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R B Masterton

Publications and source records attributed to R B Masterton.

At least 37 records · Page 2Linked to original sources

Descending pathways to the spinal cord: II. Quantitative study of the tectospinal tract in 23 mammals.

To study the early evolution of the mammalian motor systems, we have collected quantitative data on the nuclear origins of tracts descending into the spinal cord in 99 individuals representing 23 species of mammals and one species of reptile. In each individual, the spinal cord was hemisected at the C1-C2 junction and raw HRP immediately applied to the cut fibers. After a 3-day survival period, brain and spinal cord sections were treated with conventional tetramethylbenzidine procedures. In every case, this procedure resulted in heavy retrograde labeling of neural somata throughout the neuraxis from coccygeal cord to cerebral neocortex. Many thousands of supraspinal neurons were vividly labeled within at least 27 discrete cell groups in every mammal (Nudo and Masterton, '88). Despite the vast number and wide diversity of heavily labeled neurons, however, relatively few labeled somata were found in the superior colliculus. The total number of labeled cells in the tectum contralateral to the hemisection was highest in the cat (909) and second highest in the raccoon (628). In the remaining animals, the number was considerably less--averaging only 243 in the 23 mammalian species, 193 in the 21 noncarnivores, and 95 in the iguana. In 7 species of primates the average was 220, and in 3 species of Old World monkeys the average was 142. This wide variation in the number of tectospinal neurons is not related to body size, brain size, or absolute and relative tectum size. Arranging the animals in order of their kinship or recency-of-last-common-ancestor with Man, the average number of labeled tectal cells tends to decrease slightly, whereas arranging the same animals in order of their kinship with the cat or raccoon shows a marked and statistically reliable increase. Neither the evolutionary increase in the tectospinal tract along the Carnivora lineage nor the slight decrease along Man's lineage is altered by mathematical corrections for allometric or scaling factors. Of an array of morphological, visual, motor, and ecological traits tested statistically as a possible source of the variation in size of the tectospinal tract, only a primarily carnivorous feeding preference was found to be reliably related. The relatively small number of tectospinal fibers in most mammals in our sample, including the primates, suggests that the tectospinal tract in Man may be quite small, perhaps far too small to warrant continuing description as a "major descending tract."

Animals↗

Descending pathways to the spinal cord: a comparative study of 22 mammals.

In order to estimate the qualitative commonalities and range of variation among major descending spinal pathways relevant to mankind's ancestral lineage, the supraspinal cell groups originating fibers descending directly to the spinal cord were examined in 22 mammalian species. In a standardized retrograde tract-tracing procedure, flakes of raw HRP were applied directly to the freshly cut fibers of the spinal cord after it had been hemisected at the C1-C2 junction. After a 72-hour survival period, brain and spinal cord tissues were processed by conventional HRP-processing techniques. This procedure was performed on 94 individual animals. Of this total, 41 individual cases were eliminated by a rigorous culling procedure. The results are based on 53 individuals representing 15 species selected for their successive kinship with mankind and seven species in two other lineages selected for the convergence of their visual or sensorimotor systems with anthropoids. The 22 species represent 19 genera, 14 families, eight orders, and two subclasses of Mammalia. The results show that at least 27 supraspinal cell groups, each containing intensely labeled cells, can be readily identified in each of the species. Despite vast quantitative differences in cell number and cell size, this qualitative uniformity among the relatively large number of diverse taxa suggests that the same pathways were probably present in the extinct ancestors throughout mankind's mammalian lineage and are probably still present in extant viviparous mammals as well. If so, these pathways are as old in phylogenetic history as the last common ancestor of marsupial and placental mammals--dating from the late Jurassic to early Cretaceous, perhaps 145-120 million years ago. Further comparison of the results with similar experimental findings in members of other vertebrate classes supports the notion that several of these same pathways can be traced to even more remote ancestry, with some possibly as old as the entire vertebrate subphylum--dating from the early Devonian or before, perhaps 430 million years ago. Within mankind's ancestral lineage, from the appearance of vertebrates to the appearance of mammals, there seems to have been an irregular stepwise augmentation of the set of descending pathways until the full mammalian complement was finally attained with the appearance of the corticospinal tract.

Animals↗

Role of the acoustic striae in hearing: contribution of dorsal and intermediate striae to detection of noises and tones.

