We examined the organization and cortical projections of the somatosensory thalamus using multiunit microelectrode recording techniques in anesthetized monkeys combined with neuroanatomical tracings techniques and architectonic analysis. Different portions of the hand representation in area 3b were injected with different anatomical tracers in the same animal, or matched body part representations in parietal areas 3a, 3b, 1, 2, and areas 2 and 5 were injected with different anatomical tracers in the same animal to directly compare their thalamocortical connections. We found that the somatosensory thalamus is composed of several representations of cutaneous and deep receptors of the contralateral body. These nuclei include the ventral posterior nucleus (VP), the ventral posterior superior nucleus (VPs), the ventral posterior inferior nucleus (VPi), and the ventral lateral nucleus (VLp). Each nucleus projects to several different cortical fields, and each cortical field receives projections from multiple thalamic nuclei. In contrast to other sensory systems, each of these somatosensory cortical fields is uniquely innervated by multiple thalamic nuclei. These data indicate that multiple inputs are processed simultaneously within and across several, ‘hierarchically connected’ cortical fields.

We studied cortical connections of functionally distinct movement zones of the posterior parietal cortex (PPC) in galagos identified by intracortical microstimulation with long stimulus trains (~500 msec). All these zones were in the anterior half of PPC, and each of them had a different pattern of connections with premotor (PM) and motor (M1) areas of the frontal lobe and with other areas of parietal and occipital cortex. The most rostral PPC zone has major connections with motor and visuomotor areas of frontal cortex as well as with somatosensory areas 3a and 1-2 and higher order somatosensory areas in the lateral sulcus. The dorsal part of anterior PPC region representing hand-to-mouth movements is connected mostly to the forelimb representation in PM, M1, 3a, 1-2, and somatosensory areas in the lateral sulcus and on the medial wall. The more posterior defensive and reaching zones have additional connections with nonprimary visual areas (V2, V3, DL, DM, MST). Ventral aggressive and defensive face zones have reciprocal connections with each other as well as connections with mostly face, but also forelimb representations of premotor areas and M1 as well as prefrontal cortex, FEF, and somatosensory areas in the lateral sulcus and areas on the medial surface of the hemisphere. Whereas the defensive face zone is additionally connected to nonprimary visual cortical areas, the aggressive face zone is not. These differences in connections are consistent with our functional parcellation of PPC based on intracortical long-train microstimulation, and they identify parts of cortical networks that mediate different motor behaviors.

The posterior parietal cortex (PPC) of monkeys and prosimian galagos contains a number of subregions where complex, behaviorally meaningful movements, such as reaching, grasping, and body defense, can be evoked by electrical stimulation with long trains of electrical pulses through microelectrodes. Shorter trains of pulses evoke no or simple movements. One possibility for the difference in effectiveness of intracortical microstimulation is that long trains activate much larger regions of the brain. Here, we show that long-train stimulation of PPC does not activate widespread regions of frontal motor and premotor cortex but instead, produces focal, somatotopically appropriate activations of frontal motor and premotor cortex. Shorter stimulation trains activate the same frontal foci but less strongly, showing that longer stimulus trains do not produce less specification. Because the activated sites in frontal cortex correspond to the locations of direct parietalfrontal anatomical connections from the stimulated PPC subregions, the results show the usefulness of optical imaging in conjunction with electrical stimulation in showing functional pathways between nodes in behavior-specific cortical networks. Thus, longtrain stimulation is effective in evoking ethologically relevant sequences of movements by activating nodes in a cortical network for a behaviorally relevant period rather than spreading activation in a nonspecific manner.complex movements | nonhuman primate | neocortex P osterior parietal cortex (PPC) in primates is widely considered to be involved in creating intentions to perform specific motor behaviors, such as grasping, reaching, or directing eyes to new targets (1-5). These intentions are then implemented through connections with primary motor (M1) and premotor (PM) cortex (6-8). Representations of simple movements of various body parts in frontal motor cortex (M1-PM) have been traditionally revealed by use of short bursts of electrical pulses delivered with microelectrodes (9-12). By introducing the use of longer (500 ms) trains of electrical pulses, Graziano et al. (13,14) and Graziano (15) have identified zones in M1-PM of macaque where grasping, reaching, and other complex, functionally significant movements are evoked. In addition, they have identified matching zones in PPC and M1-PM regions where similar defensive movements of the arm and face can be evoked (16,17). Our more recent studies with long-train stimulation have identified a series of functional zones in PPC of prosimian galagos (18,19). These PPC movement zones are preferentially interconnected with functionally matched zones in PM and motor cortex (20). M1 cortex seems to be an essential node in these parietal-frontal networks, because PPC stimulation was ineffective when M1 activity was blocked.Although long-train stimulation has the potential to reveal much that is new about the functional organization of PPC and the parietal-frontal network that is involved in the production of movements, we do not yet know how long-train effect...

