Pallidal and entopeduncular intracellular responses to striatal, cortical, thalamic, and sensory inputs

Intracellular recordings were made from pallidal and entopeduncular neurons in cats. Responses were evoked by direct brain stimulation and auditory and somatosensory stimuli. Brain sites stimulated were caudate nucleus, the precruciate area of the cerebral cortex, and the central median-parafascicular region of the thalamus. The predominant synaptic response pattern for all types of stimulation was an EPSP-IPSP sequence. Thirty percent of the responses were IPSPs only. Relatively few “pure” EPSPs were recorded. These patterns of synaptic responses were compared with those evoked by comparable stimuli to caudate neurons. In particular, the relatively high percentage of “pure” IPSPs in pallidal and entopeduncular cells contrasted with the rate occurrence of “pure” IPSPs in caudate neurons. This difference in incidence of response types may be attributed to anatomical differences in the fine structure of these nuclei.     

Caudate intracellular response to thalamic and cortical inputs

Intracellular recordings of cat caudate neuronal responses evoked by stimulation of the cerebral cortex or of a number of thalamic sites were made. The predominant response was an EPSP-IPSP sequence. A higher percentage of “pure” EPSPs were recorded from the stimulation of centromedian-parafascicular region than from stimulation of other thalamic sites. The outcomes of these experiments were generally in agreement with recent reports concerning the fine structure of the caudate nucleus. The combined anatomical and physiological data suggest that the great majority of striatal input fibers are excitatory and the majority of interneurons are inhibitory in their synaptic effects.     

Projection from the external pallidum to the reticular thalamic nucleus in the squirrel monkey

Small injections of biocytin in the external segment of the pallidum (GPe) of the squirrel monkey (Saimiri sciureus) led to anterograde labeling of fibers in the thalamic reticular nucleus (NRT). These fibers reached NRT by coursing along the ventral tip of the internal capsule or by directly piercing the internal capsule more dorsally. They arborized profusely within the entire rostrocaudal extent of the nucleus. Within NRT, biocytin-labeled fibers were long, slightly varicosed, and emitted numerous short collaterals whose terminal portions consisted of clusters of large varicosities. Some of these varicosities were closely apposed to cell bodies and proximal dendrites of NRT neurons. Small injections of wheat germ-agglutinated horseradish peroxidase in the rostral pole of NRT led to retrograde cell labeling within the entire rostrocaudal extent of GPe. These retrogradely-labeled cells did not display immunoreactivity for choline acetyltransferase. Hence, beside the well-established projection from the internal pallidum to the thalamus, our findings support the existence of another pallidothalamic projection whereby GPe neurons could exert a powerful influence upon the thalamocortical neurons via a relay in NRT.     

Vestibular-nerve inputs to the vestibulo-ocular reflex: a functional-ablation study in the squirrel monkey

Advantage was taken of differences in the electrical excitability of vestibular-nerve fibers to characterize the afferent input to the canal-related vestibulo-ocular reflex. Large anodal (inhibitory) currents, when delivered to both ears, result in a selective, reversible ablation of irregular afferents. Their background discharge and responses to head rotations are temporarily abolished. The same currents have less effect on the background discharge and no effect on the rotational sensitivity of regular afferents. Eye movements were evoked by head rotations in alert monkeys. The ablating currents did not alter the ocular responses to sinusoidal head rotations in yaw or pitch planes. Responses to rapid changes in head velocity were similarly unaffected. It is concluded that irregular afferents do not make a net contribution to the reflex. Slow-phase eye movements evoked by unilateral galvanic currents are consistent with this conclusion. The results are incorporated into a systems model of the reflex. There are three conclusions from the model: (1) the signal to motoneurons consists of the sum of three components related, respectively, to head velocity, eye position, and filtered eye velocity; (2) regular afferents provide the best match to the dynamic requirements of the reflex; and (3) the central pathways responsible for all three signal components receive regular inputs.     

