Relationship between the corticostriatal terminals from areas 9 and 46, and those from area 8A, dorsal and rostral premotor cortex and area 24c: an anatomical substrate for cognition to action

Our previous data indicate that there are specific features of the corticostriatal pathways from the prefrontal cortex. First, corticostriatal pathways are composed of focal, circumscribed projections and of diffuse, widespread projections. Second, there is some convergence between terminal fields from different functional regions of the prefrontal cortex. Third, anterior cingulate projections from area 24b occupy a large region of the rostral striatum. The goal of this study was to determine whether these features are also common to the corticostriatal projections from area 8A (including the frontal eye field; FEF), the supplementary eye field (SEF), dorsal and rostral premotor cortex (PMdr) and area 24c. Using a new approach of three-dimensional reconstruction of the corticostriatal pathways, along with dual cortical tracer injections, we mapped the corticostriatal terminal fields from areas 9 and 46, 8A-FEF, SEF, PMdr and 24b and c. In addition, we placed injections of retrogradely transported tracers into key striatal regions. The results demonstrated that: (i) a diffuse projection system is a common feature of the corticostriatal projections from different frontal regions; (ii) key striatal regions receive convergent projections from areas 9 and 46 and from areas 8A-FEF, SEF, PMdr and 24c, suggesting a potential pivotal role of these striatal regions in integrating cortical information; (iii) projections from area 24c, like those from area 24b, terminate widely throughout the striatum, interfacing with terminals from several frontal areas. These features of the corticostriatal frontal pathways suggest a potential integrative striatal network for learning.     

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.     

Projections of the claustrum to the primary motor,premotor, and prefrontal cortices in the macaque monkey

The claustrum is interconnected with the frontal lobe, including the motor cortex, prefrontal cortex, and cingulate cortex. The goal of the present study was to assess whether the claustral projections to distinct areas within the frontal cortex arise from separate regions within the claustrum. Multiple injections of tracers were performed in 15 macaque monkeys, aimed toward primary motor area (M1), pre-supplementary motor area (pre-SMA), SMA-proper, rostral (PMd-r) and caudal (PMd-c) parts of the dorsal premotor cortex (PM), rostral (PMv-r) and caudal (PMv-c) parts of the ventral PM, and superior and inferior parts of area 46. The distribution of retrogradely labeled neurons showed no clear segregation along the rostrocaudal axis of the claustrum; they were usually located along the entire anteroposterior extent of the claustrum. For all motor cortical areas, there was a general trend of the labeled neurons to occupy the dorsal and intermediate parts of the claustrum along the dorsoventral axis. The same territories were labeled after injection in area 46, but in addition numerous labeled neurons were found in the most ventral part of the claustrum. At higher resolution, however, there was clear evidence that the territories projecting to pre-SMA and SMA-proper formed separate, interdigitating, clusters along the dorsoventral axis. A comparable local segregation was observed for the two subdivisions of area 46, whereas there was more local overlap among the subareas of PM. The projections from the claustrum to the multiple subareas of the motor cortex and to area 46 arise from largely overlapping territories, with, however, some degree of local segregation.     

Thalamocortical and intracortical connections of monkey cingulate motor areas

Although there has been an increasing interest in motor functions of the cingulate motor areas, data concerning their input organization are still limited. To address this issue, the patterns of thalamic and cortical inputs to the rostral (CMAr), dorsal (CMAd), and ventral (CMAv) cingulate motor areas were investigated in the macaque monkey. Tracer injections were made into identified forelimb representations of these areas, and the distributions of retrogradely labeled neurons were analyzed in the thalamus and the frontal cortex. The cells of origin of thalamocortical projections to the CMAr were located mainly in the parvicellular division of the ventroanterior nucleus and the oral division of the ventrolateral nucleus (VLo). On the other hand, the thalamocortical neurons to the CMAd/CMAv were distributed predominantly in the VLo and the oral division of the ventroposterolateral nucleus-the caudal division of the ventrolateral nucleus. Additionally, many neurons in the intralaminar nuclear group were seen to project to the cingulate motor areas. Except for their well-developed interconnections, the corticocortical projections to the CMAr and CMAd/CMAv were also distinctively preferential. Major inputs to the CMAr arose from the presupplementary motor area and the dorsal premotor cortex, whereas inputs to the CMAd/CMAv originated not only from these areas but also from the supplementary motor area and the primary motor cortex. The present results indicate that the CMAr and the caudal cingulate motor area (involving both the CMAd and the CMAv) are characterized by distinct patterns of thalamocortical and intracortical connections, reflecting their functional differences.     

