Interconnections between the prefrontal cortex and the premotor areas in the frontal lobe

We examined interconnections between a portion of the prefrontal cortex and the premotor areas in the frontal lobe to provide insights into the routes by which the prefrontal cortex gains access to the primary motor cortex and the central control of movement. We placed multiple injections of one retrograde tracer in the arm area of the primary motor cortex to define the premotor areas in the frontal lobe. Then, in the same animal, we placed multiple injections of another retrograde tracer in and around the principal sulcus (Walker's area 46). This double labeling strategy enabled us to determine which premotor areas are interconnected with the prefrontal cortex. There are three major results of this study. First, we found that five of the six premotor areas in the frontal lobe are interconnected with the dorsolateral prefrontal cortex. Second, the major site for interactions between the prefrontal cortex and the premotor areas is the ventral premotor area. Third, the prefrontal cortex is interconnected with only a portion of the arm representation in three premotor areas (supplementary motor area, the caudal cingulate motor area on the ventral bank of the cingulate sulcus, and the dorsal premotor area), whereas it is interconnected with the entire arm representation in the ventral premotor area and the rostral cingulate motor area. These observations indicate that the output of the prefrontal cortex targets specific premotor areas and even subregions within individual premotor areas.     

Reevaluation of ipsilateral corticocortical inputs to the orofacial region of the primary motor cortex in the macaque monkey

An anatomical approach to possible areas in the cerebral cortex involved in somatic motor behavior is to analyze the cortical areas containing neurons that connect directly to the primary motor cortex (MI). To define the cortical areas related to orofacial movements, we examined the distribution of cortical neurons that send their axons to the orofacial region of the MI in the macaque monkey. Injections of retrograde tracers into the electrophysiologically identified orofacial region of the MI revealed that labeled neurons were distributed in the following cortical areas: the orbital cortex (area 12), insular cortex, frontoparietal operculum (including the deep part of the cortical masticatory area and the secondary somatosensory cortex), ventral division of the premotor cortex (especially in its lateral part), orofacial region of the supplementary motor area, rostral division of the cingulate motor area (CMA), and CMA on the ventral bank. A number of labeled neurons were also seen in the MI around the injection sites and in the parietal cortex (including the primary somatosensory cortex and area 7b). No labeled neurons were found in the dorsal division of the premotor cortex. Fluorescent retrograde double labeling further revealed virtually no overlap of distribution between cortical neurons projecting to the orofacial and forelimb regions of the MI. Based on the present results, we discuss the functional diversity of the cortical areas related to orofacial motor behavior and the somatotopical organization in the premotor areas of the frontal cortex. J. Comp. Neurol. 389:34–48, 1997.© 1997 Wiley-Liss, Inc.     

Cortical connections of the inferior arcuate sulcus cortex in the macaque brain

Injections of the retrograde/anterograde tracers Wheat Germ Agglutinin-Horseradish peroxidase (WGA-HRP) into the cortex along the banks of the inferior limb of the arcuate sulcus in the cortex of 4 macaque monkeys (Macaca fascicularis) were used to investigate its cortico-cortical connections. All injections produced transported label within the sulcus principalis, the ventral lateral prefrontal cortex, the anterior cingulate sulcus and the dorsal insular cortex. The distribution of label within each of these areas differed slightly depending on the injection site. Injections along the caudal bank of the inferior arcuate sulcus label premotor, supplementary motor, and precentral motor areas but produce relatively sparse prefrontal labeling. Posteriorly label is transported to the inferior parietal cortex and the dorsal opercular bank of the Sylvian fissure. Injections along the rostral bank of the sulcus do not label motor areas but produce labeling in dorsal, lateral and orbital prefrontal areas, and in cortex along the ventral bank of the superior branch of the arcuate sulcus. Posteriorly label is transported to cortical areas in the superior temporal gyrus including the dorsal bank of the superior temporal sulcus. The more dorsal rostral bank injection produced both superior temporal and some sparse inferior parietal labeling and the more ventral rostral bank injection produced extensive superior temporal labeling but no parietal labeling. No labeling was ever seen in cortex ventral to the fundus of the superior temporal sulcus. Although other auditory recipient prefrontal areas have been reported, this is the first demonstration of a region chiefly devoted to auditory connections within the ventral frontal cortex. Its adjacency to areas associated with vocal muscle movement, and its connections to midline cortical areas associated with vocal functions in both primates and humans may provide important clues to the organization of Broca's language area.     