1. Behavioral thresholds were obtained from cats, first with only their right ear and right dorsal, intermediate, and ventral acoustic striae (DAS, IAS, and VAS, respectively) intact, and then again with only their right ventral acoustic stria intact. 2. Using usual definitions of "threshold" the loss of the dorsal and intermediate acoustic striae results in no measurable deficit in the detection of noises or tones on a silent background. 3. In sharp contrast, even partial damage of the ventral acoustic stria (i.e., trapezoid body section) results in marked deficits in sound detection. 4. Therefore, the ventral acoustic stria is both necessary and sufficient to maintain normal acoustical sensitivity. 5. However, loss of the dorsal and intermediate striae seems to result in a degradation of reliability in the detection of suprathreshold sounds--perhaps akin to a deficit in listening.

Acoustic Stimulation↗

Stimulation-induced [14C]2-deoxyglucose labeling of synaptic activity in the central auditory system.

The relative contribution of active synapses and discharging neurons to [14C]2-DG labeling in film autoradiographs of the auditory system was studied in a series of three experiments, two in cat, one in chick. In the first, the lateral superior olive in cats was specially prepared so that its inhibitory afferents could be stimulated without concurrent stimulation of its excitatory afferents. The film autoradiographs showed clear 2-DG labeling in the vicinity of the activated inhibitory synapses. In the second experiment, the medial superior olive in cat was specially prepared so that it could be stimulated antidromically without concurrent orthodromic stimulation. The film autoradiographs showed little or no elevations in 2-DG labeling of the antidromically stimulated nucleus over its unstimulated contralateral control despite heavy labeling of nearby orthodromically stimulated nuclei. In the third experiment, the highly polarized nucleus laminaris of a chick was specially prepared so that one set of its excitatory afferents could be stimulated without concurrent stimulation of the other set. The film autoradiographs showed that the distribution of heavy 2-DG labeling matched the distribution of the activated synapses and not the distribution of discharging postsynaptic membrane. The outcomes of the three experiments taken together suggest that it is active synapses and not actively discharging neurons that dominate typical [14C]2-DG film autoradiographs, at least of the vertebrate central auditory system. It follows that [14C]2-DG labeling of central auditory system tissue is not necessarily evidence of local cell discharge but instead evidence of synaptic activity whether excitatory or inhibitory, and whether or not it is accompanied by significant levels of postsynaptic cell discharge.

Acoustic Stimulation↗

Origin of mammalian thalamocortical projections. I. Telencephalic projections of the medial geniculate body in the opossum (Didelphis virginiana).

Telencephalic projections from the medial geniculate nucleus (MG) in opossum were traced with tritiated leucine autoradiography and by horseradish peroxidase and fluorescent dye retrograde labeling techniques. The results show that the opossum's MG contains two separate populations of neurons-one in the anterior two-thirds of MG projecting to auditory neocortex, the other occupying the entire caudal one-third of MG and projecting mostly to lateral amygdala and putamen. Because the subcortical projection of the MG in opossum is larger than that seen in any other mammal to date, it is reminiscent of the subcortical projections of the MG in reptiles and birds. Furthermore, when the subcortical projections of the MG in reptiles and opossums are compared with similar subcortical projections of the MG in rats, cats, and monkeys, the proportion of the MG neurons projecting to subcortical structures is seen to be inversely related to the recency of each animal's common ancestry with primates. The possibility that the subcortical projection of the MG in mammals is homologous with that seen in reptiles or birds implies that it might be a dwindling vestige of the projection present in the common ancestry of reptiles and mammals.

Animals↗

The sensory contribution of a single vibrissa's cortical barrel.

The sensory contribution of the cortex containing the cortical barrel of the C1 vibrissa was studied in rats using the ablation-behavior method. Three independent experiments were performed, each requiring stimulus transduction by the C1 vibrissa but varying in their perceptual demands. The first required detection of sinusoidal oscillations of the vibrissa generated by an oscillating airstream directed vertically onto the vibrissa tip. The second required detection of a change in rate of the oscillation. The third required the blinded rat to jump a gap in an elevated runway after palpating the far side with its vibrissa. Psychophysical determinations of the single vibrissa system's thresholds before and after ablation of the cortex containing its barrel show that normal sensitivity either for detecting an oscillation or for detecting a change in oscillation frequency are not dependent on either the contralateral or the ipsilateral cortical barrelfield. In contrast to the lack of effect of barrelfield ablation on the spatial and temporal acuity of the vibrissa, the third experiment shows that a rat's ability to collect situation-relevant information with the vibrissa is lost after ablation of the cortex containing its contralateral barrel but not after ablation of the cortex containing its homologous ipsilateral barrel. The results of repeated retesting of an individual rat's ability to make a jump-no jump decision on the basis of vibrissa-transduced information at each stage of a series of successive single-vibrissa removals and unilateral barrelfield ablations show that the loss of the cortex containing the vibrissa's contralateral barrel is tantamount to loss of the vibrissa itself.