Converging evidence from microstimulation, architecture, and connections for multiple motor areas in the frontal and cingulate cortex of prosimian primates

In the present study, somatotopic organization, architectonic features, and patterns of connections were used to define motor areas in the frontal and cingulate cortex of the prosimian primate Galago garnetti. Sites throughout portions of the motor cortex were electrically stimulated with microelectrodes at the approximate depth of layer V. In some of the same animals, injections in primary motor cortex (M1), and in the spinal cord, revealed patterns of connections with physiologically identified motor areas. Results were related to cortical architecture in brain sections processed for Nissl, myelin, cytochrome oxidase, acetylcholinesterase, or neurofilaments. Evidence was obtained for a number of fields previously identified in simian primates, including M1, dorsal premotor field with caudal (PMDc) and rostral (PMDr) divisions, ventral premotor area (PMV), supplementary motor area (SMA), presupplementary motor area (pre-SMA), frontal eye field (FEF), and cingulate motor areas, CMAr and CMAc located rostrally and caudally, respectively. In addition, we distinguished area 6Ds of Preuss and Goldman-Rakic (1991a) between PMV and PMDc, and a more posterior cingulate sensorimotor area (CSMA) with motor connections that may correspond to the supplementary sensory area of monkeys. Areas M1, SMA, PMDc, PMV, CMAr, CMAc, and CSMA projected to the spinal cord, while all of these areas and 6Ds projected to M1. Although area M1 had the lowest stimulation thresholds for evoked movements, movements were also evoked from the other motor areas, as well as from somatosensory areas 3a and 3b. These results indicate that prosimian galagos have a complex of motor areas that closely resembles that in monkeys and suggest that at least 10 motor fields emerged early in primate evolution.     

Corticostriatal and corticosubthalamic input zones from the presupplementary motor area in the macaque monkey: comparison with the input zones from the supplementary motor area

The presupplementary motor area (pre-SMA) is a cortical motor-related area which lies in the medial wall of the frontal lobe, immediately anterior to the supplementary motor area (SMA). This area has been considered to participate in the control of complex forelimb movements in a way different from the SMA. In an attempt to analyze the patterns of projections from the pre-SMA to the basal ganglia, we examined the distributions of pre-SMA inputs in the striatum and the subthalamic nucleus and compared them with the SMA input distributions. To detect morphologically the terminal fields from the pre-SMA and the forelimb region of the SMA, anterograde tracers were injected into such areas that had been identified electrophysiologically in the macaque monkey. Corticostriatal inputs from the pre-SMA were distributed mainly in the striatal cell bridges connecting the rostral aspects of the caudate nucleus and the putamen, as well as in their neighboring striatal portions. These input zones were located, with no substantial overlap, rostral to corticostriatal input zones from the SMA forelimb region. Corticosubthalamic input zones from the pre-SMA were almost localized in the medial aspect of the nucleus, where corticosubthalamic inputs from the SMA forelimb region were also distributed predominantly. However, the major terminal fields from the pre-SMA were centered ventrally to those from the SMA. The present results indicate that the corticostriatal and corticosubthalamic input zones from the pre-SMA appear to be segregated from the SMA-derived input zones. This implies the possibility of parallel processing of motor information from the pre-SMA and SMA in the cortico-basal ganglia circuit.     