Ipsilateral cortical connections of motor, premotor, frontal eye, and posterior parietal fields in a prosimian primate, Otolemur garnetti

The ipsilateral connections of motor areas of galagos were determined by injecting tracers into primary motor cortex (M1), dorsal premotor area (PMD), ventral premotor area (PMV), supplementary motor area (SMA), and frontal eye field (FEF). Other injections were placed in frontal cortex and in posterior parietal cortex to define the connections of motor areas further. Intracortical microstimulation was used to identify injection sites and map motor areas in the same cases. The major connections of M1 were with premotor cortex, SMA, cingulate motor cortex, somatosensory areas 3a and 1, and the rostral half of posterior parietal cortex. Less dense connections were with the second (S2) and parietal ventral (PV) somatosensory areas. Injections in PMD labeled neurons across a mediolateral belt of posterior parietal cortex extending from the medial wall to lateral to the intraparietal sulcus. Other inputs came from SMA, M1, PMV, and adjoining frontal cortex. PMV injections labeled neurons across a large zone of posterior parietal cortex, overlapping the region projecting to PMD but centered more laterally. Other connections were with M1, PMD, and frontal cortex and sparsely with somatosensory areas 3a, 1-2, S2, and PV. SMA connections were with medial posterior parietal cortex, cingulate motor cortex, PMD, and PMV. An FEF injection labeled neurons in the intraparietal sulcus. Injections in posterior parietal cortex revealed that the rostral half receives somatosensory inputs, whereas the caudal half receives visual inputs. Thus, posterior parietal cortex links visual and somatosensory areas with motor fields of frontal cortex.     

Projections from the superior temporal sulcus to the agranular frontal cortex in the macaque

The aim of this study was to investigate the organization of the projections from the superior temporal sulcus (STS) to the various areas forming the agranular frontal cortex. Injections of retrograde neuronal tracers were made in the various agranular areas, in nine macaque monkeys. The results showed that two rostral premotor areas, F6 (pre-SMA) and F7, and the ventrorostral part of area F2 (F2vr) are targets of projections from the upper bank of the STS (uSTS). F6 and the dorsorostral part of F7 (supplementary eye field, SEF) are targets of projections from the rostral part of the uSTS, corresponding to the so-called 'superior temporal polysensory area' (STP). In contrast, the ventral part of area F7 (not including the SEF) and F2vr are targets of afferents from the caudal part of the uSTS. Ventral F7 is the target of weak afferents from the caudalmost and dorsalmost part of the uSTS (area 7a), whilst F2vr is the target of projections from a relatively more rostral and ventral sector of the uSTS, close to the fundus of the sulcus. This sector should correspond to area MST. In conclusion, F6 and SEF receive high order information from STP, whereas ventral F7 and F2vr receive information from areas of the dorsal visual stream.     

Posterior parietal cortex in rhesus monkey: II. Evidence for segregated corticocortical networks linking sensory and limbic areas with the frontal lobe

We have examined the circuitry connecting the posterior parietal cortex with the frontal lobe of rhesus monkeys. HRP-WGA and tritiated amino acids were injected into subdivisions 7m, 7a, 7b, and 7ip of the posterior parietal cortex, and anterograde and retrograde label was recorded within the frontal motor and association cortices. Our main finding is that each subdivision of parietal cortex is connected with a unique set of frontal areas. Thus, area 7m, on the medial parietal surface, is interconnected with the dorsal premotor cortex and the supplementary motor area, including the supplementary eye field. Within the prefrontal cortex, area 7m's connections are with the rostral sector of the frontal eye field (FEF), the dorsal bank of the principal sulcus, and the anterior bank of the inferior arcuate sulcus (Walker's area 45). In contrast, area 7a, on the posterior parietal convexity, is not linked with premotor regions but is heavily interconnected with the rostral FEF in the anterior bank of the superior arcuate sulcus, the dorsolateral prefrontal convexity, the rostral orbitofrontal cortex, area 45, and the fundus and adjacent cortex of the dorsal and ventral banks of the principal sulcus. Area 7b, in the anterior part of the posterior parietal lobule, is interconnected with still a different set of frontal areas, which include the ventral premotor cortex and supplementary motor area, area 45, and the external part of the ventral bank of the principal sulcus. The prominent connections of area 7ip, in the posterior bank of the intraparietal sulcus, are with the supplementary eye field and restricted portions of the ventral premotor cortex, with a wide area of the FEF that includes both its rostral and caudal sectors, and with area 45. All frontoparietal connections are reciprocal, and although they are most prominent within a hemisphere, notable interhemispheric connections are also present. These findings provide a basis for a parcellation of the classically considered association cortex of the frontal lobe, particularly the cortex of the principal sulcus, into sectors defined by their specific connections with the posterior parietal subdivisions. Moreover, the present findings, together with those of a companion study (Cavada and Goldman-Rakic: J. Comp. Neurol. this issue) have allowed us to establish multiple linkages between frontal areas and specific limbic and sensory cortices through the posterior parietal cortex. The networks thus defined may form part of the neural substrate of parallel distributed processing in the cerebral cortex.     

