Cerebello-thalamo-cortical projections to the posterior parietal cortex in the macaque monkey

This study reinvestigated the functional neuroanatomy of phonological and visual working memory in humans. Articulatory suppression was used to deprive the human subjects of species-specific verbal strategies in order to make the functional magnetic resonance imaging results more comparable to findings in non-human primates. Both phonological and visual working memory processes activated similar prefronto-parietal networks but were found to be differentially distributed along several cortical structures, in particular along the anterior and posterior parts of the intermediate frontal sulcus. These results suggest that a domain-specific topographical organization of neural working memory mechanisms in the primate brain is conserved in evolution. However, the findings also underline the critical dynamic influence that the additional availability of language may have on working memory processes and their functional implementation in the human brain.     

Thalamo-cortical projections to the posterior parietal cortex in the monkey

Thalamo-cortical projections to the posterior parietal cortex (PPC) were investigated electrophysiologically in the monkey. Cortical field potentials evoked by the thalamic stimulation were recorded with electrodes chronically implanted on the cortical surface and at a 2.0-3.0 mm cortical depth in the PPC. The stimulation of the nucleus lateralis posterior (LP), nucleus ventralis posterior lateralis pars caudalis (VPLc), and nucleus pulvinaris lateralis (Pul.l) and medialis (Pul.m) induced surface-negative, depth-positive potentials in the PPC. The LP and VPLc projected mainly to the superior parietal lobule (SPL) and the anterior bank of the intraparietal sulcus (IPS), and the Pul.m mainly to the inferior parietal lobule (IPL) and the posterior bank of the IPS. The Pul.l had projections to all of the SPL, the IPL and both the banks. The significance of the projections is discussed in connection with motor functions.     

Topographic organization of projections from the amygdala to the visual cortex in the macaque monkey

The topography of amygdaloid projections to the visual cortices in the macaque monkey was examined by injecting the fluorescent tracers Fast Blue and Diamidino Yellow at different locations in the occipital and temporal lobes and mapping the distribution of retrogradely labeled cells in the amygdala. Injections involving regions from rostral area TE to caudal area V1 all resulted in labeled cells within the basal nucleus of the amygdala. Relatively few double-labeled cells were observed even when the two injections were separated by less than 3 mm. The projections were rostrocaudally organized such that projections to caudal visual areas originated from dorsal and caudal portions of the magnocellular division of the basal nucleus while projections to more rostrally situated visual areas originated in more rostral and ventral portions of the basal nucleus. When injections involved rostral and medial portions of area TE, retrogradely labeled cells were observed in the accessory basal and lateral nuclei in addition to the basal nucleus. These data confirm that the amygdala gives rise to feedback projections to all levels of the "ventral stream" visual pathway. The projections do not appear to be diffusely distributed since few double-labeled cells were observed. The largest cells of the basal nucleus, those located in the magnocellular division, project the farthest in the visual system and innervate all occipital and temporal levels. The smaller cells, in the intermediate and parvicellular regions, project to more rostral and medial portions of the visual cortex. These results suggest that the amygdala may have substantial modulatory control over sensory processing at all stages of the ventral-stream visual cortical hierarchy.     

Amygdalospinal projections in the macaque monkey

Injection of horseradish peroxidase into the cervical cord in the macaque monkey led to the retrograde labeling of neurons in the caudal part of the central nucleus of the amygdala ipsilateral to the spinal half where the injection was made. Although the number of labeled neurons in the amygdala was small, they were constantly found in 7 macaque monkeys (3 Japanese monkeys, 3 crab-eating monkeys and 1 rhesus monkey) which were injected with the enzyme into the upper and middle cervical cord segments.     

Neurophysiology of prehension. III. Representation of object features in posterior parietal cortex of the macaque monkey

