves receiving crush injury or after lesions farther from the retina (i.e. tectal ablation). In addition, the entire retinal nerve stump after all types of injury was characterized by the appearance of an actively growing axon population situated circumferentially under the glia limitans. The latter fibres are believed to represent regrowing axons which are being added onto the nerve, external to the original axon population and are suspected to modify actively the glial terrain and glia limitans.     

Structure-function relationships in the primate superior colliculus. I. Morphological classification of efferent neurons

1. Neurons in the superior colliculus (SC) of anesthetized paralyzed squirrel monkeys were injected intracellularly with horseradish peroxidase (HRP) to establish a morphological classification of tectal efferent neurons in this species. These neurons were physiologically identified by their antidromic responses following stimulation of the contralateral predorsal bundle or SC. These cells also responded with postsynaptic potentials to stimulation of the ipsilateral substantia nigra and cerebral peduncle and the contralateral tectum. 2. Quantitative light microscopic analysis of the somatodendritic profiles and axonal trajectories of 27 recovered cells revealed the existence of three major groups of tectal efferent neurons: L (n = 7), X (n = 8), and T (n = 12). 3. L neurons are small or medium size cells with relatively elaborate dendritic trees and are located mainly in the superficial layers of the SC. They participate in the ipsilateral descending and dorsal ascending tectofugal bundles. Intrinsic collaterals of L axons deploy a large number of boutons both near the parent cell body and more ventrally within the deeper tectal layers. 4. X neurons are mostly large in size and multipolar in shape with relatively complex dendritic trees. Their cell bodies are situated mainly in the stratum griseum intermedium and occasionally in the stratum opticum. Axons of X neurons participate in the crossed descending and ipsilateral ventral ascending projections of the SC. In addition, the axonal system of about half of the X neurons includes recurrent collaterals. 5. T neurons are located mainly in the ventral stratum opticum and the dorsal stratum griseum intermedium. They have small or medium-sized, trapezoid or ovoid cell bodies and relatively simple radiating or vertical dendritic trees. Their axons usually participate in two of the major tectofugal bundles besides providing a commissural component and recurrent collaterals. 6. Morphological details revealed in the present study support the notion that distinct tectofugal axonal systems originate from efferent neurons of the primate SC that differ both as to their location in the tectum as well as the appearance of their somata and dendritic trees. The resulting morphological classification of tectal efferent cells provides a framework for the analysis of tectal function in terms of populations of identified neurons.     

Aberrant retinal projections to midbrain targets mediate spared visual orienting function in hamsters with neonatal lesions of superior colliculus

Summary Rodents, cats, and most nonmammalian vertebrates with bilateral tectal deafferentation or ablation in adulthood are extremely deficient at orienting to visual stimuli; yet animals with neonatal lesions of superficial layers of the superior colliculus (SC) show partial sparing of this response, particularly for targets in the central visual field. In this study, we sought to determine whether these spared orienting abilities are mediated by aberrant retinal projections to the remaining intermediate layers of the SC, or whether visual cortex (VC) mechanisms or alternative behavioral strategies are responsible. Neonatal golden hamsters received either bilateral heat lesions of the SC (rlSC), or a heat lesion of the right SC and enucleation of the right eye (rSCrE). This latter procedure causes axons from the left eye to recross the tectal midline and terminate in the wrong (left) SC (Schneider 1973). As adults, both groups of hamsters were extremely deficient in visually guided approach to stationary targets, although rlSC-lesioned hamsters showed some sparing for central field targets and rSCrE-lesioned hamsters often made wrong-direction turns for targets in the left peripheral field. We then subjected both groups of neonatally lesioned hamsters to bilateral aspiration lesions of the VC. Retesting showed no change in visual orienting behavior as a result of the cortical lesions. Labeling of the optic tract with horseradish peroxidase (HRP) revealed abundant aberrant retinal projections to remaining intermediate layers of the SC and thalamic nucleus lateralis posterior (LP), as well as supernormal innervation of pretectal nuclei, the dorsal terminal nucleus of the accessory optic tract, and the ventral nucleus of the lateral geniculate body (LGv). We conclude that the spared visual orienting capabilities of hamsters with rlSC and rSCrE lesions are mediated by the aberrant midbrain projections, and that cortical mechanisms are not involved in spared visual orienting functions following these neonatal lesions.     