The organization and connections of somatosensory cortex in marmosets

Microelectrode mapping methods were used to define and describe 3 representations of the body surface in somatosensory cortex of marmosets: S-I proper or area 3b of anterior parietal cortex, S-II, and the parietal ventral area (PV) of the upper bank of the lateral sulcus. In the same animals, injections of anatomical tracers were placed into electrophysiologically determined sites in area 3b or S-II. Mapping results and patterns of connections were later related to architectonic fields that were delimited in sections cut parallel to the surface of manually flattened cortex and stained for myelin. There were several major results. (1) Recordings from area 3b revealed a characteristic somatotopic organization of foot to face in a mediolateral sequence as previously reported in other members of the marmoset family (Carlson et al., 1986). (2) Multiple injections of WGA-HRP in area 3b demonstrated dense, patchy interconnections with ipsilateral S-II, PV, area 3a, and area 1, less dense interconnections with primary motor cortex (M-I), the supplementary motor area (SMA), limbic cortex of the medial wall (L), and rostrolateral parietal cortex of the lateral sulcus (PR), and callosal connections with areas 3b, S-II, and PV. Injections of 3 different tracers into the representation of 3 body regions in area 3b indicated that the connections with areas 3a, 3b, 1, S-II, and PV are topographically organized. (3) Recordings from cortex on the upper bank of the lateral sulcus demonstrated a somatotopic representation of the body surface that matches that of S-II of other mammals. S-II immediately adjoined areas 3b along the dorsal lip of the lateral sulcus. The face representation in S-II was adjacent to the face representation in 3b while the trunk, hindlimb, and forelimb were represented in a caudorostral sequence deeper in the sulcus. (4) Injections in S-II revealed ipsilateral connections with areas 3a, 3b, 1, a presumptive area 2, PV, PR, M-I, SMA, limbic cortex, the frontal eye fields, and the frontal ventral visual area. Dense callosal connections were with S-II and PV. (5) The recordings also revealed a systematic representation just rostral to S-II that has not been previously described in primates.(ABSTRACT TRUNCATED AT 400 WORDS)     

Distribution of cat-301 immunoreactivity in the frontal and parietal lobes of the macaque monkey

The distribution of the monoclonal antibody Cat-301 was examined in the frontal and parietal cortex of macaque monkeys. In both regions the distribution was uniform within cytoarchitecturally defined areas (or subareas) but varied between them. In all areas, Cat-301 labeled the soma and proximal dendrites of a restricted population of neurons. In the frontal lobe, Cat-301-positive neurons were intensely immunoreactive and present in large numbers in the motor cortex (area 4), premotor cortex (area 6, excluding its lower ventral part), the supplementary motor area (SMA), and the caudal prefrontal cortex (areas 8a, 8b and 45). In the parietal lobe, large numbers of intensely immunoreactive neurons were evident in the post-central gyrus (areas 1 and 2), the superior parietal lobule (PE/5), and the dorsal bank (PEa), fundus (IPd), and deep half of the ventral bank (POa(i] of the intraparietal sulcus (IPS). Two major patterns of laminar distribution were evident. In motor, supplementary motor, premotor (excluding the lower part of its ventral division), and the caudal prefrontal cortex (Walker's areas 8a, 8b and 45), and throughout the parietal cortex (with the exception of area 3), Cat-301-positive neurons were concentrated in the lower part of layer III and in layer V. The laminar positions of labeled cells in these areas were remarkably constant, as were the proportions of labeled neurons that had pyramidal and nonpyramidal morphologies (means of 30.2% and 69.8%, respectively). In contrast, in prefrontal areas 9, 10, 11, 12, 13, 14, and 46, in the cingulate cortex (areas 23, 24 and 25), and in the lower part of the ventral premotor cortex, Cat-301-positive neurons were spread diffusely across layers II to VI and a mean of 3.6% of the labeled neurons were pyramidal while 96.4% were nonpyramidal. Area 3 was unique among frontal and parietal areas, in that the labeled neurons in this area were concentrated in layers IV and VI. The areas in the frontal lobe which were heavily labeled are thought to be involved in the control of somatic (areas 4 and 6) and ocular (areas 8 and 45) movements. Those in parietal cortex may be classified as areas with somatosensory functions (1, 2, PE/5, and PEa) and areas which may participate in the analysis of visual motion (Pandya and Seltzer's IPd and POa(i), which contain Maunsell and Van Essen's VIP). The parietal somatosensory areas are connected to frontal areas with somatic motor functions, while POa(i) is interconnected with the frontal eye fields (8a and 45).(ABSTRACT TRUNCATED AT 250 WORDS)     

