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

Tokuno, Hironobu; Takada, Masahiko; Nambu, Atsushi; Inase, Masahiko

doi:10.1002/(sici)1096-9861(19971208)389:1<34::aid-cne3>3.0.co;2-f

Cited by 66 publications

(41 citation statements)

References 52 publications

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“…2), which were representative of sulcal and gyral locations in many other regions of the cortex. Although previous macaque anatomical studies have shown that each of these cortical positions gives rise to long-range axonal projections (9,28,(43)(44)(45)(46)(47), we found that the resulting track lines in most cases failed to escape the local white matter environment. In fact, of the four seeds shown in this example only seed 2, on the precentral gyrus, extended beyond the superficial association fibers and into the deeper white matter.…”

Section: Resultscontrasting

confidence: 80%

Superficial white matter fiber systems impede detection of long-range cortical connections in diffusion MR tractography

Reveley

Seth

Pierpaoli

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

414

399

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In vivo tractography based on diffusion magnetic resonance imaging (dMRI) has opened new doors to study structure-function relationships in the human brain. Initially developed to map the trajectory of major white matter tracts, dMRI is used increasingly to infer long-range anatomical connections of the cortex. Because axonal projections originate and terminate in the gray matter but travel mainly through the deep white matter, the success of tractography hinges on the capacity to follow fibers across this transition. Here we demonstrate that the complex arrangement of white matter fibers residing just under the cortical sheet poses severe challenges for long-range tractography over roughly half of the brain. We investigate this issue by comparing dMRI from very-high-resolution ex vivo macaque brain specimens with histological analysis of the same tissue. Using probabilistic tracking from pure gray and white matter seeds, we found that ∼50% of the cortical surface was effectively inaccessible for long-range diffusion tracking because of dense white matter zones just beneath the infragranular layers of the cortex. Analysis of the corresponding myelin-stained sections revealed that these zones colocalized with dense and uniform sheets of axons running mostly parallel to the cortical surface, most often in sulcal regions but also in many gyral crowns. Tracer injection into the sulcal cortex demonstrated that at least some axonal fibers pass directly through these fiber systems. Current and future high-resolution dMRI studies of the human brain will need to develop methods to overcome the challenges posed by superficial white matter systems to determine long-range anatomical connections accurately. diffusion MRI | tractography | neuroanatomy | white matter | connectome T he primate cerebral cortex consists of dozens of areas distinguished by their cytoarchitectonic profiles (1), sensory maps (2), functional specialization (3), and spontaneous activity covariation (4). Attention within neuroscience has increasingly focused on understanding how connectivity among these regions underpins brain function in health and in disease (5). The macaque monkey (Macaca mulatta) has been a fruitful neuroscientific model because the functional organization of its brain is similar in many ways to that of the human (6-8). Tracer injections in the macaque have revealed that virtually all cortical areas give rise to long-range connections, many of which project to other cortical areas, potentially to form processing hierarchies (9). This understanding continues to shape views of functional organization in the human brain. However, studying long-range connections through tracer injections is time consuming, inefficient, and prone to sampling biases, because a given experiment can measure connectivity to only one or a small number of cortical sites. Moreover, although in many respects the macaque brain is a good approximation of the human brain, both species have undergone profound evolutionary changes since the time of their most recent...

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Section: Resultscontrasting

confidence: 80%

Superficial white matter fiber systems impede detection of long-range cortical connections in diffusion MR tractography

Reveley

Seth

Pierpaoli

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

414

399

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Section: Discussionmentioning

confidence: 99%

“…We speculated that this strong connectivity between the M l face area and CMA may be explained by postulating the ventral part of M l (face area) and CMA to be part of the same circuit, working together with the lateral part of the facial nucleus, to pro vide the lower face motor innervation [Morecraft et al, 2004]. Indeed, studies in nonhuman primates have demon strated that the frontal and cingulate facial areas are selec tively and reciprocally interconnected at the cortical level [Morecraft and Van Hoesen, 1992; Morecraft et al, 1996 Morecraft et al, , 2001 Muakkassa and Strick, 1979;Tokuno et al, 1997].The results of the analysis of our previous motor-related data and those of the meta-analysis were concordant in defining the spatial positions of the upper limb (hand) and lower limb (foot) activations; moreover, they all showed the volume of activation to be bigger for hand rather than foot movement. In the results of the FC analysis of our previous data, as well as in those of the present rs-fMRI study, the center of mass of the foot representation in the medial wall was located more dorsally with respect to the results of the meta-analysis.…”

mentioning

confidence: 99%

Discovering the somatotopic organization of the motor areas of the medial wall using low‐frequency bold fluctuations