Neurons in posterior parietal cortex (PPC) may serve both proprioceptive and exteroceptive functions during prehension, signaling hand actions and object properties. To assess these roles, we used digital video recordings to analyze responses of 83 hand-manipulation neurons in area 5 as monkeys grasped and lifted objects that differed in shape (round and rectangular), size (large and small spheres), and location (identical rectangular blocks placed lateral and medial to the shoulder). The task contained seven stages -- approach, contact, grasp, lift, hold, lower, relax -- plus a pretrial interval. The four test objects evoked similar spike trains and mean rate profiles that rose significantly above baseline from approach through lift, with peak activity at contact. Although representation by the spike train of specific hand actions was stronger than distinctions between grasped objects, 34% of these neurons showed statistically significant effects of object properties or hand postures on firing rates. Somatosensory input from the hand played an important role as firing rates diverged most prominently on contact as grasp was secured. The small sphere -- grasped with the most flexed hand posture -- evoked the highest firing rates in 43% of the population. Twenty-one percent distinguished spheres that differed in size and weight, and 14% discriminated spheres from rectangular blocks. Location in the workspace modulated response amplitude as objects placed across the midline evoked higher firing rates than positions lateral to the shoulder. We conclude that area 5 neurons, like those in area AIP, integrate object features, hand actions, and grasp postures during prehension.     

Thalamocortical and the dual pattern of corticothalamic projections of the posterior parietal cortex in macaque monkeys

The corticothalamic projection includes a main, modulatory projection from cortical layer VI terminating with small endings whereas a less numerous, driving projection from layer V forms giant endings. Such dual pattern of corticothalamic projections is well established in rodents and cats for many cortical areas. In non-human primates (monkeys), it has been reported for the primary sensory cortices (A1, V1, S1), the motor and premotor cortical areas and, in the parietal lobe, also for area 7. The present study aimed first at refining the cytoarchitecture parcellation of area 5 into the sub-areas PE and PEa and, second, establishing whether area 5 also exhibits this dual pattern of corticothalamic projection and what is its precise topography. To this aim, the tracer biotinylated dextran amine (BDA) was injected in area PE in one monkey and in area PEa in a second monkey. Area PE sends a major projection terminating with small endings to the thalamic lateral posterior nucleus (LP), ventral posterior lateral nucleus (VPL), medial pulvinar (PuM) and, but fewer, to ventral lateral posterior nucleus, dorsal division (VLpd), central lateral nucleus (CL) and center median nucleus (CM), whereas giant endings formed restricted terminal fields in LP, VPL and PuM. For area PEa, the corticothalamic projection formed by small endings was found mainly in LP, VPL, anterior pulvinar (PuA), lateral pulvinar (PuL), PuM and, to a lesser extent, in ventral posterior inferior nucleus (VPI), CL, mediodorsal nucleus (MD) and CM. Giant endings originating from area PEa formed restricted terminal fields in LP, VPL, PuA, PuM, MD and PuL. Furthermore, the origin of the thalamocortical projections to areas PE and PEa was established, exhibiting clusters of neurons in the same thalamic nuclei as above, in other words predominantly in the caudal thalamus. Via the giant endings CT projection, areas PE and PEa may send feedforward, transthalamic projections to remote cortical areas in the parietal, temporal and frontal lobes contributing to polysensory and sensorimotor integration, relevant for visual guidance of reaching movements for instance.     

An autoradiographic study of cortical projections from motor thalamic nuclei in the macaque monkey.

The special areal and laminar distributions of cortical afferent connections from various thalamic nuclei in the monkey (Macaca fuscata) were studied by using the anterograde axonal transport technique of autoradiography. The following findings were obtained. The superficial thalamocortical (T-C) projections, terminating in the (superficial half of) cortical layer I, arise mainly from the nucleus ventralis anterior, pars principalis (VApc) and nucleus ventralis lateralis, pars oralis (VLo), and possibly from the nucleus ventralis lateralis, pars medialis (VLm) and nucleus ventralis anterior, pars magnocellularis (VAmc). The VApc gives rise to the superficial T-C and deep T-C projections onto the postarcuate premotor area around the arcuate genu and spur, and onto the dorsomedial part of the caudal premotor area as well as the supplementary motor area (SMA). The VApc also gives rise to only deep T-C projections onto the remaining premotor area and onto the rostral bank of the arcuate sulcus as well as the ventral bank of the cingulate sulcus at the level of the premotor area. The VLo gives rise to the superficial T-C projections onto the ventrolateral part of the motor area (mainly to the forelimb motor area) and onto the dorsomedial part to the mesial cortex at the rostral level of the motor area. The VAmc gives rise to the superficial T-C projections onto the banks of the arcuate genu and adjacent region of area 8. Area X, the nucleus ventralis posterolateralis, pars oralis (VPLo), nucleus ventralis posterolateralis, pars caudalis (VPLc), nucleus ventralis posteromedialis (VPM) and possibly the nucleus ventralis lateralis, pars caudalis (VLc) send only deep T-C projections. The dorsal and medial parts of the VLc project onto the premotor area, the rostral part of the motor area and the SMA, and also the ventral bank of the cingulate sulcus. Area X projects onto the premotor area, the SMA, and the caudal part of area 8. The thalamic relay nuclei projecting onto the frontal association cortex were found to be the VAmc, medial VLc and area X.     