Prefrontal granular cortex of the rhesus monkey. I. Intrahemispheric cortical afferents.

In 6 adolescent rhesus monkeys, unilateral injections of horseradish peroxidase (HRP) were made into 6 regions on the convexity of the prefrontal granular cortex.The afferents to each zone were considered with respect to whether they were local afferents (from adjacent frontal areas) or distal afferents (from outside frontal lobe). The strongest input onto prefrontal granular cortex comes from the temporal lobe and especially areas in and around the superior temporal gyrus. Area 10 in the frontal pole region receives input primarily from area 22 in the superior temporal gyrus and dorsal portion of the superior temporal sulcus. That portion of area 46 above the principal sulcus receives input primarily from area 22 in the upper bank of the superior temporal sulcus while area 46 below the principal sulcus has input from the insula of the superior temporal sulcus and area 21 in the lower bank of the superior temporal sulcus. The cortex within the concavity of the acurate sulcus differs in that the dorsal half (including areas 46 and 8a) receives input primarily from the dorsal bank and to a lesser degree the insula of the superior temporal sulcus while the ventral portion of this region including areas 45 and 46 receives input primarily from the lower bank of the superior temporal sulcus, inferior temporal gyrus and insula of the superior temporal sulcus. Input was noted from cingulate areas 23 and 24 to all 6 injected regions while retrosplenial cortex was noted to project to all but one of the injected regions, i.e. area 10. In addition, some labeled neurons were seen in area 7 after injections into area 46 and some were also seen in the inferior temporal gyrus and parahippocampal region after injections into the arcuate region. Finally, labeled neurons were noted in area 19 after injections into the ventral portion of the prefrontal granular cortex bounded by the arcuate sulcus.The HRP-positive neurons that comprised the intrahemispheric cortical afferents to prefrontal granular cortex were located primarily in layer iii. They were pyramidal in shape and ranged in size from small to medium. These neurons were found to be distributed in a horizontal band in which the number of labeled neurons waxed and waned, or they were distributed in a patchy or clumped manner. The possibility that both patterns of distribution represent a vertical or columnar organization to these afferent neurons is discussed.     

Cytoarchitecture and intrafrontal connections of the frontal cortex of the brain of the hamadryas baboon (Papio hamadryas).