Spinal and cortical inhibition of intestinal motility in the squirrel monkey

Cortical control over intestinal motility was examined by stimulating the cerebral cortex and recording subsequent changes in gut volume in the chloralose-anesthetized squirrel monkey. Also, correlations were made between the cortical areas effecting changes in gut motility and those receiving sensory input from the bowel, by recording evoked potentials from the same areas following stimulation of the splanchnic nerve. It was found that: (a) intestinal motility is inhibited by stimulation of frontal polysensory cortex; (b) such inhibition does not occur following stimulation of primary sensory motor cortex; (c) visceral afferents carried in the splanchnic nerve converge with somatic inputs on the same frontal cortical area controlling gut motility; (d) the cortical control may act, at least in part, by modulation of the intestino-intestinal inhibitory reflex (I₃-R); and (e) the I₃-R in the squirrel monkey is similar to that previously described in carnivores.     

Lamination and differential distribution of thalamic afferents within the sensory-motor cortex of the squirrel monkey

The structure of the first somatic sensory area (areas 3,1 and 2), of the motor area (area 4) and the intervening transitional field (area 3a) is described in the squirrel monkey (Saimiri sciureus) using Nissl, Bodian, Weil and Golgi preparations. The laminar arrangement of both cells and axons is briefly described and this is correlated with the Nauta and autoradiographic techniques. The latter method was used particularly in order to assess quantitative differences in the density of thalamic projections to the five cytoarchitectonic fields. In the somatic sensory areas thalamic afferents terminate not only in layer IV but to a large extent also in a recognizable part of layer III (layer IIIb). In area 4 thalamic terminals fill much of layer III, reaching almost to layer II. In area 3a the extent is intermediate between that seen in areas 3 and 4. It is thought that the extensive spread of thalamic terminals is related to the elongated form of a particular class of spine-bearing cell whose somata are situated in layer IV (Jones, 1975). In all areas a small proportion of thalamic afferents end also in layer I. Evidence is presented to indicate that specific afferent fibers emanating from the ventrobasal and ventrolateral complexes of the thalamus terminate in both the deep and superficial parts of layer I While “non-specific” afferents from other thalamic sources end in the superficial part. The autoradiographic studies indicate that there are considerable differences between the number of thalamic afferents ending in area 3 on the hand and in areas 1 and 2 on the other. Given this and the nature of the degenerating thalamic afferents observed in Nauta preparations, it is possible to identify thalamic afferents in normal Golgi preparations and significant differences are detectable in areas 4, 3 and 1 and 2. It is yet uncertain whether the slightly thinner, more sparsely distributed thalamic afferents ending in areas 1 and 2 are branches of those directed primarily to area 3.     

Long-term potentiation in freely moving rats reveals asymmetries in thalamic and cortical inputs to the lateral amygdala

Long-term memory underlying Pavlovian fear conditioning is believed to involve plasticity at sensory input synapses in the lateral nucleus of the amygdala (LA). A useful physiological model for studying synaptic plasticity is long-term potentiation (LTP). LTP in the LA has been studied only in vitro or in anaesthetized rats. Here, we tested whether LTP can be induced in auditory input pathways to the LA in awake rats, and if so, whether it persists over days. In chronically implanted rats, extracellular field potentials evoked in the LA by stimulation of the auditory thalamus and the auditory association cortex, using test simulations and input/output (I/O) curves, were compared in the same animals after tetanization of either pathway alone or after combined tetanization. For both pathways, LTP was input-specific and long lasting. LTP at cortical inputs exhibited the largest change at early time points (24 h) but faded within 3 days. In contrast, LTP at thalamic inputs, though smaller initially than cortical LTP, remained stable until at least 6 days. Comparisons of I/O curves indicated that the two pathways may rely on different mechanisms for the maintenance of LTP and may benefit differently from their coactivation. This is the first report of LTP at sensory inputs to the LA in awake animals. The results reveal important characteristics of synaptic plasticity in neuronal circuits of fear memory that could not have been revealed with in vitro preparations, and suggest a differential role of thalamic and cortical auditory afferents in long-term memory of fear conditioning.     

