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R B Masterton

Publications and source records attributed to R B Masterton.

At least 19 recordsLinked to original sources

Variation and evolution of mammalian corticospinal somata with special reference to primates.

The morphology of the somata originating the corticospinal tract was examined in 24 species of mammals to identify commonalities and major sources of variation among the different species. Horseradish peroxidase was applied to a hemisection of the spinal cord at the C1-C2 junction. After tetramethylbenzidine processing, the labeled somata throughout the cerebral cortex were plotted and counted. Then, 23 morphological characteristics of the corticospinal somata were examined, including their number, size, and density across the cortical surface. The results show that morphological characteristics of corticospinal somata are closely related to an animal's body, brain, and cerebral cortex size. That is, mammals with large neocortical surfaces tend to have larger as well as more corticospinal somata; mammals with large bodies tend to have corticospinal somata that are less densely distributed. Moreover, the probable increase in the ratio of local noncorticospinal somata to corticospinal somata implies that the evolution of the corticospinal tract was accomplished by an increase in "support" or "server" cells as well as an increase in the size of the tract itself. The results also show that several characteristics are reliably related to an animal's taxonomic classification and hence its ancestry. Comparisons among three mammalian lineages indicate that some characteristics may have changed uniquely in the anthropoid primate lineage, and thus, presumably, in the human lineage. The results suggest that if morphological characteristics of the corticospinal tract important in the evolution of the specialized motor abilities in anthropoid primates are sought, then examination of the role of changes in soma diameter, rostral (motor)/caudal (sensory) ratios of density, concentration, surface density, and volume density may be more instructive than examination of the total number of corticospinal neurons alone.

Animals

Hearing in primitive mammals: Monodelphis domestica and Marmosa elegans.

Although opossums of the Family Didelphidae usually serve as a parsimonious starting point for tracing the otological and neurological evolution of modern mammals, audiological data for Didelphid opossums is available only for the North American opossum (Didelphis virginiana) which because of its large size, may be one of the least representative genera of the family. The present report extends the audiological data to two other species of Didelphid opossums, Monodelphis domestica, and Marmosa elegans. At 60 dB SPL, the hearing of Monodelphis extends from 3.6 kHz to 77 kHz, with a range of best sensitivity from 8 to 64 kHz while the hearing of Marmosa extends from 3.8 kHz to 80 kHz, with a range of best sensitivity from 8 to 64 kHz. Neither species was found to be particularly sensitive to tones, with the average lowest threshold near 20 dB SPL for Monodelphis and 33 dB SPL for Marmosa. These results indicate that like the North American opossum both genera are sensitive to high frequencies yet relatively insensitive to sound. Because the hearing of the three genera of Didelphids agree in several respects, it can be concluded that sensitivity to high frequencies almost certainly was present in ancient mammals, probably following quickly after the acquisition of a 3 ossicle middle ear linkage. It is not unlikely that the utility value of high frequency hearing, rather than highly sensitive hearing, may have been a primary source of selective pressure for this morphological transformation.

Acoustic Stimulation

Role of acoustic striae in hearing: mechanism for enhancement of sound detection in cats.

We report the results of behavioral studies in cats conducted first, to demonstrate the presence of a monaural mechanism for the enhancement of signal to noise; and then to examine the necessity or sufficiency of the acoustic striae for this mechanism. The results show that cats do indeed have a monaural mechanism for enhancing the detection of tones in co-located background noise for noise levels at least as high as 60 dB SPL. The ablation-behavior results show that surgical section of the dorsal (DAS) and most of the intermediate (IAS) striae has no measurable effect on this mechanism. In sharp contrast, even partial section of the trapezoid body results in a profound and permanent deficit and this deficit is not accounted for by hearing loss alone. It is concluded that the ascending and descending fibers in the dorsal and intermediate acoustic striae are neither necessary nor sufficient for enhancing the detection of salient sounds in a noisy environment while the ascending or descending fibers in the ventral acoustic stria are sufficient and probably necessary.

Acoustic Stimulation

Inter- and intra-laminar distribution of tectospinal neurons in 23 mammals.

Based on retrograde labeling from the high cervical spinal cord, the inter- and intra-laminar distributions of tectospinal tract (TST) somata within the tectum of 23 mammals and one reptile are described. The results show that TST somata are found only in the intermediate and deep layers. Although more TST somata are usually found in the intermediate layer, there are no useful relationships for predicting the number in one layer given the number in the other. The ratio of numbers of TST somata in the intermediate relative to the deep layer varies widely, from 0:1 (in rabbits) to over 8:1 (in marmosets). Within both layers the majority of TST somata (> 80%) are found in the lateral half of the tectum--the area subversing the lower visual field. In contrast, the variation between temporal and nasal visual fields is adequately accounted for by the animal's 'visual axis'--the azimuth of its field of best vision. In general, the present results uphold the idea that the significance of the TST somata, and perhaps of the tectospinal tract itself, is to be found in directing the head so that the retinal area of best vision can be brought to bear on stimuli either almost outside, or about to pass outside, of the area of best vision. The larger and possibly universal predominance of TST somata subserving the lower visual field suggests that the tectospinal tract may be primarily concerned with adjusting the step dimensions of the forelegs to accommodate obstacles to normal progression.