A study was made of the cytoarchitecture of the lateral and medial frontal cortex in the hamadryas baboon (Papio hamadryas). The frontal corticocortical connections of areas 46, 8, 6, and 4 were investigated by injection of wheat-germ agglutinine conjugated to horseradish peroxiase (WGA-HRP) into different regions of areas 46, 8, and 6. The lateral region of the frontal lobe of the baboon consists of broad areas of motor (area 4), premotor (area 6), and the dorsolateral prefrontal cortex, each of which is further divided into subdivisions with distinct cytoarchitectural features: areas 4a, 4b, 4c; 6aα, 6aβ, 6aγ, 6bα, and 6β; 8A and 8B; 45; 46 and 46ps; 9; 10; and 12. Although the frontal cortex of the baboon brain exhibits the same basic cytoarchitectural features as the frontal corticies of the cercopithecus (campbelli?) (Vogt and Vogt, '19) or the macaque (Walker, '40; Barbas and Pandya, '87, '89), the baboon frontal cortex is very different from that of the macaque and cercopithecus in terms of cytoarchitecture: (1) the baboon frontal cortex has an additional area, termed here “6aγ”, within area 6, which has cytoarchitectural characteristics that are intermediate between those of areas 6 and 8; (2) the aggregation of giant pyramidal cells (> 50 μm. in diameter) is found only in area 4a in the baboon, whereas such aggregates are found in areas 4a and 4b and, occasionally, in area 4c in the macaque; and (3) area 46 of the prefrontal cortex of the baboon can be subdivided into the cortex that surrounds the principal sulcus (area 46) and the upper and lower banks of the principal sulcus (area 46ps). Retrogradely WGA-HRP labeled cells and anterogradely WGA-HRP labeled terminals coexisted in the frontal cortex in a columnar fashion, indicative of a reciprocity among the connections. The frontal cortico-cortical connections of areas 46, 8, 6, and 4 in the hamadryas baboon were organized as follows: (1) areas 46, 8, and 6 were connected to one another, (2) area 4 was connected only to area 6, and (3) these connections showed a gross ventrodorsal topography: the ventral regions of each of areas 46, 8, and 6 were connected more strongly to the ventral than the dorsal regions of the other areas; the dorsal regions of each of areas 46, 8, and 6 were connected more strongly to the dorsal than the ventral regions of the other areas. Moreover, the ventral region of area 6 was more strongly connected to the ventral than to the dorsal region of area 4, whereas the dorsal region of area 6 was more strongly connected to the dorsal than to the ventral region of area 4.     

Sensory and premotor connections of the orbital and medial prefrontal cortex of macaque monkeys

Sensory and premotor inputs to the orbital and medial prefrontal cortex (OMPFC) were studied with retrograde axonal tracers. Restricted areas of the lateral and posterior orbital cortex had specific connections with visual-, somatosensory-, olfactory-, gustatory-, and visceral-related structures. More medial areas received few direct sensory inputs. Within the lateral and posterior orbital cortex, area 121 received a substantial projection from visual areas in the inferior temporal cortex (TE). Area 12m received somatosensory input from face, digit, or forelimb regions in the opercular part of area 1–2, in area 7b, in the second somatosensory area (SII), and in the anterior infraparietal area (AIP). Areas 13m and 131 also received a projection from the opercular part of areas 1–2 and 3b. The posteromedial and lateral agranular insular areas (Iapm and Ial, respectively) received fibers from the ventral part of the parvicellular division of the ventroposterior medial nucleus of the thalamus (VPMpc) that may represent a visceral afferent system. The dorsal part of VPMpc projected to the adjacent gustatory cortex. These restricted inputs from several sensory modalities and the convergent corticocortical connections to orbital areas 13l and 13m suggest a network related to feeding. The OMPFC was also connected to premotor cortex in ventral area 6 (areas 6va and 6vb), in cingulate area 24c, and probably in the supplementary eye field. Area 6va projected to area 12m, whereas a region of area 6vb projected to area 131. The region of the supplementary eye field projected to areas 121, 120, and 12r. Area lal received fibers from area 24c. Lighter and more diffuse projections also reached wider areas of the OMPFC. For example, injections in several orbital areas labeled a few cells scattered through the anterior part of area TE and the superior temporalrus. There was also a projection to the intermediate agranular insular area (Iai) and to areas 13a and 12o from the apparently multimodal areas in the superior temporal sulcus and gyrus. © 1995 Wiley-Liss, Inc.     

Quantitative analyses of neurons projecting to primary motor cortex zones controlling limb movements in the rat

The objective was to determine if projections of single neurons to primary motor cortex preferentially terminate in several efferent zones that could form synergies for the execution of limb movements. Intracortical microstimulation was used to identify zones evoking hip flexion (HF), elbow flexion (EF), and both plantarflexion (PF) and dorsiflexion (DF) about the ankle. Histological examination showed that the zones from which some movements were evoked extended beyond the agranular cortex into granular cortex. Fluorogold, Fast blue, and propridium iodide or rhodamine-labeled dextran were injected into three of these four efferent zones in each rat. There was a virtual absence of multiple-labeled cells despite having an intermingling of different-colored cells of which 15% in frontal cortex were less than 1.2 mm away from a neighboring neuron that projected to a different efferent zone. This suggests that single neurons projecting to the motor cortex do not hard-wire specific synergies but rather project to single efferent zones in order to offer the greatest degree of freedom for the generation of movements. The distribution of ventral posterolateral and ventrolateral thalamic nucleus labeling depended on whether the injections were in granular or agranular cortex. Conversely, frontal cortex projections to motor efferent zones were made irrespective of their location in either granular or agranular cortex and thereby supporting their presumed role in the control of movements. Hindlimb motor cortex injections yielded retrograde labeling that extended into the more localised distribution of frontal cortex neurons retrogradely labeled from forelimb injections. This may allow hindlimb movements to be synchronized by forelimb movements during walking on challenging terrain.     

