R.B. Masterton

The Role of the Corticospinal Tract in the Evolution of Human Digital Dexterity

A morphometric analysis of the corticospinal tracts relation to digital dexterity was performed on 21 species theoretically related to mans 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.A morphometric analysis of the corticospinal tracts relation to digital dexterity was performed on 21 species theoretically related to mans 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.

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 animals 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.

Comparative Morphometry of Mammalian Central Auditory Systems: Variation in Nuclei and Form of the Ascending System

The volumes of the ten largest subcortical auditory nuclei were measured individually in a sample of 53 mammals, including 16 Australian and four American marsupials. The nuclear sizes relative to the total of subcortical auditory tissue were normalized and then analyzed individually for statistically reliable deviations. The overall form of the entire system of ten nuclei and two nuclear subsystems (cochlear nuclei, superior olives) were also analyzed for similarities and notable deviations among the animals. The results show that the absolute size of the auditory system varies more than 139-fold among the 53 mammals (with moles the smallest and humans the largest). Log auditory system volume and log brain weight are closely correlated (r = 0.903, p <0.0001). Bats, kangaroo rats, marmosa opossums, and Norway rats have the largest auditory systems relative to their brain size, while humans have the smallest by far. The other primates also have auditory system/brain size ratios smaller than the sample average, suggesting that the condition in humans is one result of an expansion of non-auditory brain parts rather than a reduction of the auditory system over geological time. The relative sizes of the ten nuclei are well ordered, with the inferior colliculus the largest nucleus by far and medial superior olive the smallest. Because the size of the superior olives, collectively, is reliably related to the size of anteroventral cochlear nucleus (r = 0.744, p <0.001), and not to the size of dorsal cochlear nucleus, the interconnectivity of the subcortical auditory system is probably a factor in the size of the nuclei. In its overall form, the subcortical auditory system is highly similar among mammals, with an average correlation across nuclei of 0.923. This high value means that the overall form of the system has been relatively stable over geological time. The animals with least deviation from the average form are ring-tailed possums, bandicoots, and yellow-bellied gliders, all marsupials. Those with the most unusual forms are mice, bats, and kangaroo rats, all placentals.

Role of acoustic striae in hearing: Reflexive responses to elevated sound-sources

This report is the fourth in a series describing the results of ablation-behavior experiments directed to the ascending output of the cochlear nuclei as it is conducted centrally within the acoustic striae. This fourth report focuses on the unique physiology of the fusiform or output cells of the dorsal cochlear nucleus whose axons course through the dorsal acoustic stria (DAS). Because electrophysiological studies have shown that the cues for sensing the elevation of a sound source would seem to be best analyzed by the dorsal cochlear nucleus and projected centrally via its DAS, we tested normal cats and cats deprived of DAS for their ability to orient to elevated sources of broad-band noise. For behavioral testing, we made use of reflexive or unconditioned orienting responses to elevated sound sources using a similar method to one we have used previously for azimuth testing (Thompson GC, Masterton RB. Brainstem auditory pathways involved in reflexive head orientation to sound. J Neurophysiol 1978;41:1183-1202). The results show that cats deprived of their DAS do indeed have a marked deficit in their ability to orient to an elevated sound source. Further behavioral testing indicated that this deficit is not the secondary result of an attentional or peripheral motor deficit. Although the present results do not prove that the reflexive deficit is strictly auditory in nature, the deficit is notable in that it is the only one yet known to result from a lesion of the dorsal cochlear nucleus or its central projections.

Role of acoustic striae in hearing: discrimination of sound-source elevation

After years of systematic experimentation, we finally uncovered one thing the dorsal system contributes to hearing which the ventral system may not -- the mechanism for orienting to an elevated sound source [Sutherland, D.P., Masterton, R.B., Glendenning, K.K. (1998) Behav. Brain Res. in press]. This paper follows up this one positive result on a historical background of uniformly negative results. The focus of this report is on the fusiform cells of the dorsal cochlear nucleus whose axons course through the dorsal acoustic stria (DAS). Because electrophysiological studies have shown that the cues for sensing the elevation of a sound source would seem to be best analyzed by the dorsal cochlear nucleus, we tested, behaviorally, normal cats and cats deprived of their DAS or intermediate acoustic stria, bilaterally or ipsilaterally (with or without their contralateral ear deafened), for their ability to orient to elevated sources of broad-band noise. For behavioral testing, we made use of a conventional shock-avoidance procedure. The results lead to the conclusion that DCN and DAS may play no role in learned elevation discriminations. This result builds on that of another of our papers which suggests that a deficit in reflexive discrimination of elevation is strictly auditory in nature [Sutherland, D.P., Masterton, R.B., Glendenning, K.K. (1998) Behav. Brain Res. in press].

Auditory Cortex of the Long-Eared Hedgehog (Hemiechinus auritus)

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.

Origins of Anthropoid Intelligence

The development of the extrastriate visual system relative to the striate system was estimated indirectly by measuring the volumes of the lateral posteriorpulvinar complex and lateral geniculate nucleus in six varieties of mammals selected on the basis of their propinquity with Anthropoidea [oppossums, hedgehogs, rats, squirrels, tree shrews and bushbabies]. The same animals were tested on two related behavioral tasks [spatial and visual reversal learning] whose successful achievement requires a simple sort of abstraction. The results show that the ability to learn visual reversal, but not spatial reversal, corresponds closely to the relative degree of development of the extrastriate system. Since the variation in both these behavioral and morphological characteristics also parallels the phylogenetic dimension, the recency of common ancestry to anthropoids, the evolutionary origin of the anthropoid capacity for visual abstraction is suggested.

Anatomical-Behavioral Analyses of Hindbrain Sound Localization Mechanisms

The representation of visual and somesthetic sensory hemifields on the contralateral side of the nervous system is an axiom of neurology. In sharp contrast to these rather strict contralateral representations, however, it is usually held that the representation of space in the central auditory system is bilateral. That is, stimulation of one ear alone, or stimulation by a sound source located in one hemifield, evokes activity on both sides of the brain. The bilaterality of this evoked activity is easily deducible anatomically and clearly demonstrable electrophysiologically (e.g., Held, 1893; Stotler, 1953; Rosenzweig, 1954; and see review by Brugge and Geisler, 1978). Recently, it has also become possible to visualize its distribution by means of the radioactively-labeled 2-deoxyglucose (2-DG) technique for marking neural tissue of high metabolic activity (Sokoloff et al., 1977).

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 hedgehogs 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.

Inter- and Intra-Laminar Distribution of Tectospinal Neurons in 23 Mammals (Part 2 of 2)

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 descri