Cauda¹,

Geminiani²,

D’Agata³

et al. 2010

Human Brain Mapping

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bstract: This study explored the somatotopy of the motor areas of the medial wall of the cerebral hemisphere, in the human brain. In a sample of 16 healthy participants, we drew 9 regions of interest (ROI) over the primary motor area (M l), each corresponding to a well-known somatic representation. Using functional magnetic resonance imaging, we investigated the resting state functional connectivity between each selected ROI and the motor areas of the medial wall. The main finding was the identifi cation of a rostrocaudal gradient of connectivity in which the more we move from cranial to caudal body representation areas in M l, the more the corresponding connected area in the medial wall is shifted rostrocaudally, confirming the somatotopic schema found in the SMA. We also reanalyzed data obtained in a previous experiment, we performed using hand and foot motor tasks; the reanalysis con sisted in traditional BOLD and functional connectivity analyses. Finally, we performed a meta-analysis of 28 studies of hand and foot motor tasks, mapping their cerebral representations using the tools pro vided by the Brainmap database. All data converge in confirming a somatotopic representation of the medial wall motor areas, with hand representation placed more rostrally and ventrally than that of the foot. Hum Brain Mapp 32:1566Mapp 32: -1579Mapp 32: , 2011 e 2010 W iiey-Liss, inc.Keywords: motor areas; medial wall; supplementary motor area; SMA; cingulate motor areas; resting state; functional connectivity; seed voxel correlation; functional magnetic resonance imaging; fMRI; somatotopy IN T R O D U C T IO NEver since they were first identified, the motor areas of the medial wall have remained, in large part, a mystery. Originally the only recognized motor area in the mesial face of the brain was the supplementary motor area (SMA), located in the medial portion of Brodmann's cytoarchitectonic area 6 [Penfield and Welch, 1951; Woolsey et al., 1952]. This knowledge was derived through electrical stimulation of the cortical surface of the human brain during surgery for brain tumors. We now know of five premotor areas, located in subfields of Brod mann's areas 6, 23, and 24. These premotor areas include the SMA, the pre-SMA [Rizzolatti et a l, 1996;Tanji 1996], and three areas located within the cingulate sulcus-the rostral, dorsal, and ventral cingulate motor areas (CMAr, CM Ad, and CMAv, respectively). The SMA and pre-SMA are located in the dorsomedial frontal cortex, rostrally to the leg representation of the primary motor cortex (M l). The SMA is located caudal to the vertical projection of the commissure, while the pre-SMA lies rostral to this line. The three cingulate motor areas are located within the homonym sulcus: the CMAr and CMAv in the ventral bank of the sulcus and the CMAd in the dorsal bank; each cingulate motor area corresponds to a different cytoarchitectonic field.The somatotopic organization of the motor areas of the medial wall was originally studied in nonhuman primates by observing movements evoked by int...

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“…In macaque monkeys, face-M1 receives corticocortical inputs from the ventral division of the premotor cortex, whose counterpart cortical regions in humans are implicated in speech [37]. In patients with persistent developmental stuttering, the white matter of speech-relevant brain regions in the left motor and premotor regions display abnormal fractional anisotropy values, indicating functional disconnection between speech-relevant brain areas [38].…”

Section: Discussionmentioning

confidence: 99%

Primary face motor area as the motor representation of articulation

et al. 2007

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No clinical data have yet been presented to show that a lesion localized to the primary motor area (M1) can cause severe transient impairment of articulation, although a motor representation for articulation has been suggested to exist within M1. Here we describe three cases of patients who developed severe dysarthria, temporarily mimicking speech arrest or aphemia, due to a localized brain lesion near the left face representation of the human primary motor cortex (face-M1). Speech was slow, effortful, lacking normal prosody, and more affected than expected from the degree of facial or tongue palsy. There was a mild deficit in tongue movements in the sagittal plane that impaired palatolingual contact and rapid tongue movements. The speech disturbance was limited to verbal output, without aphasia or orofacial apraxia. Overlay of magnetic resonance images revealed a localized cortical region near face-M1, which displayed high intensity on diffusion weighted images, while the main portion of the corticobulbar fibers arising from the lower third of the motor cortex was preserved. The cases suggest the existence of a localized brain region specialized for articulation near face-M1. Cortico-cortical fibers connecting face-M1 with the lower premotor areas including Broca's area may also be important for articulatory control.

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

Cited by 66 publications

References 52 publications

Superficial white matter fiber systems impede detection of long-range cortical connections in diffusion MR tractography

Superficial white matter fiber systems impede detection of long-range cortical connections in diffusion MR tractography

Discovering the somatotopic organization of the motor areas of the medial wall using low‐frequency bold fluctuations

Primary face motor area as the motor representation of articulation

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