A second forelimb motor area exists in rat frontal cortex

Intracortical microstimulation of 40–50 points in the frontal cortex of ketamine-anesthetized rats using perpendicular penetrations has demonstrated a second forelimb area located rostrally near the frontal pole as well as confirming the existence of a more caudally located forelimb area just anterior to bregma. Cortex where neck and/or vibrissae movements were evoked separated the two forelimb areas. The rostral and caudal forelimb areas defined by microstimulation correspond with patches of corticospinal neurons labeled with HRP following injections of this tracer into the cervical enlargement. Digit movements were commonly evoked from the rostral forelimb area but were rarely elicited from the caudal forelimb area. The question of whether the rostral forelimb region is part of primary or supplementary motor cortex is not yet able to be answered.     

Early coding of reaching: frontal and parietal association connections of parieto-occipital cortex

The ipsilateral association connections of the cortex of the dorsal part of the rostral bank of the parieto-occipital sulcus and of the adjoining posterior part of the superior parietal lobule were studied by using different retrograde fluorescent tracers. Fluoro-Ruby, Fast blue and Diamidino yellow were injected into visual area V6A, and dorso-caudal (PMdc, F2) and dorso-rostral (PMdr, F7) premotor cortex, respectively. The parietal area of injection had been previously characterized physiologically in behaving monkeys, through a variety of oculomotor and visuomanual tasks. Area V6A is mainly linked by reciprocal projections to parietal areas 7m, MIP (medial intraparietal) and PEa, and, to a lesser extent, to frontal areas PMdr (rostral dorsal premotor cortex, F7) and PMdc (F2). All these areas project to that part of the dorsocaudal premotor cortex that has a direct access to primary motor cortex. V6A is also connected to area F5 and, to a lesser extent, to 7a, ventral (VIP) and lateral (LIP) intraparietal areas. This pattern of association connections may explain the presence of visually-related and eye-position signals in premotor cortex, as well as the influence of information concerning arm position and movement direction on V6A neural activity. Area V6A emerges as a potential 'early' node of the distributed network underlying visually-guided reaching. In this network, reciprocal association connections probably impose, through re-entrant signalling, a recursive property to the operations leading to the composition of eye and hand motor commands.     

Input-output organization of jaw movement-related areas in monkey frontal cortex

The brain mechanisms underlying mastication are not fully understood. To address this issue, we analyzed the distribution patterns of cortico-striatal and cortico-brainstem axon terminals and the origin of thalamocortical and intracortical fibers by injecting anterograde/retrograde tracers into physiologically and morphologically defined jaw movement-related cortical areas. Four areas were identified in the macaque monkey: the primary and supplementary orofacial motor areas (MIoro and SMAoro) and the principal and deep parts of the cortical masticatory area (CMaAp and CMaAd), where intracortical microstimulation produced single twitch-like or rhythmic jaw movements, respectively. Tracer injections into these areas labeled terminals in the ipsilateral putamen in a topographic fashion (MIoro vs. SMAoro and CMaAp vs. CMaAd), in the lateral reticular formation and trigeminal sensory nuclei contralaterally (MIoro and CMaAp) or bilaterally (SMAoro) in a complex manner of segregation vs. overlap, and in the medial parabranchial and K?lliker-Fuse nuclei contralaterally (CMaAd). The MIoro and CMaAp received thalamic projections from the ventrolateral and ventroposterolateral nuclei, the SMAoro from the ventroanterior and ventrolateral nuclei, and the CMaAd from the ventroposteromedial nucleus. The MIoro, SMAoro, CMaAp, and CMaAd received intracortical projections from the ventral premotor cortex and primary somatosensory cortex, the ventral premotor cortex and rostral cingulate motor area, the ventral premotor cortex and area 7b, and various sensory areas. In addition, the MIoro and CMaAp received projections from the three other jaw movement-related areas. Our results suggest that the four jaw movement-related cortical areas may play important roles in the formation of distinctive masticatory patterns.     