Observations on the secondary vestibulocerebellar projections in the macaque monkey

Summary The distribution of retrogradely labeled cells in the nuclei of the vestibular nuclear complex following injections of horseradish peroxidase in various parts of the cerebellar cortex (except the nodulus and paraflocculus) has been mapped in the macacus rhesus monkey. In the main the findings correspond to those made in other mammalian species (cf. Table 1). The flocculus receives afferents bilaterally from the superior, medial and descending vestibular nuclus, group y, the interstitial nucleus of the vestibular nerve and also from the abducent nucleus. The projection to the posterior vermis (lobules VIII and IX), expecially to lobule IX, is more abundant than that to lobules VI–VII. The projection to the anterior lobe vermis appears to be modest. Evidence for projections to the cerebellar hemispheres was not obtained. Whether the lateral vestibular nucleus projects to the cerebellum in the macaque is uncertain. The regular occurrence of weakly labeled cells among heavily labeled ones suggests that many of the cerebellar projecting cells may have axonal branches passing to other destinations. The findings lend support to the notion that there are precise topical relations within the entire secondary vestibulocerebellar projection. For example, in the medial nucleus the sites of origin of fibers to the flocculus and uvula are different. Surprisingly, many cells in group z were found to project to the uvula and — to a lesser extent — to lobule VIII. The group z may, therefore, not be a pure relay nucleus in a spinothalamic pathway, as generally assumed. The rather marked cerebellar projection of the abducent nucleus, expecially to the flocculus, is of interest for the analysis of cerebellar control of eye movements in the macaque.     

Direct projections from the extrathalamic forebrain structures to the neocortex in the macaque monkey

Extrathalamic direct projections from the subcortical forebrain structures to the neocortex were examined in the macaque monkey by the horseradish peroxidase method. The enzyme, when injected into discrete regions in the neocortex, labeled cell bodies of extrathalamic forebrain neurons in the basal nucleus of Meynert, nucleus of the diagonal band, medial septal nucleus, hypothalamus, claustrum and dorsolateral part of the basal amygdaloid nucleus. Neurons in the basal nucleus of Meynert, lateral hypothalamus and claustrum appeared to send their axons widely, but not diffusely, to the neocortex.     

Contralateral cortical projections to the superior colliculus in the macaque monkey

Summary Cortical projections from the contralateral hemisphere to the superior colliculus (SC) were studied in macaque monkey using retrograde transport of the enzyme horseradish peroxidase (HRP). After single or multiple injections of HRP into SC, labelled cells were found contralaterally in layer V of the anterior bank of the arcuate sulcus, the origin of this contralateral projection being confined to the anterior part of Brodmann's area 6. Only a few labelled cells appeared in adjacent area 8. Labelled cells occured in patches, forming bands which were found to run in a ventromedial direction. A similar pattern was seen homotopically in ipsilateral area 6. Thus, this anterior part of area 6 gives rise to a bilateral projection to the SC. The findings emphasize structural differences in a region of the frontal lobe which has been considered functionally uniform as frontal eye field.Supported by Deutsche Forschungsgemeinschaft (SFB 50/C6 and Di 212/2)     

Somatotopical projections from the supplementary motor area to the red nucleus in the macaque monkey

Direct projections from the supplementary motor area (SMA) to the red nucleus were investigated in the Japanese monkey (Macaca fuscata). The anterograde tracer, horseradish peroxidase conjugated to wheat germ agglutinin (WGA-HRP), was injected into various regions of the SMA after intracortical microstimulation mapping. After WGA-HRP injection into the orofacial, forelimb, or hindlimb region of the SMA, anterogradely labeled axon terminals were found, respectively, in the medial, intermediate, or lateral portion of the parvocellular part of the red nucleus, bilaterally with an ipsilateral predominance. The results indicate the clear somatotopical arrangement of corticorubral projections from the SMA.     