Comparison of neuronal activity in the rostral supplementary and cingulate motor areas during a task with cognitive and motor demands

A number of cortical motor areas have been identified on the medial wall of the hemisphere in monkeys. However, their specific role in motor control remains unclear. In this study, we sought to describe and compare the functional properties of the presupplementary (pre-SMA) and rostral cingulate (CMAr) motor areas in two monkeys performing a visually instructed, delayed, sequential movement. We recorded 134 task-related neurons in the pre-SMA and 149 in the CMAr. The main difference between the two areas was the abundance of responses to targets (46%) in the pre-SMA, while CMAr activity was more related to reward (28%). Neuronal responses to targets were more phasic and higher in frequency in the pre-SMA than in the CMAr. During the delay, the percentage of neuronal responses was similar in the two areas. The discharge pattern was different depending upon whether the delay duration was fixed or variable but in most neurons was the same regardless of the sequence performed. Movement-related changes were common in the pre-SMA (75%) and in the CMAr (81%) but they occurred earlier in the former. Neurons activated exclusively during movement were more numerous in the CMAr. Finally, neuronal activity in the pre-SMA was more related to the sequential aspect of the task compared to the CMAr. Our results suggest that although the two areas share functional properties, they also participate in different aspects of motor behaviour. Their functional properties reflect their anatomical positions, which give them the potential to integrate external stimuli (pre-SMA) and internal states (CMAr) during motor planning.     

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.     

Origin of thalamic inputs to the primary, premotor, and supplementary motor cortical areas and to area 46 in macaque monkeys: a multiple retrograde tracing study.

The origin of thalamic inputs to distinct motor cortical areas was established in five monkeys to determine whether the motor areas receive inputs from a common thalamic nucleus and the extent to which the territories of origin overlap. To not rely on the rough definition of cytoarchitectonic boundaries in the thalamus, monkeys were subjected to multiple injections of tracers (four to seven) in the primary (M1), premotor (PM), and supplementary (SMA) motor cortical areas and in area 46. The cortical areas were distributed into five groups, each receiving inputs from a specific set of thalamic nuclei: 1) M1; 2) SMA-proper and the caudal part of the dorsal PM (PMdc); 3) the rostral and caudal parts of the ventral PM (PMvr and PMvc); 4) the rostral part of the dorsal PM (PMdr); and 5) the superior and inferior parts of area 46 (area 46sup and area 46inf). A major degree of overlap was obtained for the origins of the thalamocortical projections directed to areas 46inf and 46sup and for those terminating in SMA-proper and PMdc. PMvc and PMvr received inputs from adjacent and/or common thalamic regions. In contrast, the degree of overlap between M1 and SMA was smaller. The projection to M1 shared relatively limited zones of origin with the projections directed to PM. Thalamic inputs to the motor cortical areas (M1, SMA, PMd, and PMv), in general, were segregated from those directed to area 46, except in the mediodorsal nucleus, in which there was clear overlap of the territories sending projections to area 46, SMA-proper, and PMdc.     

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.     

Identification of multiple nonprimary motor cortical areas with simple movements

The human cortex reportedly contains at least five nonprimary motor areas: in the frontolateral convexity, the dorsal and ventral premotor cortex (PMd and PMv), and in the frontomesial wall, the presupplementary and supplementary motor areas (pre-SMA and SMA), and the rostral, dorsal and ventral cingulate areas (CMAr, CMAd, and CMAv). Activation of these regions in neuroimaging studies has been generally associated either with the performance of complex motor tasks or with reorganization occurring with motor recovery in the presence of pathology. Recent evidence from neuroimaging studies suggests that the same areas are activated with well controlled simple movements in healthy subjects providing support to the observation that their contribution may be more quantitative rather than exclusively specific to a certain aspect of motor behaviour. An important consequence of this observation is that activation of multiple nonprimary motor areas during simple motor tasks should not be considered unique to patients with upper or lower motoneuron lesions but rather as a normal physiological process.     

Origins of callosal projections to the supplementary motor area (SMA): a direct comparison between pre-SMA and SMA-proper in macaque monkeys.