Auditory belt and parabelt projections to the prefrontal cortex in the Rhesus monkey

Recent anatomical and electrophysiological studies have expanded our knowledge of the auditory cortical system in primates and have described its organization as a series of concentric circles with a central or primary auditory core, surrounded by a lateral and medial belt of secondary auditory cortex with a tertiary parabelt cortex just lateral to this belt. Because recent studies have shown that rostral and caudal belt and parabelt cortices have distinct patterns of connections and acoustic responsivity, we hypothesized that these divergent auditory regions might have distinct targets in the frontal lobe. We, therefore, placed discrete injections of wheat germ agglutinin-horseradish peroxidase or fluorescent retrograde tracers into the prefrontal cortex of macaque monkeys and analyzed the anterograde and retrograde labeling in the aforementioned auditory areas. Injections that included rostral and orbital prefrontal areas (10, 46 rostral, 12) labeled the rostral belt and parabelt most heavily, whereas injections including the caudal principal sulcus (area 46), periarcuate cortex (area 8a), and ventrolateral prefrontal cortex (area12vl) labeled the caudal belt and parabelt. Projections originating in the parabelt cortex were denser than those arising from the lateral or medial belt cortices in most cases. In addition, the anterior third of the superior temporal gyrus and the dorsal bank of the superior temporal sulcus were also labeled after prefrontal injections, confirming previous studies. The present topographical results suggest that acoustic information diverges into separate streams that target distinct rostral and caudal domains of the prefrontal cortex, which may serve different acoustic functions. J. Comp. Neurol. 403:141–157, 1999. © 1999 Wiley-Liss, Inc.     

Topographical organization of the cortical afferent connections of the prefrontal cortex in the cat

The topographical distribution of the cortical afferent connections of the prefrontal cortex (PFC) in adult cats was studied by using the retrograde axonal transport of horseradish peroxidase technique. Small single injections of the enzyme were made in different locations of the PFC, and the areal location and density of the subsequent neuronal labeling in neocortex and allocortex were evaluated in each case. The comparison of the results obtained in the various cases revealed that four prefrontal sectors (rostral, dorsolateral, ventral, and dorsomedial) can be distinguished, each exhibiting a particular pattern of cortical afferents. All PFC sectors receive projections from the ipsilateral insular (agranular and granular subdivisions) and limbic (infralimbic, prelimbic, anterior limbic, cingular, and retrosplenial areas) cortices. These cortices provide the most abundant cortical projections to the PFC, and their various subdivisions have different preferential targets within the PFC. The premotor cortex and the following neocortical sensory association areas project differentially upon the various ipsilateral PFC sectors: the portion of the somatosensory area SIV in the upper bank of the anterior ectosylvian sulcus, the visual area in the lower bank of the same sulcus, the auditory area AII, the temporal area, the perirhinal cortex, the posterior suprasylvian area, area 20, the posterior ectosylvian area, the suprasylvian fringe, the lateral suprasylvian area (anterolateral and posterolateral subdivisions), area 5, and area 7. The olfactory peduncle, the prepiriform cortex, the cortico-amygdaloid transition area, the entorhinal cortex, the subiculum (ventral, posteroventral, and posterodorsal sectors), the caudomedial band of the hippocampal formation and the postsubiculum are the allocortical sources of afferents to the PFC. The dorsolateral PFC sector is the target of the largest insular, limbic, and neocortical sensory association projections. The dorsomedial and rostral sectors receive notably less abundant cortical afferents than the dorsolateral sector. Those to the dorsomedial sector arise from the same areas that project to the dorsolateral sector and are more abundant to the dorsal part, where the medial frontal eye field cortex is located. The rostral sector receives projections principally from all other PFC sectors, and from the limbic and insular cortices. The projections from the allocortex reach preferentially the ventral PFC sector. Intraprefrontal connections are most abundant within each PFC sector. Commissural interprefrontal connections are largest from the site homotopic to the HRP injection.(ABSTRACT TRUNCATED AT 400 WORDS)     