Posterior parietal projections to the intraparietal sulcus of the rhesus monkey

Summary A cyto- and myeloarchitectonic parcellation of the intraparietal sulcus in the rhesus monkey was correlated with the pattern of afferent connections from the parietal lobe as determined by autoradiographic techniques. Area PEa in the upper bank receives topographically-organized input from the ventral and caudal superior parietal lobule and the medial surface of the parietal lobe. Area POa in the lower bank is the recipient of a projection from the rostral inferior parietal lobule. Area IPd, situated in the depth of the intraparietal sulcus, receives converging input from the caudal superior parietal lobule, medial surface of the parietal lobe, and mid-and caudal inferior parietal lobule. Finally, intrinsic sequences of connections, directed from rostral to caudal and caudal to rostral, exist within both areas PEa and POa, each having a distinctive laminar pattern of origins and terminations.Preliminary results of this investigation were presented at the meeting of the Society for Neuroscience, Boston, November 1983     

Topographic organization for delayed saccades in human posterior parietal cortex

Posterior parietal cortex (PPC) is thought to play a critical role in decision making, sensory attention, motor intention, and/or working memory. Research on the PPC in non-human primates has focused on the lateral intraparietal area (LIP) in the intraparietal sulcus (IPS). Neurons in LIP respond after the onset of visual targets, just before saccades to those targets, and during the delay period in between. To study the function of posterior parietal cortex in humans, it will be crucial to have a routine and reliable method for localizing specific parietal areas in individual subjects. Here, we show that human PPC contains at least two topographically organized regions, which are candidates for the human homologue of LIP. We mapped the topographic organization of human PPC for delayed (memory guided) saccades using fMRI. Subjects were instructed to fixate centrally while a peripheral target was briefly presented. After a further 3-s delay, subjects made a saccade to the remembered target location followed by a saccade back to fixation and a 1-s inter-trial interval. Targets appeared at successive locations "around the clock" (same eccentricity, approximately 30 degrees angular steps), to produce a traveling wave of activity in areas that are topographically organized. PPC exhibited topographic organization for delayed saccades. We defined two areas in each hemisphere that contained topographic maps of the contra-lateral visual field. These two areas were immediately rostral to V7 as defined by standard retinotopic mapping. The two areas were separated from each other and from V7 by reversals in visual field orientation. However, we leave open the possibility that these two areas will be further subdivided in future studies. Our results demonstrate that topographic maps tile the cortex continuously from V1 well into PPC.     

Memory related motor planning activity in posterior parietal cortex of macaque

Summary Unit recording studies in the lateral bank of the intraparietal cortex (area LIP) have demonstrated a response property not previously reported in posterior cortex. Studies were performed in the Rhesus monkey during tasks which required saccadic eye movements to remembered target locations in the dark. Neurons were found which remained active during the time period for which the monkey had to withhold eye movements while remembering desired target locations. The activity of the cells was tuned for eye movements of specific direction and amplitude, and it was not necessary for a visual stimulus to fall within the response field. The responses appeared to represent a memory-related motor-planning signal encoding motor error. The relation of the activity to the behavior of the animal suggests that the response represents the intent to make eye movements of specific direction and amplitude.     

Protracted postnatal development of corticospinal projections from the primary motor cortex to hand motoneurones in the macaque monkey

We have studied the development of corticospinal projections from the hand area of the primary motor cortex to the spinal cord using anterograde transport of WGA-HRP. In the neonate, as in the adult, corticospinal projections to the intermediate zone at the C8/T1 spinal level were clearly present. However, in contrast to the adult, there was only very faint and barely visible labelling in the dorso-lateral motor nuclei which supply the hand muscles. No aberrant projections to other motor nuclei were seen. By 2.5 months, a ring of dense labelling was present around the dorso-lateral motor nuclei, but labelling was still sparse in the central region. This labelling was more pronounced at 11 months, but was still not as heavy as in the adult. There was no labelling among the ventral motoneurones at any age. The conduction velocity (c.v.) of the fastest corticospinal fibres was determined in each of the monkeys. There was an age-related increase in c.v. within the spinal cord. At birth, the fastest axons had a c.v. of only 8 m·s^-1. At 11 months c.v. was still substantially slower (55 m·s^-1) than the adult value of 73 m·s^-1. In contrast, by 11 months, the axonal c.v. within the brain was close to the adult value, suggesting a rostro-caudal maturation of the corticospinal system. Our results demonstrate that corticospinal projections in the macaque monkey mature gradually over a period of at least 11 months, much longer than previously thought.     