Animals↗

Origin of interhemispheric fibers in acallosal opossum (with a comparison to callosal origins in rat).

The neocortical origins of the anterior commissure in the acallosal, marsupial opossum were studied with the horseradish peroxidase (HRP) method. Following complete surgical transection of the anterior commissure, HRP was applied directly to the cut fiber tips. This procedure resulted in very large numbers of vividly labeled cells within the neocortex. The labeled cells were plotted and counted for comparison among cytoarchitectonic areas and among cortical layers. For comparative purposes, the neocortical origins of the corpus callosum are studied with the same procedure in the rat. No cytoarchitectonic area was entirely devoid of labeled cells in either species. The concentration of labeled cells throughout the entire neocortex averaged 25.2 cells/0.05 mm3 in opossum and 31.2 cells/0.05 mm3 in rat. The concentrations of labeled cells were correlated for the eight cytoarchitectonic areas common to the two species, though they were different enough in number to be statistically reliable. The distribution of labeled cells both among and within cytoarchitectonic areas was often more homogeneous in opossum than in rat. Although cortical layer 1 had no labeled cells in either species, the distribution of labeled cells across the remaining cortical layers differed sharply between the two species. In opossum, layer 3 had the most labeled cells (averaging 55% of the total number) while layer 5 had considerably less (averaging 12%). In rat, layer 5 had as many labeled cells as layer 3--both layers averaging 43% of the total number of labeled cells. In both species, striate cortex deviated markedly from other cytoarchitectonic areas. Although both species had very few labeled cells in striate cortex, those that were labeled were invariably supragranular in opossum and infragranular in rat. The similarities and dissimilarities in the topographic distribution of the origins of the two types of interhemispheric fiber systems seem to parallel the degree of cortical (and thalamic) differentiation in the two animals. However, the differences in laminar distribution are much greater and in particular, the small contribution of layer 5 in opossum as opposed to rat may well be functionally significant.

Animals↗

Acoustic chiasm II: Anatomical basis of binaurality in lateral superior olive of cat.

The afferent projections to the lateral superior olive (LSO) were examined with horseradish peroxidase, horseradish peroxidase-wheat germ agglutinin conjugate, 125I-wheat germ agglutinin and tritiated leucine autoradiograhy, anterograde axonal degeneration, and 14C-2-deoxyglucose methods. The pathway to the ipsilateral LSO orginates in the spherical cells in anteroventral cochlear nucleus. Although some of the fibers pass above the lateral nucleus of the trapezoid body, most pass below it and turn at right angles to enter the LSO either directly through its ventral, lateral, or dorsal borders, or through its ventral or dorsal hilus. They end in unpolarized terminal fields throughout the LSO. Most if not all of these fibers are true collaterals of axons continuing across the midline in the trapezoid body. Verifying Held's (1893) finding of a major direct projection from the cochlear nucleus to the contralateral medial nucleus of the trapezoid body (MTB) and Rasmussen's ('46) finding of a major projection from the MTB to the LSO, the present results illustrate that this two-neuron pathway probably supplies all but a very small component of the relatively direct input to the LSO from the contralateral ear. This pathway originates in the globular cells of the ventral cochlear nucleus and relays mostly though not exclusively through the "principal cells" in the more rostral parts of the MTB. It terminates mostly in perisomal endings in unpolarized fields throughout the LSO, though most heavily within the (high frequency) medial and middle limbs and less heavily in the LSO's (low frequency) lateral limb. In addition to this indirect pathway, there is a small direct pathway to the contralateral LSO as suggested by Goldberg and Brown ('69) and Warr ('72, '82). This direct pathway to the contralateral LSO, like the direct ipsilateral pathway, probably originates in the spherical cell region of the ventral cochlear nucleus, crosses the midline in the trapezoid body, and terminates in a small circumscribed area within the LSO's ventromedial (high frequency) area. The 2-deoxyglucose method applied to cats in which the ipsilateral and contralateral pathways have been surgically isolated shows that each of the pathways converging on the LSO is topographically and tonotopically organized with the ipsilateral and the combined contralateral terminations in strict tonotopic register.

