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A new technique is described that may demonstrate two-stage connection at the light microscopic level. Anterograde transneuronal transport of [3H]uridine is used in conjunction with retrograde transport of horseradish peroxidase (HRP). The two compounds are injected separately into different brain regions. Under conditions of proper controls, neuron somata that are double labelled are interpreted as receiving an afferent projection from the region injected with [3H]uridine and sending an efferent projection to the region injected with HRP. Thus, the technique can demonstrate two-stage connections in the nervous system.

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The subcortical afferents and cortical projections of the lateral dorsal nucleus of the thalamus were investigated using anterograde and retrograde axonal transport of horseradish peroxidase (HRP). The lateral dorsal nucleus receives afferent projections from several nuclei of the pretectal complex, and sends efferent projections to several subdivisions of limbic cortex. These connections constitute a two stage pathway that could convey visual and somatosensory information to the limbic system.

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Some brainstem and neocortical neurons projecting to the external nucleus of the inferior colliculus were identified by retrograde axonal transport of horseradish peroxidase (HRP). Large pressure injections of HRP were used to define the population of cells in the dorsal column and trigeminal nuclei projecting to the entire inferior colliculus. Subsequently, tiny injections of HRP were delivered electrophoretically to various parts of the external nucleus using micropipettes. In each case the electrophoretic placements were made in sites identified as somatic by their response to foot shock or manual stimulation of the body. Receptive fields were found to be large and almost always bilaterally symmetric. Areas excitable by stimulation of the upper body were often found adjacent to areas excitable by stimulation of the lower body, tail, or, rarely, the face and head. In general, sites in the external nucleus which were identified by their responsiveness to stimulation of the body were not responsive to click stimuli. No topographic representation of the body was evident. After small electrophoretic injections of HRP absolutely restricted to the external nucleus, HRP-filled neurons were found bilaterally in the nucleus gracilis, nucleus Bischoff, (the midline and tail representation of the dorsal column nuclei), nucleus cuneatus, and nucleus trigeminalis, subnucleus caudalis. Ipsilateral neocortical cellular filling was found primarily in a continuous strip along the caudal and inferior margin of the parietotemporal cortex, in the area corresponding to SMII (Pubols, '77). Rarely, filled cells were found in the parietal area corresponding to SMI and in the temporal pole. In sum, small somatic-activated loci of the external nucleus receive bilateral, topographically convergent projections from hindbrain somatosensory structures and from the SMII cortex.

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Following lesions of the dorsal column nuclei, spinal cord and sensorimotor cortex, anterograde degeneration was traced to a common target in the central midbrain; the intercollicular terminal zone. Although not all the midbrain projections of the three pathways are contained within this zone, it receives overlapping projections from each of the three body-related somesthetic pathways studied. The intercollicular terminal zone covers the entirety of the external nucleus of the inferior colliculus and the intercollicular nucleus of Mehler, spilling over into adjacent parts of the central gray and deep layers of the superior colliculus. Little evidence of somatotopy in the somesthetic projections was disclosed, and bilateral input was found in each experimental case, regardless of the type of lesion. Golgi-stained material was examined to explore the basis of the extensiveness of the terminal zone. These materials showed that the dendritic spread of neurons in the external nucleus of the inferior colliculus and the intercollicular nucleus, taken together, covers the entirety of the intercollicular terminal zone. That is, the dendrites invade the same portions of the central gray and deep layers of the superior colliculus which are covered by the terminal field. We conclude that a tripartite division of the sensory midbrain may be justified: with the somesthetic modality being represented anatomically in a fashion at least roughly analogous to that of vision and audition.

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Four varieties of mammals whose medial superior olives range from large to none at all were tested for their ability to localize single, brief tone pips at various frequencies. Although each animal could localize high-frequency tone pips, their ability to localize middle- and low-frequency tone pips corresponded to the size of their medial superior olive (MSO). Since this latter range of frequencies is the one in which binaural phase-difference cues predominate, this anatomical-behavioral correspondence supports the idea that MSO is the chief binaural time-analyzing center for sound localization.

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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.

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