Effects of lesion of paramedian pontomedullary reticular formation by kainic acid injection on the visually triggered horizontal orienting movements in the cat

A localized lesion was made in the nucleus reticularis pontis caudalis (NRPC) and the nucleus reticularis gigantocellularis (NRG) by kainic acid injection, and its effects on visually triggered orienting eye and head movements in the horizontal direction were investigated in alert head-free cats. Before the lesion, trained cats could orient the head and eyes to the target presented in the periphery of the visual field, with rapid eye (saccade) and swift head movements. After the unilateral lesion, they were unable to direct the head toward the target on the lesioned side in 64% of the trials tested during 2 weeks after the lesion, while they managed in 36% of the trials, although the movement was reduced both in speed and amplitude. The saccadic eye movement was completely absent through all trials. In contrast, eye and head movements to the intact side were as normal as the control. The present results suggest that the NRPC and NRG play an essential role in relaying a descending command of ipsiversive visually triggered orienting movements of eyes and head in the horizontal direction.     

Anatomical pathways from the optic tectum to the spinal cord subserving orienting movements in the barn owl

Summary Electrical stimulation of the optic tectum in many vertebrate species elicits eye, head or body orienting movements in the direction of the receptive field location recorded at the site of stimulation; in the barn owl, tectal stimulation produces short latency saccadic head movements (du Lac and Knudsen 1990). However, the barn owl, like other avians, lacks a direct projection from the tectum to the spinal cord, implying that less direct connections underlie tectally mediated head movements. In order to determine the pathways by which the tectum gains access to spinal cord circuitry, we searched for overlap regions between tectal efferent projections and the locations of cells afferent to the spinal cord. Tectal efferent pathways and terminal fields were revealed by anterograde labeling using horseradish peroxidase (HRP) or tritiated amino acids injected into the optic tectum. Cells afferent to the spinal cord were identified by means of retrograde labeling using HRP, rhodamine, or rhodamine-coupled latex beads injected into the cervical spinal cord. A comparison of results from the anterograde and retrograde labeling experiments demonstrated several areas of overlap. All of the cell groups that both received heavy tectal input and contained a high proportion of cells projecting to the spinal cord were located in the medial half of the midbrain and rhombencephalic tegmentum, and included the red nucleus, the interstitial nucleus of Cajal, the medial reticular formation, the nucleus reticularis pontis gigantocellularis, and the nucleus reticularis pontis oralis. All of these cell groups receive their tectal input from the medial efferent pathway, one of three major output pathways from the tectum. The other two output pathways (the rostral and the caudal) project to regions containing no more than a few scattered cells that are afferent to the spinal cord. Based on these data and on the functions of homologous cell groups in other vertebrates, we hypothesize that the medial efferent pathway and its brainstem target nuclei are primarily responsible for tectally mediated orienting head movements in the barn owl.     

Phrenic reflexes in the decerebrate and spinal rabbit

Investigations were undertaken to study the characteristics of phrenic reflexes with partial or total elimination of the descending neuronal pathways. Experiments were performed on 17 decerebrate, vagotomized, paralysed and artificially ventilated rabbits. The experimental procedure included a midsagittal section of the medulla or a hemisection followed by a total transection of the spinal cord at C1. The effects of compression of the rostral or caudal parts of the thorax, pressure on the muscles at the lumbar level and passive movements of the hindlimb were studied on the efferent vagal and phrenic neurograms. Partial elimination of the descending pathways evoked an increase in the intensity of the spinal reflexes. Characteristics of the reflexes which we have obtained after lesions of the medulla or spinal cord enable us to search for their central path. After transection of the spinal cord, no sustained phasic phrenic nerve activities were observed. The results suggest that after high cordotomy the phrenic motoneuronal pool has a potential capability for generating phasic bursts and additional inputs are required for their development.