Viscerosomatic interactions in the thalamic ventral posterolateral nucleus (VPL) of the squirrel monkey

In anesthetized squirrel monkeys single cell recordings were performed using tungsten microelectrodes. The responses of 29 viscerosomatoceptive and somatoceptive VPL neurons to noxious distension of the urinary bladder, the lower esophagus and the distal colon and to innocuous and noxious somatic stimuli were assessed when these stimuli were presented separately or together. Neuronal responses were defined as additive or interactive depending on the relative changes in responses to individual somatic or visceral stimuli, and on their responses during conditioning (somatic and visceral stimuli applied concurrently). In 13 neurons interactions between the somatosensory and visceral inputs could be demonstrated. The dominant interactive effect was inhibition, although facilitatory effects were seen as well (2 of 13). The magnitude or direction of the interactions seemed independent of the location of the somatic and visceral receptive fields. The mean population response of the neurons showing interactions was 4.66 spikes/s to somatic stimulation, and 0.07 spikes/s to visceral stimulation. During conditioning the mean interactive effect was −62% of the calculated additive effect. This implies that overall the somatic responses are halved during a coincident visceral stimulus. In a subgroup of the VPL neurons, which were classified as pure somatic responsive (n=14) due to their unresponsiveness during visceral stimulation alone, a third (n=5) still exhibited visceral convergence during conditioning. The latter neurons, therefore, receive visceral inputs, which function in a purely interactive (modulatory) manner. It is concluded that part of the described effects is due to competition (cross modality suppression) between the visceral and somatic inputs. We further conclude that the suppression of somatic information by noxious visceral stimuli may contribute to a more effective processing of the discriminatory aspects of nociceptive visceral information previously demonstrated in VPL.     

Origin of brain stem and temporal cortical afferent fibers to the septal region in the squirrel monkey

The origins of the brain stem and temporal cortical projections to the septal region in the squirrel monkey were investigated with the horseradish peroxidase (HRP) retrograde axonal transport technique. After HRP injections placed into the septal region, labeled cells were observed in brain stem sites which generally correspond to regions which are associated with known monoamine cell groups previously identified in the primate. These structures include the nucleus locus ceruleus, dorsal tegmental nucleus of Gudden, nucleus reticularis tegmenti pontis, nucleus annularis, ventral tegmental region, and the medial aspect of the lateral hypothalamus. Temporal cortical efferent fibers to the septal region arise principally from layers II and III of the perirhinal region, suggesting the presence of a second-order olfactory innervation of this structure.     

Maturation of thalamic inputs into the associative cortical areas during postnatal ontogenesis in cats

Thalamic afferents into the sensorimotor and parietal cortex (area 7) were studied using the method of retrograde axonal transport of horseradish peroxidase (HRP) in kittens of three age groups. Following HRP injection into the sensorimotor cortex of 1- to 3-day-old kittens, labeled cells were found in the following nuclei: ventral posterolateral (VPL), ventral posteromedial (VPM), medialis dorsalis (MD), centrum medianum (CM), ventral posteromedial (VPM), medialis dorsalis (MD), centrum medianum (CM), and centralis lateralis (CL). In 9- to 10-day-old kittens the number of labeled cells and density of reaction product within the cells was found to increse markedly. In 21- to 30-day-old kittens, besides the above-mentioned nuclei, labeled cells were also revealed in n. ventralis lateralis (VL). A similar trend was seen following HRP injections into area 7. In 1- to 3-day-old kittens, labeled cells were found in n. lateralis posterior (LP), in n. ventralis anterior (VA), and in Pulvinar (Pulv). Both in the 9-to 10-day-old and the 21- to 30-day-old kittens, labeled cells were also demonstrated in n. lateralis dorsalis (LD) and CL. For both of the cortical areas the number of labeled cells and the density of labeling within the cells increase during postnatal ontogenesis. This may be attributed to the growing number of axon terminals. In general, our results suggest that differences in the thalamic connections of single cortical areas can be distinguished during the postnatal ontogenesis of the brain.     

Organization of visual cortical inputs to the striatum and subsequent outputs to the pallido-nigral complex in the monkey.