The two subdivisions of the supplementary motor area (SMA), the pre-SMA (rostrally) and SMA-proper (caudally), exhibit distinct functional properties and clear differences with respect to their connectivity with the spinal cord, the thalamus, and other homolateral motor cortical areas. The goal of the present study was to establish in monkeys whether these subdivisions also differ with regard to their callosal connectivity. Two fluorescent retrograde tracers (Fast Blue and Diamidino Yellow) were injected in each animal, one in the pre-SMA and the second in the SMA-proper. Tracer injections in the pre-SMA or in SMA-proper resulted in significant numbers of labeled neurons in the opposite SMA, premotor cortex (PM), cingulate motor areas (CMA), and cingulate gyrus. Labeled neurons in M1 were rare, being observed only after injection in the SMA-proper. The two subdivisions of the SMA differed in the proportion of labeled neurons found across areas providing their callosal inputs. The SMA-proper receives about half of its callosal inputs from its counterpart in the other hemisphere (42-65% across monkeys). A comparable proportion of neurons was found in the pre-SMA after injection in the opposite pre-SMA (32-47%). The pre-SMA receives more callosal inputs from the rostral halves of the dorsal PM, the ventral PM, and the CMA than from their caudal halves. In addition, the pre-SMA, but not the SMA-proper, receives callosal inputs from the prefrontal cortex. The SMA-proper receives more callosal inputs from the caudal halves of the dorsal PM and ventral PM than from their rostral halves. The two subdivisions of the SMA receive callosal inputs from the same cortical areas (except the prefrontal cortex and M1), but they differ with respect to the quantitative contribution of each area of origin. In conclusion, quantitative data now support the notion that pre-SMA receives more transcallosal inputs than the SMA-proper.     

Motor-related functional subdivisions of human lateral premotor cortex: epicortical recording in conditional visuomotor task.

OBJECTIVE: To clarify the functional subdivisions of the human lateral premotor cortex (PM) in the visuomotor control. METHODS: Event-related potentials (ERPs) were epicortically recorded from PM in 5 epilepsy patients. S1-Go/NoGo choice delayed reaction time (RT), S1-warned S2-Go simple RT and control fixation paradigms were compared using paired visual stimuli (S1, S2). RESULTS: Signal-related activity peaked at 176-194 ms after S1 in the ventrorostral PM (PMvr) in all 3 paradigms, indicating its role in signal perception. Early set-related activity was recorded with its peak <810 ms after S1 in the dorsorostral PM (PMdr) and was larger in the choice than in the simple RT paradigm, suggesting its role in signal selection. Its cognitive component was recorded as surface-positive transients at PMdr, while its motoric aspect, seen as negative transients, extended to the caudal PM. Late sustained set-related activity was observed in preparation for hand movement in the caudal PM at the hand and face positive motor areas. After presentation of S2, movement-related activity was observed at the hand sensorimotor area for motor execution, following the signal-related activity at PMvr. CONCLUSIONS: The present ERP study suggests the temporally sequential representation of predominantly 'cognitive' function in the rostral PM and 'motor' function in the caudal PM. SIGNIFICANCE: The rostrocaudal cognitive-motor gradient was demonstrated in the lateral premotor cortex in humans by means of an epicortical ERP approach.     

Frontal granular cortex input to the cingulate (M3), supplementary (M2) and primary (M1) motor cortices in the rhesus monkey

Although frontal lobe interconnections of the primary (area 4 or M1) and supplementary (area 6m or M2) motor cortices are well understood, how frontal granular (or prefrontal) cortex influences these and other motor cortices is not. Using fluorescent dyes in rhesus monkeys, we investigated the distribution of frontal lobe inputs to M1, M2, and the cingulate motor cortex (area 24c or M3, and area 23c). M1 received input from M2, lateral area 6, areas 4C and PrCO, and granular area 12. M2 received input from these same areas as well as M1; granular areas 45, 8, 9, and 46; and the lateral part of the orbitofrontal cortex. Input from the ventral part of lateral area 6, area PrCO, and frontal granular cortex targeted only the ventral portion of M1, and primarily the rostral portion of M2. In contrast, M3 and area 23c received input from M1, M2; lateral area 6 and area 4C; granular areas 8, 12, 9, 46, 10, and 32; as well as orbitofrontal cortex. Only M3 received input from the ventral part of lateral area 6 and areas PrCO, 45, 12vl, and the posterior part of the orbitofrontal cortex. This diversity of frontal lobe inputs, and the heavy component of prefrontal input to the cingulate motor cortex, suggests a hierarchy among the motor cortices studied. M1 receives the least diverse frontal lobe input, and its origin is largely from other agranular motor areas. M2 receives more diverse input, arising primarily from agranular motor and prefrontal association cortices. M3 and area 23c receive both diverse and widespread frontal lobe input, which includes agranular motor, prefrontal association, and frontal limbic cortices. These connectivity patterns suggest that frontal association and frontal limbic areas have direct and preferential access to that part of the corticospinal projection which arises from the cingulate motor cortex. © 1993 Wiley-Liss,Inc.     