Animals

Acoustic chiasm V: inhibition and excitation in the ipsilateral and contralateral projections of LSO.

When this series of experiments was begun in 1984, the activity of each lateral superior olive (LSO) in the mammalian hindbrain was known to encode the hemifield of acoustic space containing a sound source. However, the almost random bilaterality of its ascending projections seemed to jumble that identification before reaching the midbrain. At the same time, electrophysiological studies of LSO and its efferent target in the inferior colliculus, along with the strictly contralateral deficits in sound localization resulting from unilateral lesions above the level of the superior olives, indicated that hemifield allegiance was largely maintained (though reversed) at the midbrain. Here we present seven lines of biochemical evidence, some combined with prior ablations, supporting the notion that the anatomical segregation of the ipsilateral and contralateral fibers ascending from the LSO is accompanied by a corresponding segregation of their neurotransmitters: most of the ascending ipsilateral projection is probably glycinergic and, hence, inhibitory in effect, while most of the contralateral projection is probably glutamatergic/aspartergic and, hence, excitatory in effect. Taken together, the inhibitory ipsilateral projections and the excitatory contralateral projections serve to amplify functional contralaterality at the higher levels of the auditory system.

Acoustic Stimulation

Role of the central auditory system in hearing: the new direction.

The mammalian central auditory system contains a large number of subcortical auditory nuclei, which were once thought to form a simple relay system, taking signals from the ear to the cortex where all information processing would have occurred. Now it appears that these subcortical nuclei are themselves responsible for the extraction and analysis of the dimensions of sounds. Not only do the nuclei encode dimensions defining the nature of the sound, but also they extract features of sound location. Three major nuclei in the superior olivary complex of mammals extract the horizontal direction of a sound source, and it seems likely that other nuclei in the auditory system encode elevation and distance. This shift in viewpoint away from the attributes of sound to the attributes of sound sources is an important new step in the investigation of the role of the central auditory system in hearing.

Acoustic Stimulation

Psychoacoustical contribution of each lateral lemniscus.

Although each lateral lemniscus is required for sound localization in its contralateral hemifield, no auditory function is yet known for the neural activity evoked in the lemniscus ipsilateral to a sound source. In an attempt to assess the role played by the ipsilateral lemniscus, monaural cats were tested on an array of psychoacoustical tasks before and after surgical section of one or the other lateral lemniscus. The results show that the lemniscus contralateral to the remaining intact ear is either necessary or sufficient for 24 of the 26 tests administered. However, the lemniscus ipsilateral to the intact ear is both necessary and sufficient (or alternatively, the contralateral lemniscus makes no obvious contribution) to normal thresholds in two of the tasks: detection of low-frequency tones (< 4 kHz) and detection of low-frequency AM modulation. Because of their projections to the ipsilateral inferior colliculus via the ipsilateral lemniscus, the anatomical substrate of these two unusual tasks is probably the fibers from the MSO and possibly, the LSO, ipsilateral to the intact ear.

Acoustic Stimulation

Acoustic chiasm. IV: Eight midbrain decussations of the auditory system in the cat.

Conventional retrograde and orthograde axonal transport tract-tracing techniques were used in cats to explore the auditory decussations and commissures in the upper pons and midbrain. In all, 8 decussations differing either in origin or in contralateral termination were found. Three of the 8 decussations (from the dorsal nucleus of the lateral lemniscus to the contralateral dorsal nucleus of the lateral lemniscus, from the dorsal nucleus of the lateral lemniscus to the contralateral inferior colliculus, from the sagulum to the contralateral sagulum) reach their targets via the commissure of Probst. The remaining 5 decussations (from the inferior colliculus to the contralateral inferior colliculus or medial geniculate, from the intermediate nucleus of the lateral lemniscus to the contralateral medial geniculate, from the sagulum to the contralateral inferior colliculus or medial geniculate) reach their targets via the commissure of the inferior colliculus. The results also suggest that the commissure of Probst is not a general avenue for decussating auditory fibers of the lateral lemniscus but is instead a specific avenue only for fibers from the dorsal nucleus of the lateral lemniscus and sagulum. The results also show that, in the cat at least, the dorsal nucleus of the lateral lemniscus does not project beyond the inferior colliculus to either the superior colliculus or medial geniculate--the cells previously reported as doing so are probably those of the immediate neighbors of the dorsal nucleus, the intermediate nucleus of the lateral lemniscus and sagulum.

Animals

Acoustic chiasm. III: Nature, distribution, and sources of afferents to the lateral superior olive in the cat.