To determine the organization of visual inputs and outputs of the striatum, we placed multiple retrograde and anterograde tracers into physiologically identified portions of the striatum known to receive inputs from visual cortex in seven macaques. The injection sites included the tail and genu of the caudate nucleus (14 cases), the head of the caudate (1 case), and the ventral putamen (3 cases). Retrogradely labeled cells were located predominantly in layer 5 of the ipsilateral cortex but were also found in layers 3 and 6. After caudate injections, labeled cells were found both in large, nearly continuous regions of cortex topographically related to the site of the injection, and in several smaller cortical regions that were discontinuous and common to many or all of the injection sites. The continuously labeled regions included nearly all known visual cortical areas, except for the striate cortex. After injections in the rostral tail, the continuously labeled region included the rostral portion of Bonin and Bailey's (Urbana: University of Illinois Press. '47) area TE and adjacent portions of TF, TH, TG, and, occasionally, area 35 (Brodmann, Leipzig: J.A. Barth. '09). After injections into the posterior tail and ventral genu, the labeled region shifted posteriorly in TE and TF, and into TEO and the ventral parts of prestriate areas V4, V3, and (sparsely) V2. As the injection site was advanced into the dorsal genu, the labeled region shifted dorsally toward the parietal lobe, including prestriate areas MT and PO, parietal area PG (Brodmann's area 7), the ventral and lateral intraparietal sulcal areas (VIP and LIP, respectively), and area PE and adjacent area LC (Brodmann's areas 5 and 23, respectively). The discontinuous areas labeled by many different injections included the principal sulcus/frontal eye field region, the anterior cingulate cortex, and the superior temporal polysensory area. Thus, whereas temporal, occipital, and parietal visual cortical areas project into the caudate largely according to proximity, certain multimodal cortical areas seem to have a much wider projection. To determine whether visual cortical areas have additional projections to the caudate beyond the territory of our retrograde injection sites in the tail and genu. 3H-labeled amino acids were injected into areas TE, V4, and MT in three additional monkeys. The topographic location of label in the tail and genu of the caudate in these cases was consistent with the results from injections of retrograde tracers into the caudate.(ABSTRACT TRUNCATED AT 400 WORDS)     

Converging visual and somatic sensory cortical input to the intraparietal sulcus of the rhesus monkey

A cyto- and myeloarchitectonic study reveals the presence of a distinct cortical zone ("area POa") in the lower bank of the intraparietal sulcus of the rhesus monkey. Using both autoradiographic and silver impregnation techniques, an analysis of cortical connections shows two overlapping projections to this sulcal zone. These come from (1) the middle portion of the preoccipital gyrus (area OA) and (2) the rostral inferior parietal lobule (area PF).     

Columnar aggregation of prefrontal and anterior cingulate cortical cells projecting to the thalamic mediodorsal nucleus in the monkey

The columnar arrangement of the prefrontal and anterior cingulate cortex cells that project to the thalamic mediodorsal (MD) nucleus in rhesus and Formosan monkeys was studied by injecting horseradish peroxidase into the MD nucleus. Labelled cells appeared ipsilaterally in layers V and VI in the dorsolateral, medial, and orbital prefrontal cortex, and in layer VI in the anterior cingulate cortex. Labelled cells were aligned in the radially oriented cords of neurons and grouped into clusters, 25-200 microns wide, thus forming columns. Radial cellular cords with no labelled cells were interspersed between the labelled radial cords.     

The organization of hypothalamocerebellar cortical fibers in the squirrel monkey (Saimiri sciureus)

The organization and distribution of hypothalamocerebellar cortical fibers in squirrel monkey were investigated by using horseradish peroxidase (HRP, WGA-HRP) and 3H-leucine as anterograde tracers. Following hypothalamic injections, anterogradely labeled fibers coursed bilaterally through the periventricular gray (ipsilateral preponderance) and into the cerebellar white matter. Sparse numbers of labeled fibers appeared to descend into the reticular formation and enter the cerebellum via the brachium pontis. The pattern of cerebellar cortical labeling does not conform to that of mossy or climbing fibers. Labeled axons enter and branch within the granular layer, proceed around Purkinje cell somata, and enter the molecular layer. Within the latter some labeled fibers branch outwardly in a fanlike manner whereas others ascend before branching. Many fibers within the molecular layer ultimately assume an orientation that is similar to that of parallel fibers. The distribution patterns of hypothalamocerebellar cortical axons resemble those reported for monoaminergic fibers in the cerebellar cortex. Afferent fibers to the cerebellar cortex (including hypothalamocerebellar) that do not terminate as mossy or climbing fibers may collectively constitute a third general category of cerebellar afferent axons. On the basis of their distribution within all cortical layers these fibers are designated as multilayered fibers. The morphology of multilayered fibers stands in contrast to the presumptive mossy fiber labeling seen in lobules IX and X following large injections. Such labeling may represent a subpopulation of hypothalamocerebellar fibers or result from enzyme deposition in areas bordering the hypothalamus that project to cerebellar structures.