Multisynaptic projections from the ventrolateral prefrontal cortex to the dorsal premotor cortex in macaques – anatomical substrate for conditional visuomotor behavior

Lines of evidence indicate that both the ventrolateral prefrontal cortex (vlPFC) (areas 45/12) and dorsal premotor cortex (PMd) (rostral F2 in area 6) are crucially involved in conditional visuomotor behavior, in which it is required to determine an action based on an associated visual object. However, virtually no direct projections appear to exist between the vlPFC and PMd. In the present study, to elucidate possible multisynaptic networks linking the vlPFC to the PMd, we performed a series of neuroanatomical tract‐tracing experiments in macaque monkeys. First, we identified cortical areas that send projection fibers directly to the PMd by injecting Fast Blue into the PMd. Considerable retrograde labeling occurred in the dorsal prefrontal cortex (dPFC) (areas 46d/9/8B/8Ad), dorsomedial motor cortex (dmMC) (F7 and presupplementary motor area), rostral cingulate motor area, and ventral premotor cortex (F5 and area 44), whereas the vlPFC was virtually devoid of neuronal labeling. Second, we injected the rabies virus, a retrograde transneuronal tracer, into the PMd. At 3 days after the rabies injections, second‐order neurons were labeled in the vlPFC (mainly area 45), indicating that the vlPFC disynaptically projects to the PMd. Finally, to determine areas that connect the vlPFC to the PMd indirectly, we carried out an anterograde/retrograde dual‐labeling experiment in single monkeys. By examining the distribution of axon terminals labeled from the vlPFC and cell bodies labeled from the PMd, we found overlapping labels in the dPFC and dmMC. These results indicate that the vlPFC outflow is directed toward the PMd in a multisynaptic fashion through the dPFC and/or dmMC.     

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.     

Corpus callosum connections of subdivisions of motor and premotor cortex, and frontal eye field in a prosimian primate, Otolemur garnetti

The callosal connections of motor and premotor fields in the frontal cortex of galagos were examined by placing multiple tracers into the primary motor area (M1), dorsal premotor area (PMD), ventral premotor area (PMV), supplementary motor area (SMA), and frontal eye field (FEF) following intracortical microstimulation. Retrogradely labeled neurons in the opposite hemisphere were plotted and superimposed onto brain sections stained with myelin and cytochrome oxidase for architectonic analysis. The main callosal connections of M1 and the caudal portion of PMD (PMDc) were with homotopic sites, and the major callosal connections of the rostral portion of PMD (PMDr), SMA, and FEF were with homotopic sites and adjoining cortex in the frontal lobe. In addition, M1 forelimb representation had sparse callosal connections, whereas M1 trunk and face representations, as well as the premotor areas, had dense callosal connections. The sparse interhemispheric connections of the forelimb sector of M1 suggests that the control of each forelimb is largely from the contralateral M1 in galagos, as in other primates.     

Cortical connections of the frontoparietal opercular areas in the Rhesus monkey

The connections of the frontoparietal opercular areas were studied in rhesus monkeys by using antero- and retrograde tracer techniques. The rostral opercular cortex including the gustatory and proisocortical motor (ProM) areas is connected with precentral areas 3, 1, and 2 as well as with the rostral portion of the opercular area which resembles the second somatosensory type of cortex (area SII) and the ventral portion of area 6. Its distant connections are with the ventral portion of prefrontal areas 46, 11, 12, and 13 as well as with the rostral insula and cingulate motor area (CMAr). The mid opercular region (areas 1 and 2) is connected with pre- and postcentral areas 3, 1, and 2 as well as SII. Additionally, it is connected with the ventral portion of area 6, area 44, area ProM, the gustatory area, and the rostral insula. Its distant connections are with area 4, the ventral portion of area 46, area 7b, and area POa in the intraparietal sulcus (IPS). The rostral parietal opercular region is connected with the postcentral portions of areas 3, 1, and 2; areas 5, 7, and SII; the gustatory area; and the vestibular area. Its other connections are with area 4, area 44, the ventral portion of area 46, area ProM, CMAr, and the supplementary motor area (SMA). The caudal opercular region is connected with the dorsal portion of area 3; areas 2, 5, and 7a; and areas PEa as well as IPd of IPS. It is also connected with area SII, insula, and the superior temporal sulcus. Its distant connections are with area 44; the dorsal portion of area 8 and the ventral portion of area 46; as well as CMAr, SMA, and the supplementary sensory area. This connectivity suggests that the ventral somatosensory areas are involved in sensorimotor activities mainly related to head, neck, and face structures as well as to taste. Additionally, these areas may have a role in frontal (working) and temporal (tactile) memory systems. J. Comp. Neurol. 403:431–458, 1999. © 1999 Wiley-Liss, Inc.     

