Robert M. Benjamin

Projection of taste nerve afferents to anterior opercular- insular cortex in squirrel monkey (Saimiri sciureus)

Abstract Cortex buried within the sylvian fissure of deeply anesthetized squirrel monkeys was probed with steel microelectrodes to record slow wave responses evoked by electrical stimulation of the three nerves innervating the tongue. A responsive locus was located in the most anterior opercular-insular cortex. Only stimulation of the two ipsilateral taste nerves (the chorda tympani and the lingual-tonsilar branch of the glossopharyngeal) was effective. Electrical stimulation of the contralateral taste nerves, the contra- and ipsilateral lingual nerves and mechanical stimulation of the tongue evoked no responses in this region. Ablation of the responsive region did not cause any retrograde degeneration of the thalamic taste relay in the ventromedial nuclear complex. If the other taste nerve projection areas located in somatic sensory area I were included in the lesion, complete degeneration of thalamic taste neurons resulted. It was concluded that the taste system has only sustaining projections to the neocortex.

Differential effects of cortical lesions in infant and adult cats on roughness discrimination.

Clinical evidence indicates that central neural damage occurring in infancy does not produce as severe behavioral impairment as equivalent injury in the adult. Kennards experimental studies on the primate motor cortex support this conclusion (4, 5, 6). The present study demonstrates an analogous phenomenon in the somatic sensory system. The behavioral effects of ablation of somatic sensory areas I and II in newborn cats were compared with results of equivalent lesions inflicted on mature animals. Six months after operation these two groups of animals with lesions and matching normal control groups were trained on four stages of roughness discrimination of progressing difficulty: (a) very rough versus smooth; (b) various degrees of roughness versus smooth; (c) very rough versus least rough; (d) various degrees of roughness versus three standard grades of roughness. With one exception, all animals operated at maturity were unable to learn even the simplest (very rough versus smooth) discrimination. By contrast, all animals operated in infancy were indistinguishable from normal on all but the most difficult tasks. The differential results could not be attributed to differences in extent of lesions or age at testing and must be related to some normal characteristic of the nervous system which changes in ontogeny.

Cortical projections of the thalamic mediodorsal nucleus in the rabbit.

The cortical projection of the thalamic mediodorsal nuclear complex (MD) in the rabbit was mapped retrograde horseradish peroxidase and anterograde tritiated proline techniques. The projection field occupied the entire medial wall rostral to a mid corpus callosal level, wrapped around the frontal pole onto the lateral convexity and tailed off caudally on the dorsal bank of the rhinal sulcus. The projection of the lateral approximately one-half of MD, the half which does not receive olfactory input, was confined to medial cortex supply all but the most rostral region. This projection field of lateral MD was precisely organized in two dimensions with the most lateral part projecting most caudally and the most dorsal part projecting most ventrally. A representation for the third, anterior-posterior (A-P), dimension was not evident since any cortical point within the field was supplied by a cylinder of cells extending the entire A-P extent of lateral MD. The medial half of MD, which does receive olfactory input, projected to the remaining rostral medical cortex, the lateral convexity and rhinal sulcal region. The inverse dorsoventral relationship was partially preserved and on overlapping A-P gradient was present with sulcal projections originating more caudally in medial MD and the rostral medial projection originating more rostrally.

Central Projections of the Gustatory System

The central gustatory pathways will be discussed in a progression, beginning with the first order terminations in the medulla oblongata, through the second order relay in the thalamus, and to the terminal projections in the cerebral cortex. The analysis of these central projections will be confined to the rat, cat, and primate. In each section consideration is first given to studies related to the localization of the gustatory projections and then, where data is available, to the characteristics of single and multiunit taste responses to adequate stimulation. An attempt has been made to maintain the historical transition of ideas within each section. Finally, some of the particular methodological problems associated with the gustatory system are outlined.

Unit discharges in the mediodorsal nucleus of the squirrel monkey evoked by electrical stimulation of the olfactory bulb

Summary The thalamic mediodorsal nucleus (MD) of the squirrel monkey was explored with microelectrodes for units responsive to electrical stimulation of the olfactory bulb. All responsive units were localized throughout the magnocellular subdivision of MD, most (88%) ipsilateral to the stimulated bulb. Other parts of MD were unresponsive. Latencies to the first poststimulus spike ranged from 4 to 50 msec with a median value of 14 msec. In preparations with both frontal poles ablated eliminating the possibility of stimulus spread to orbitofrontal cortical neurons and subsequent anti- or orthodromic activation of Mc cells, the shortest response latency was 6 msec. Thus relatively direct and extensive connections exist between the olfactory bulb and one cytoarchitectonic subdivision of this prominent ‘association’ nucleus in a microsmatic primate.

Projection of tongue nerve afferents to somatic sensory area I in squirrel monkey (Saimiri sciureus).