Animals↗

Neural mechanisms for sound localization.

Although the efforts to find a place map of sound direction within the auditory system of mammals has been reinspired by the recent discoveries in owl, progress to date has not been encouraging. Neither the inferior colliculus nor auditory cortex has yielded immediate evidence of such a map, despite ingenious and persistent efforts to find it. Thus, at present, the evidence suggests that a head-referenced map of auditory space is more likely to be found in structures more motor than sensory in function--in the deep layers of the superior colliculus or brainstem tegmentum, for example. Insofar as these structures have been implicated in eye, ear, and head orientation toward a sound source, one might expect that premotor units for orienting would be sensitive to sound direction and thus, collectively, constitute a map of auditory azimuth isomorphic to the map of motor azimuth. However, even for these structures, the possibility for significant variation among mammalian species exists. Because many candidate motor structures (such as the deep superior colliculus) receive input from the cerebral cortex, and because the role of auditory cortex in sound localization seems to vary widely among mammals (38, 51) an equal amount of variation in auditory-motor maps may also exist.

Animals↗

The role of the corticospinal tract in the evolution of human digital dexterity.

A morphometric analysis of the corticospinal tract's relation to digital dexterity was performed on 21 species theoretically related to man's ancestral lineage. The results indicate that the Primate line is not unique among mammals with respect to the cortical control of digital dexterity. A comparative analysis suggests that two changes took place early in Primate evolution: a reduction in functional distance (i.e. number of synapses) between neocortex and spinal motor neurons innervating the digits, and an extension of direct neocortical influence beyond the cervical segments of the spinal cord. A further change progressed throughout Primate evolution, from the mid-Eocene to the present, in which the overall size of the corticospinal tract increased steadily as though consolidating the cortical influence over body musculature, especially that of the digits.

Animals↗

Acoustic chiasm: efferent projections of the lateral superior olive.

The efferent connections of the cat's lateral superior olive (LSO) were examined first with kainic acid-induced anterograde degeneration and tritiated leucine autoradiography and then by systematic repetition of HRP and fluorescent dye retrograde tract-tracing techniques. The results show that virtually all LSO cells have axons ascending either contralaterally or ipsilaterally to high pontine and midbrain levels of the brainstem. Most terminate in the ventrolateral division of either the ipsilateral or contralateral central nucleus of the inferior colliculus, some terminate in the ipsilateral or contralateral dorsal nucleus of the lateral lemniscus, and a small number terminate in the ipsilateral intermediate nucleus of the lateral lemniscus. Only a small proportion (less than 5%) of LSO cells project to both sides via axon collaterals. The ipsilateral, contralateral, and bilateral projections arise from three overlapping subpopulations of cells within LSO: Those projecting ipsilaterally are concentrated in its lateral limb; those projecting contralaterally are concentrated in its medial limb; the few projecting bilaterally are thinly scattered throughout. Therefore, a lateral-medial gradient is present across LSO based on the laterality of its cell's efferent targets. This gradient parallels LSO's tonotopic gradient: The higher the characteristic frequency of an LSO cell, the more likely it is to project contralaterally. This arrangement of LSO's ascending projections, with most of its lateral cells projecting ipsilaterally and most of its medial cells projecting contralaterally, is similar to the arrangement of the optic chiasm in animals with overlapping eye-fields. Its presence seems to provide an anatomical basis for some recent electrophysiological and behavioral reports of chiasm-like properties of the superior olivary complex.

Animals↗

Origins of anthropoid intelligence IV. Role of prefrontal system in delayed alternation and spatial reversal learning in a conservative eutherian (Paraechinus hypomelas).