After large but incomplete lesions of ascending dorsal column afferents in the cervical spinal cord, the hand representation in the contralateral primary somatosensory cortex (area 3b) of monkeys is largely or completely unresponsive to touch on the hand. However, after weeks of spontaneous recovery, considerable reactivation of the hand territory in area 3b can occur. Because the reactivation process likely depends on the sprouting of remaining axons from the hand in the cuneate nucleus of the lower brainstem, we sought to influence cortical reactivation by treating the cuneate nucleus with an enzyme, chondroitinase ABC, that digests perineuronal nets, promoting axon sprouting. Dorsal column lesions were placed at a spinal cord level (C5/C6) that allowed a portion of ascending afferents from digit 1 to survive in squirrel monkeys. After 11-12 wk of recovery, the contralateral forelimb cortex was reactivated by stimulating digit 1 more extensively in treated monkeys than in control monkeys. The results are consistent with the proposal that the treatment enhances the sprouting of digit 1 afferents in the cuneate nucleus and that this sprouting allowed these preserved inputs to activate cortex more effectively.plasticity | primates I mmediately after a major loss of sensory inputs from an arm or other part of the body in primates and other mammals, most or all of the corresponding part of the somatotopic representation in the primary somatosensory cortex no longer responds to touch (1-3). However, preserved inputs may activate some of the deprived cortex, and over weeks of recovery more and more of the deprived cortex responds to remaining inputs. When somatosensory inputs from the hand have been largely removed in monkeys by cutting ascending branches of cutaneous afferents in the dorsal column pathways of the spinal cord (2, 4, 5) or by selectively cutting the dorsal roots of peripheral nerves subserving a part of the hand (3), most of the territory of the representation of the hand in the contralateral primary somatosensory cortex (area 3b) initially fails to respond to touch on the hand. In food-retrieval tasks, hand use is impaired, and the monkeys look for food pellets already in their hand as although unsure whether they have grasped the food object (5, 6). However, hand use rapidly recovers over days to weeks as the remaining inputs from the hand reactivate more and more of the cortical territory for the hand. Thus, the reactivation of cortex by preserved afferents from the hand appears to be important in the behavioral recovery.The mechanisms of the reactivation are not understood completely, but at least some of the reactivation occurs at the first relay of information from the preserved dorsal column afferents in the cuneate nucleus of the lower brainstem and upper spinal cord (7,8). It appears that preserved axon terminals of primary afferents, and possibly second-order neurons in the spinal cord (5), sprout in the cuneate nucleus to activate neurons more effectively (9, 10). Similar amplifications of ...

To better reveal the pattern of corticotectal projections to the superficial layers of the superior colliculus (SC), we made a total of ten retrograde tracer injections into the SC of three macaque monkeys (Macaca mulatta). The majority of these injections were in the superficial layers of the SC, which process visual information. To isolate inputs to the purely visual layers in the superficial SC from those inputs to the motor and multisensory layers deeper in the SC, two injections were placed to include the intermediate and deep layers of the SC. In another case, an injection was placed in the medial pulvinar, a nucleus not known to be strongly connected with visual cortex, to identify possible projections from tracer spread past the lateral boundary of the SC. Four conclusions are supported by the results: 1) all early visual areas of cortex, including V1, V2, V3, and the middle temporal area, project to the superficial layers of the SC; 2) with the possible exception of the frontal eye field, few areas of cortex outside of the early visual areas project to the superficial SC, although many do, however, project to the intermediate and deep layers of the SC; 3) roughly matching retinotopy is conserved in the projections of visual areas to the SC; and 4) the projections from different visual areas are similarly dense, although projections from early visual areas appear somewhat denser than those of higher order visual areas in macaque cortex.

We placed injections of anatomical tracers into representations of the tongue, teeth, and face in the primary somatosensory cortex (area 3b) of macaque monkeys. Our injections revealed strong projections to representations of the tongue and teeth from other parts of the oral cavity responsive region in 3b. The 3b face also provided input to the representations of the intra-oral structures. The primary representation of the face showed a pattern of intrinsic connections similar to that of the mouth. The area 3b hand representation provided little to no input to either the mouth or face representations. The mouth and face representations of area 3b received projections from the presumptive oral cavity and face regions of other somatosensory areas in the anterior parietal cortex and the lateral sulcus including areas 3a, 1, 2, the second somatosensory area (S2), the parietal ventral area (PV), and cortex that may include the parietal rostral (PR) and ventral somatosensory (VS) areas. Additional inputs came from primary motor (M1) and ventral premotor (PMv) areas. This areal pattern of projections is similar to the well-studied pattern revealed by tracer injections in regions of 3b representing the hand. The tongue representation appeared to be unique in area 3b in that it also received inputs from areas in the anterior upper bank of the lateral sulcus and anterior insula that may include the primary gustatory area (area G) and other cortical taste processing areas, as well as a region of lateral prefrontal cortex (LPFC) lining the principal sulcus.

Significance We examined the cortical control of a laryngeal muscle that is essential for vocalization in two monkey species that differ in their vocal motor skill. Our results suggest that enhancements in vocal skill are coupled to enlargements in the descending output from two premotor areas, ventral area 6 (area 6V) and the supplementary motor area (SMA). This result challenges the view that improvements in motor skills are due largely to changes in the output from the primary motor cortex.

Posterior parietal cortex (PPC) of prosimian galagos includes a rostral portion (PPCr) where electrical stimulation evokes different classes of complex movements from different subregions, and a caudal portion (PPCc) where such stimulation fails to evoke movements in anesthetized preparations ( Stepniewska, Fang et al. 2009). We placed tracer injections into PPCc to reveal patterns of its cortical connections. There were widespread connections within PPCc as well as connections with PPCr and extrastriate visual areas, including V2 and V3. Weaker connections were with dorsal premotor cortex, and the frontal eye field. The connections of different parts of PPCc with visual areas were roughly retinotopic such that injections to dorsal PPCc labeled more neurons in the dorsal portions of visual areas, representing lower visual quadrant, and injections to ventral PPCc labeled more neurons in ventral portions of these visual areas, representing the upper visual quadrant. We conclude that much of the PPCc contains a crude representation of the contralateral visual hemifield, with inputs largely, but not exclusively, from higher-order visual areas that are considered part of the dorsal visuomotor processing stream. As in galagos, the caudal half of PPC was likely visual in early primates, with the rostral PPC half mediating sensorimotor functions.