Abstract The distribution of surface positive cortical potentials evoked by electrical stimulation of the three nerves innervating the tongue was mapped in deeply anesthetized squirrel monkeys. All projections were bilateral. In terms of extent of cortex activated, and the amplitude and latency of responses, the major projection of the two taste nerves (the chorda tympani and the lingual-tonsilar branch of the glossopharyngeal) was ipsilateral. The lingual nerve projections were bilaterally more symmetrical, but the shortest latencies were generated by contralateral stimulation. These laterality relationships were also found at the thalamic relay. All responses described in this report were confined to the appropriate part of the somatotopic pattern of somatic sensory area I, in the ipsi- and bilateral tactile representation of the intraoral structures. Complete bilateral ablation of the tongue nerve projection areas did not impair taste discrimination and did not cause retrograde degeneration of thalamic taste neurons. A subsequent study revealed a second taste nerve projection on opercular-insular cortex which, if included in the lesion, did result in complete degeneration of the thalamic taste relay. It was concluded that the taste system has only sustaining projections to S I of the squirrel monkey.

Thalamic neurons responsive to temperature changes of glabrous hand and foot skin in squirrel monkey.

Abstract Extracellular discharges were recorded from single neurons located in the ventrobasal thalamus of anesthetized squirrel monkeys. Units with receptive fields on glabrous skin of hand and foot were studied. Only one type of neuron was found that responded to temperature change. These units also responded to mechanical stimuli (T + M units). This finding contrasted with a previous investigation of tongue thalamic thermal projections where units specifically responsive to thermal stimuli were seen in addition to T + M units. This difference was discussed. The neurons were located in the appropriate somatotopic region of VB external intermingled with specific mechanoreceptive neurons. Spinal cord lesions indicated that no sensitive thermal afferents reached the dorsal thalamus via the dorsal columns but probably project via the contralateral spinothalamic system. Response characteristics were analyzed with respect to rapid temperature change. All T + M units responded to cooling with increased discharge rates. No increased rates were seen with warming. It was also determined that the magnitude of the rise in discharge rate to cooling was generally proportional to the degree of cooling.

Unit discharges in the mediodorsal nucleus of the rabbit evoked by electrical stimulation of the olfactory bulb

Summary The mediodorsal nucleus of the thalamus (MD) in rabbits was explored with microelectrodes during electrical stimulation of the olfactory bulb and tract. In agreement with previous results in the squirrel monkey, unit responses were located within the medial half of MD. Response patterns included early discharges with latencies of 50 msec or less, late discharges with latencies of more than 100 msec, or dual early and late responses. The interval between early and late responses was characteristically a silent period even in units with spontaneous activity. Units which responded at an early latency were more commonly seen than those which showed only a late response. Latencies to first spike within the former group ranged from 15 to 50 msec (median = 36 msec) when the rostral olfactory bulb was stimulated and from 8 to 36 msec (median = 20m sec) when the stimulating electrode was in the rostral retrobulbar area adjacent to the lateral olfactory tract. Major features of response showed some parallels with results obtained both in the squirrel monkey MD and in the cat prepyriform cortex, a structure reported to have direct anatomical connections with the medial portion of MD.

An autoradiographic study of subcortical forebrain projections from mediodorsal and adjacent midline thalamic nuclei in the rabbit

Abstract Conclusions from lesion studies on the subcortical efferent connections of the thalamic mediodorsal nucleus have been varied and conflicting. In this autoradiographic study, tritiated proline was injected into the mediodorsal nucleus and adjacent midline nuclear areas (intermediodorsal nucleus and paraventricular nucleus of the thalamus) of 18 rabbits. Terminal labeling from injections that included parts of the paraventricular nucleus was seen in the following ipsilateral areas: central amygdaloid nucleus, lateral septum, a restricted portion of the nucleus of the stria terminalis, entorhinal cortex and the entire extent of the medial (periventricular) hypothalamus. Injections that encroached into the intermediodorsal nucleus produced ipsilateral labeling in most of the nucleus accumbens, layers II and III of the olfactory tubercle, the magnocellular portion of the posterolateral basal amygdaloid nucleus and the caudate nucleus. Injections restricted to the mediodorsal nucleus produced labeling only in the ipsilateral caudate nucleus. It is concluded that medial portions of the mediodorsal nucleus only project to the caudate nucleus; whereas the midline nuclei project to the other eight subcortical areas in addition to the caudate nucleus. By attributing to the midline nuclei many of the projections previously associated with the mediodorsal nucleus, many discrepancies from earlier reports can be explained by lesion of fibers of passage. Efferent functional relationships of the mediodorsal nucleus with subcortical centers may be established through the caudate projections or projections to other thalamic structures, such as the adjacent midline nuclei.

The distribution of olfactory input in the opossum mediodorsal nucleus.

Discharges of single cells in the thalamic mediodorsal nucleus (MD) of the opossum were recorded during electrical stimulation of the lateral olfactory tract. Responsive sites were histologically localized throughout the entire mediolateral extent of MD. In both rabbit and squirrel monkey responses are confined to the medial half of MD. Thus the lateral non-olfactory nuclear subdivision, common to both rabbit and squirrel monkey, was not found in the opossum. Firing patterns of cells were similar to those observed in rabbit and squirrel monkey. They commonly consisted of an early spike or burst of spikes, followed by a period of inactivity and then, in many cells, by a later period of response or of resumed spontaneous activity. The results indicate that olfactory input is characteristic of MD in a diverse sample of mammals but that topographic organization of the input is distinctly different in the opossum.