Ipsilateral connections of the ventral premotor cortex in a new world primate

The present study describes the pattern of connections of the ventral premotor cortex (PMv) with various cortical regions of the ipsilateral hemisphere in adult squirrel monkeys. Particularly, we 1) quantified the proportion of inputs and outputs that the PMv distal forelimb representation shares with other areas in the ipsilateral cortex and 2) defined the pattern of PMv connections with respect to the location of the distal forelimb representation in primary motor cortex (M1), primary somatosensory cortex (S1), and supplementary motor area (SMA). Intracortical microstimulation techniques (ICMS) were used in four experimentally naïve monkeys to identify M1, PMv, and SMA forelimb movement representations. Multiunit recording techniques and myelin staining were used to identify the S1 hand representation. Then, biotinylated dextran amine (BDA; 10,000 MW) was injected in the center of the PMv distal forelimb representation. After tangential sectioning, the distribution of BDA‐labeled cell bodies and terminal boutons was documented. In M1, labeling followed a rostrolateral pattern, largely leaving the caudomedial M1 unlabeled. Quantification of somata and terminals showed that two areas share major connections with PMv: M1 and frontal areas immediately rostral to PMv, designated as frontal rostral area (FR). Connections with this latter region have not been described previously. Moderate connections were found with PMd, SMA, anterior operculum, and posterior operculum/inferior parietal area. Minor connections were found with diverse areas of the precentral and parietal cortex, including S1. No statistical difference between the proportions of inputs and outputs for any location was observed, supporting the reciprocity of PMv intracortical connections. J. Comp. Neurol. 495:374–390, 2006. © 2006 Wiley‐Liss, Inc.     

Topographical projections of the cerebral cortex to the subthalamic nucleus

Corticosubthalamic projections in the rat were investigated using the autoradiographic anterograde axonal tracing technique. After unilateral injections of tritiated amino acids in the cerebral cortex, projections to the ipsilateral subthalamic nucleus (STH) could be found arising only from the frontal agranular cortex and the zone of MI-SI overlap. Injections into granular areas of the cortex (e.g., somatosensory and visual areas) did not result in labeling in STH. Following injections in the frontal agranular cortex, labeling was present in the ipsilateral but not the contralateral STH. In general, injections that involved the lateral agranular field of frontal cortex, as defined by Donoghue and Wise ('82), resulted in a greater amount of labeling in STH than injections within the medial agranular area or the zone of MI-SI overlap. The projection from the frontal agranular areas to STH is topographically organized. The rostral part of the lateral agranular cortex projects to the lateral portion of the rostral two-thirds of STH, and the caudal part of this field projects to the ventral aspect of the middle third of STH. Injections in the rostral part of the medial agranular cortex resulted in labeling throughout the ventral two-thirds of the medial half of STH. The caudal part of the medial agranular cortex projects to the dorsolateral part of the caudal two-thirds of STH. The present results reveal projections from only the frontal agranular cortex and the zone of MI-SI overlap to STH in the rat. The cortico-STH projection is ipsilateral and terminates in a topographical manner in all parts of STH.     

Architecture and frontal cortical connections of the premotor cortex (area 6) in the rhesus monkey

The premotor cortex (area 6) has several architectonic sectors that can be delineated on the basis of cytoarchitectonic and myeloarchitectonic features. Area 6 may be broadly subdivided into a dorsal and a ventral sector at the spur of the arcuate sulcus. Dorsal 6 lacks a granular layer IV, but ventral 6 has an emergent layer IV that separates laminae III and V. Dorsal 6 has a higher myelin content than ventral 6. Dorsal area 6 is further subdivided into a caudal and a rostral sector on the basis of the presence of large pyramidal cells in the caudal but not in the rostral sector. The rostral sector of area 6 can be subdivided into a medial region distinguished from a more laterally situated area by the presence of more compact and darkly stained cells in layers III and V. Ventral area 6 can be subdivided into an upper and lower division. The upper part has more prominent pyramidal cells in layers III and V, and a better developed outer Baillarger band and vertical plexus than the lower division. The efferent and afferent connections of area 6 were studied with anterograde and retrograde tracers. The frontal connections of dorsal area 6 are restricted to neighboring dorsal frontal regions. Only the caudal sector of dorsal area 6 is connected with the motor cortex. In contrast, ventral area 6 is not only connected with the prefrontal cortex, but also directly with the motor cortex, the parainsular gustatory area, and with somatosensory areas in the frontal operculum. The widespread connections of ventral area 6 may be related to the specialization of the head, neck, and face structures that are represented ventrally within the premotor cortex.