Direct projections to the prestriate cortex from the retino-recipient zone of the inferior pulvinar nucleus in the macaque monkey

It was found by the anterograde and retrograde horseradish peroxidase methods that the medial border region of the inferior pulvinar nucleus of the Japanese monkey (Macaca fuscata), where optic fibers have been shown to end [8], was connected reciprocally with the ipsilateral prestriate cortical regions around the compensatory sulcus on the medial surface of the cerebral hemisphere.     

The distribution of posterior parietal fibers in the corpus callosum of the rhesus monkey

Summary The distribution of posterior parietal fibers in the corpus callosum of the rhesus monkey was analyzed using autoradiographic techniques. Posterior parietal fibers are located in the posterior half of the body of the corpus callosum. There is some segregation of fibers with respect to their place of origin within the posterior parietal lobe. However, there is also overlap, particularly between fibers coming from the caudal inferior parietal lobule and the medial parietal lobe.Supported by the Veterans Administration, Edith Nourse Rogers Memorial Veterans Hospital, Bedford, Massachusetts and N.I.H. Grants NS 09211 and NS 16841     

Functional properties of rotation-sensitive neurons in the posterior parietal association cortex of the monkey

We studied the functional properties of rotation-sensitive (RS) neurons of the posterior parietal association cortex in detail. We classified 58 neurons as RS neurons on the basis of statistical analysis, to indicate that their responses to rotary movement were significantly greater (P<0.01) than those to linear movement of the same stimulus. We calculated rotation index, 1 — (L/R), in 82 cells, where L/R is the ratio of net response to linear movement to that to rotary movement. All the RS neurons had rotation index greater than or equal to 0.3. The recording site of these RS neurons was localized in the posterolateral part of area PG (area 7a of Vogt), on the anterior bank of the caudal superior temporal sulcus (STS), in the region partly overlapping the medial superior temporal (MST) area. We compared the response of RS neurons to rotation with that to shearing movement as well as to linear movement. In the majority of RS neurons the ratio of shearing response to rotation response (S/R) was smaller than the ratio of linear response to rotation response (L/R), indicating that the response to rotation was not due to a simple combination of linear movements in the opposite direction. Most of the RS neurons responded to the rotary movement of a single spot as well as that of a slit, although the response was smaller (average 70%) for the former. Most of the RS neurons had large receptive fields (60–180° in diameter) and their responses were independent of the position within the receptive field. The responses of most RS neurons increased monotonically with the increase in angular velocity and were also dependent on the size of the stimulus, although the rate of increase was small when the length was more than 10°. The majority of RS neurons (37/58) responded better to rotation in depth than to that in the frontoparallel plane. Some of them (12/37) responded to diagonal rotation rather than to sagittal or horizontal rotation. We found that some depth RS neurons showed reversal in the preferred direction when we used a trapezoidal window-like plate as the rotating stimulus in the monocular viewing condition, just as occurs in the case of the Ames window illusion. The response of some RS neurons (5/7) was enhanced by tracking eye movement. The enhanced responses were observed during rotary tracking but not during linear tracking. Other RS neurons (n = 2) showed maximum response to the rotation of the monkey chair in the light, as a result of convergence of visual and vestibular signals. We concluded that the continuous change of direction of movement was the most important cue for RS neurons to respond selectively to rotary movement in contrast to linear translational movement, and that these neurons were likely to discriminate the direction and orientation of the plane of rotation of the object in space.     

Retinal projections to the pulvinar nucleus of the macaque monkey: a re-investigation using autoradiography

Summary After a monocular injection of [³H]amino acid into the vitreous chamber of the eye, the distribution of retinal terminations in the pulvinar nucleus of the crab-eating monkey and pigtail macaque was studied by autoradiography. Two groups of labeled terminals were found in the bilateral inferior pulvinar nuclei: one small, dense group was located in the most rostral part of the nuclei and the other, composed of a few small clusters of the labeled terminals, was observed over the medial zone of the middle portion. The terminals were slightly predominant in the contralateral nucleus. A small amount of silver grains showing labeled retinofugal fibers was found in the dorsal surface of the thalamus just medial to the stria terminalis contralateral to the injected site, but termination of these fibers could not be traced in this study.