A conservative eutherian mammal (the hedgehog, Paraechinus hypomelas) was tested on delayed alternation performance and spatial reversal learning before and after ablations of the prefrontal cortex. The anatomical results show that the cortical focus of the projections of the medial dorsal nucleus, the prefrontal cortex, does not include the neocortex on the dorsal convexity of the hedgehog's frontal lobe but, instead, the perirhinal and pregenual neocortex immediately surrounding the frontal convexity. The behavioral results show that normal performance of hedgehogs on these two behavioral tests depends upon the integrity of their prefrontal cortex, but not on the integrity of their frontal convexity or olfactory bulbs. The similarity in the results obtained from prefrontal hedgehogs and a divergent variety of other species with prefrontal ablations indicates that the role of the prefrontal system in the abilities measured by these two tests is at least as old as Eutheria and, thus, probably imposed persistent constraints on subsequent evolutionary modifications of the prefrontal system.

Animals↗

Ascending auditory afferents to the nuclei of the lateral lemniscus.

Afferents from the hindbrain auditory system to the nuclei of the lateral lemniscus were analyzed by the use of orthograde and retrograde axon-tracing techniques. Three divisions of the nuclei of the lateral lemniscus, a dorsal, an intermediate, and a ventral division are discussed. The dorsal nucleus of the lateral lemniscus is a recipient of afferents from cells located mainly in the superior olivary complex and the contralateral dorsal nucleus of the lateral lemniscus. It receives direct afferents from only a few cells in the cochlear nuclei. In sharp contrast, the ventral nucleus of the lateral lemniscus is the recipient of afferents from many cells in the contralateral ventral cochlear nucleus and from only a few cells in the superior olivary complex. Further, it receives no afferents from cells in the contralateral nuclei of the lateral lemniscus. The intermediate nucleus of the lateral lemniscus receives afferents from some cells in the cochlear nucleus and the superior olivary complex. It is unique among the three nuclei of the lateral lemniscus in that it receives a substantial projection from the medial nucleus of the trapezoid body.

Animals↗

HRP study of the organization of auditory afferents ascending to central nucleus of inferior colliculus in cat.

The ascending auditory projections to central nucleus of inferior colliculus and its ventrolateral and dorsomedial subdivisions (ICVL and ICDM) have been studied in cat using both pressure and electrophoretic injections of horseradish peroxidase (HRP). The results indicate that the predominant ascending projections to inferior colliculus originate in (1) contralateral cochlear nucleus, (2) contralateral and ipsilateral lateral superior olive, (3) ipsilateral medial superior olive, (4) ipsilateral ventral nucleus of the lateral lemniscus, (5) ipsilateral and contralateral dorsal nucleus of the lateral lemniscus, and (6) contralateral inferior colliculus. In addition, ipsilateral cochlear nucleus, ipsilateral and contralateral intermediate nucleus of the lateral lemniscus, ipsilateral, and to a lesser extent contralateral, periolivary nuclei project to inferior colliculus. Of these nuclei, the lateral superior olive projects exclusively to ICVL and ipsilateral cochlear nucleus and contralateral inferior colliculus project mostly, if not exclusively, to ICDM. Many of these projections demonstrate a cochleotopic organization and frequency a nucleotopic organization as well. A cochleotopic organization of the projections is apparent for cochlear nucleus and superior olivary complex. A nucleotopic organization suggests that the heaviest terminations of contralateral inferior colliculus are medial and dorsal in inferior colliculus, of medial superior olive are dorsal and lateral, of superior olivary complex are rostral, of cochlear nucleus are caudal, and of ventral nucleus of the lateral lemniscus are caudal.

Animals↗

Accessory abducens nucleus and its relationship to the accessory facial and posterior trigeminal nuclei in cat.

Retrograde transport of HRP by the abducens nerve results in the labelling of its principal nucleus and, in addition, a second nucleus about 2.5 mm ventrolateral to the principal nucleus. The presence of this second or accessory nucleus of the abducens in a mammal confirms the observations of several Nineteenth Century anatomists and rebuts the conclusions of more recent investigators who argued that the nucleus was allied instead to the facial or trigeminal nerves. The same HRP technique applied to the facial or trigeminal nerves shows that the accessory nucleus of the abducens is in the same parasagittal plane as the accessory nucleus of the facial nerve and the most caudal cells of the motor trigeminal nucleus. The accessory abducens and accessory facial nuclei fall in a ventrocaudal to dorsorostral line between the principal nucleus of the facial and the motor nucleus of the trigeminal with the accessory abducens just caudal and ventral to the accessory facial.

Abducens Nerve↗