Corticocortical connections of area F3 (SMA-proper) and area F6 (pre-SMA) in the macaque monkey

The monkey mesial area 6 comprises two distinct cytoarchitectonic areas: F3 [supplementary motor area properly defined (SMA-proper)], located caudally, and F6 (pre-SMA), located rostrally. The aim of the present study was to describe the corticocortical connections of these two areas. To this purpose restricted injections of neuronal tracers (wheat germ-agglutinin conjugated to horseradish peroxidase, fluorescent tracers) were made in different somatotopic fields of F3, F6, and F1 (area 4) and their transport plotted. The results showed that F3 and F6 differ markedly in their cortical connections. F3 is richly linked with F1 and the posterior premotor and cingulate areas (F2, F4, 24d). Connections with the anterior premotor and cingulate areas (F6, F7, F5, 24c) although present, are relatively modest. There is no input from the prefrontal lobe. F3 is also connected with several postrolandic cortical areas. These connections are with areas PC, PE, and PEa in the superior parietal lobule, cingulate areas 23 and PEci, the opercular parietal areas (PFop, PGop, SII) and the granular insula. F6 receives a rich input from the anterior premotor areas (especially F5) and cingulate area 24c, whereas its input from the posterior premotor and cingulate areas is very weak. A strong input originates from area 46. There are no connections with F1. The connections with the postrolandic areas are extremely meagre. They are with areas PG and PFG in the inferior parietal lobule, the disgranular insula, and the superior temporal sulcus. A further result was the demonstration of a differential connectivity pattern of the cingulate areas 24d and 24c. Area 24d is strongly linked with F1 and F3, whereas area 24c is connected mostly with F6. The present data support the notion that the classical SMA comprises two functionally distinct areas. They suggest that F6 (the rostral area) is responsible for the “SMA” so-called high level motor functions, whereas F3 (the caudal area) is more closely related to movement execution. © 1993 Wiley-Liss, Inc.     

Organization of anterior cingulate and frontal cortical projections to the retrosplenial cortex in the rat

The retrosplenial cortex (areas 29a-d), which plays an important role in spatial memory and navigation, is known to provide massive projections to frontal association and motor cortices, which are also essential for spatial behavior. The reciprocal projections originating from these frontal cortices to areas 29a-d, however, have been analyzed to only a limited extent. Here, we report an analysis of the anatomical organization of projections from anterior cingulate area 24 and motor and prefrontal cortices to areas 29a-d in the rat, using the axonal transport of cholera toxin B subunit and biotinylated dextran amine. Area 29a receives projections from rostral area 24a, area 24b, the ventral orbital area, and the caudal secondary motor area. Rostral area 29b receives projections from caudal area 24a, whereas caudal area 29b receives projections from rostral area 24a. Area 29b also receives projections from area 24b and the ventral orbital area. Areas 29c and 29d receive projections from areas 24a and 24b and the secondary motor area in a topographic manner such that the rostrocaudal axis of areas 29c and 29d corresponds to the caudorostral axis of areas 24a and 24b and the secondary motor area. Rostral areas 29c and 29d also receive projections from the caudal primary motor area, and area 29d receives projections from the ventral, lateral, and medial orbital areas. These differential frontal cortical projections to each area of the retrosplenial cortex suggest that each area may contribute to different aspects of retrosplenial cortical function such as spatial memory and behavior.