The outcomes of seven experiments are reported, each directed to the nature and sources of the excitation and inhibition impinging on the lateral superior olive (LSO) in cats. In the first experiment, we used conventional 14C 2-DG methods to determine the specificity, precision, and extent of symmetry in the stimulation reaching LSO from the ipsilateral and contralateral ears. In Experiment 2, we sought the presence of GABA and glycine receptors in LSO using conventional, in vitro receptor-binding methods. On the basis of these results, we used in vitro high-affinity uptake methods in Experiment 3 to seek evidence that some of the terminals as well as the receptors in LSO are glycinergic. In Experiment 4, we used immunocytochemical methods to show that the somata known to supply the contralateral projections to LSO, and their terminals in LSO, are each immunoreactive with an antibody directed to a glycine-protein conjugate. In Experiment 5, we made use of a glycinergic neuron's avidity for transporting glycine retrogradely to label the likely sources of the glycinergic terminals in LSO. In Experiment 6, we used immunocytochemical methods to show that the spherical and globular cells of the ventral cochlear nucleus and terminals in LSO and in MTB are glutamatergic and/or aspartergic. In Experiment 7, we used receptor binding methods to determine whether the glutamate/aspartate receptors in LSO are probably of the kainate or of the quisqualate type. The results of the several experiments suggest that probably glutamate-quisqualate synapses mediate LSO's ipsilaterally driven excitatory responses and glycinergic synapses mediate its contralaterally driven inhibitory responses. The two types of input appear to be well matched in LSO's medial and middle limbs with glycinergic terminals mostly perisomatic and glutamatergic terminals mostly peridendritic. However, LSO's low frequency lateral limb appears to be somewhat different; it receives less stimulation from the contralateral ear. Instead, LSO's lateral limb may receive some of its glycinergic input directly from the ipsilateral ventral cochlear nucleus and/or indirectly via the juxtaposed lateral nucleus of the trapezoid body.

Afferent Pathways

Descending pathways to the spinal cord, III: Sites of origin of the corticospinal tract.

The somata of corticospinal neurons were labeled with horseradish peroxidase that had been applied to a hemisection of the spinal cord at the C1-C2 junction in 22 species of mammals. After tetramethylbenzidine processing, with and without counterstaining with cresyl violet or neutral red, the labeled cells in systematic sets of sections throughout the cerebral cortex were plotted and counted. Several morphological features of the corticospinal cells were examined including their cell type, number, density, concentration, laminar distribution, and their distribution across the cortical surface. The results show that the labeled corticospinal neurons were invariably layer V pyramidal cells. However, in many mammals they were found to be stacked one above the other within layer V, sometimes many neurons deep. Despite the concentration of corticospinal neurons within layer V, many unlabeled neurons were also present within the layer throughout the extent of the labeled region. The results also indicate that at least two spatially distinct regions of neocortex originate corticospinal fibers in each of the animals in the sample. In addition to these two regions, a third segregated region is present in the cortex of primates and an apparently different third region is present in the cortex of Glires (Rodentia and Lagomorpha). The third region of corticospinal cortex in primates is located on the lateral surface of the cortex in prosimians and New World monkeys and is buried in the caudal bank of the inferior arcuate sulcus in Old World monkeys. The results also show a predominantly contralateral corticospinal tract in all but 4 of the 22 mammals in the sample. Although these 4 mammals are each members of the order Insectivora, a less modified member of the same order possessed the predominantly contralateral projection of most mammals, hence denying the notion that a predominantly ipsilateral tract is a characteristic of Insectivora.

Animals

Descending pathways to the spinal cord, IV: Some factors related to the amount of cortex devoted to the corticospinal tract.

In the companion paper to this one (Nudo and Masterton: J. Comp. Neurol. 296:559-583, '90), we have presented data indicating that in each of 22 mammals, there are either 2 or 3 separate regions of neocortex contributing corticospinal fibers. In this paper, we describe the variation in the absolute size of these cortical regions, the total amount of neocortex contributing corticospinal fibers (CST cortex), and the total amount of neocortex (total cortex) in each of the animals. We then use strict statistical tests to examine the relationships between these measures and several other quantitative measures or descriptions of the animals' size, ancestral heritage, motor prowess, and ecological adaptation. The results show that the absolute amount of CST cortex is more closely related to the total amount of neocortex than to any other quantitative measure available. The further variation--that is, the variation in the amount of CST cortex relative to total neocortex--appears to have been random over the inferred ancestral lineages of most animals in the sample, but seems to have been almost absent along the anthropoid lineage. Because this constancy in the relative amount of CST cortex over a very long period of anthropoid ancestry is apparently unusual if not unique among mammals, it may contain a clue to the special role of the corticospinal tract among primates. Finally, the distribution of the CST among the 3 cortical regions in primates was found to be more closely related to their particular mode of ecological adaptation than to their particular combination of digital dexterity and hand-eye coordination.

Animals

Auditory cortex of the long-eared hedgehog (Hemiechinus auritus). I. Boundaries and frequency representation.

The boundaries of the primary auditory cortex of the long-eared hedgehog, Hemiechinus auritus, were determined by single-cell recordings, myeloarchitecture and retrograde horseradish peroxidase labeling in the medial geniculate, using anesthetized animals. The auditory cortex is located on the lateral surface of the temporal cortex, medial to the rhinal fissure. Responses to pure tones revealed an orderly representation of best frequencies in the primary auditory cortex, with low frequencies represented rostrally and high frequencies caudally. A second auditory field caudal to the primary one was indicated.

Animals

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