Corticobulbar projections from distinct motor cortical areas to the reticular formation in macaque monkeys

Fregosi, Michela; Contestabile, Alessandro; Hamadjida, Adjia; Rouiller, Eric M.

doi:10.1111/ejn.13576

Cited by 78 publications

(117 citation statements)

References 86 publications

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“…In PM, the BDA injections covered most of the targeted areas (see Fregosi et al ., ), namely PMd in Mk‐R12 and PMd/PMv in the other two monkeys (Mk‐R13 and Mk‐CH). In M1, in two monkeys (Mk‐Z182 and Mk‐M310), BDA was injected in absence of ICMS (based on sulci) in territories including most likely the hand and the arm territories; In Mk‐M93‐80, BDA was injected in the hand area delineated with ICMS.…”

Section: Methodsmentioning

confidence: 97%

“…The individual properties of these nine macaques are listed in Table . The BDA injection sites were illustrated for the seven cases used in the recent study of the corticobulbar projection (Fregosi et al ., ). The injection site of the additional monkey with BDA deposited in SMA‐proper has been illustrated previously as well (Tanné‐Gariépy et al ., ; their fig.…”

Section: Methodsmentioning

confidence: 97%

“…BDA, biotinylated dextran amine; ICMS, intracortical microstimulation; PM, Premotor cortex; PMv, ventral premotor cortex; SC, Superior Colliculus; SCint, intermediate nucleus of SC; SCdeep, deep nucleus of SC; Fasc., Macaca fascicularis ; Mul., Macaca mulatta .In the top row, the IDs of monkeys are as in Fregosi et al . () for seven of them (seven left most columns), with two newly inserted monkeys (two rightmost columns). The second row gives original IDs used in the laboratory, as well as in earlier reports.…”

Section: Methodsmentioning

confidence: 99%

“…Sections of the brain (including the midbrain) were cut at 50 μm in the frontal plane using a freezing microtome and collected in 5–8 series (see Table ). One series of sections was processed to visualize BDA (Rouiller et al ., ), and sections of this series including the SC were analysed using Neurolucida software (version 11; MicroBrightField Inc.) on an Olympus light microscope interfaced with a computer (see Fregosi et al ., for detail). The analysed intersection intervals ranged from 250 to 400 μm (Table ).…”

Section: Methodsmentioning

confidence: 99%

“…The motor cortical areas also influence other descending pathways via their corticobulbar (or corticoreticular), corticorubral and corticotectal projections (Kuypers, ; Lemon, , ). In a recent study (Fregosi et al ., ), the corticobulbar projection was characterized in intact adult macaque monkeys by visualizing the axonal boutons in the Ponto‐Medullary Reticular Formation (PMRF) labelled with injections of the anterograde tracer biotinylated dextran amine (BDA) in either the primary motor cortex (M1), the premotor cortex (PM) or the supplementary motor area (SMA). The non‐primary motor areas (PM and SMA) exhibited a stronger corticobulbar projection than that originating from M1 (Fregosi et al ., ).…”

Section: Introductionmentioning

confidence: 99%

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Ipsilateral corticotectal projections from the primary, premotor and supplementary motor cortical areas in adult macaque monkeys: a quantitative anterograde tracing study

Fregosi

Rouiller

2017

Eur J of Neuroscience

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The corticotectal projection from cortical motor areas is one of several descending pathways involved in the indirect control of spinal motoneurons. In non-human primates, previous studies reported that cortical projections to the superior colliculus (SC) originated from the premotor cortex (PM) and the primary motor cortex, whereas no projection originated from the supplementary motor area (SMA). The aim of the present study was to investigate and compare the properties of corticotectal projections originating from these three cortical motor areas in intact adult macaques (n = 9). The anterograde tracer biotinylated dextran amine was injected into one of these cortical areas in each animal. Individual axonal boutons, both en passant and terminaux, were charted and counted in the different layers of the ipsilateral SC. The data confirmed the presence of strong corticotectal projections from the PM. A new observation was that strong corticotectal projections were also found to originate from the SMA (its proper division). The corticotectal projection from the primary motor cortex was quantitatively less strong than that from either the premotor or SMAs. The corticotectal projection from each motor area was directed mainly to the deep layer of the SC, although its intermediate layer was also a consistent target of fairly dense terminations. The strong corticotectal projections from non-primary motor areas are in position to influence the preparation and planning of voluntary movements.

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Section: Methodsmentioning

confidence: 97%

Section: Methodsmentioning

confidence: 97%

Section: Methodsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Ipsilateral corticotectal projections from the primary, premotor and supplementary motor cortical areas in adult macaque monkeys: a quantitative anterograde tracing study

Fregosi

Rouiller

2017

Eur J of Neuroscience

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Extensive somatosensory and motor corticospinal sprouting occurs following a central dorsal column lesion in monkeys

Fisher

Lilak

Garner

et al. 2018

J of Comparative Neurology

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The corticospinal tract (CST) forms the major descending pathway mediating voluntary hand movements in primates, and originates from ∼nine cortical subdivisions in the macaque. While the terminals of spared motor CST axons are known to sprout locally within the cord in response to spinal injury, little is known about the response of the other CST subcomponents. We previously reported that following a cervical dorsal root lesion (DRL), the primary somatosensory (S1) CST terminal projection retracts to 60% of its original terminal domain, while the primary motor (M1) projection remains robust (Darian-Smith et al., J. Neurosci., 2013). In contrast, when a dorsal column lesion (DCL) is added to the DRL, the S1 CST, in addition to the M1 CST, extends its terminal projections bilaterally and caudally, well beyond normal range (Darian-Smith et al., J. Neurosci., 2014). Are these dramatic responses linked entirely to the inclusion of a CNS injury (i.e., DCL), or do the two components summate or interact? We addressed this directly, by comparing data from monkeys that received a unilateral DCL alone, with those that received either a DRL or a combined DRL/DCL. Approximately 4 months post-lesion, the S1 hand region was mapped electrophysiologically, and anterograde tracers were injected bilaterally into the region deprived of normal input, to assess spinal terminal labeling. Using multifactorial analyses, we show that following a DCL alone (i.e., cuneate fasciculus lesion), the S1 and M1 CSTs also sprout significantly and bilaterally beyond normal range, with a termination pattern suggesting some interaction between the peripheral and central lesions.

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Terminal organization of the corticospinal projection from the arm/hand region of the rostral primary motor cortex (M1r or old M1) to the cervical enlargement (C5–T1) in rhesus monkey

Morecraft,

Ge,

Stilwell‐Morecraft

et al. 2023

J of Comparative Neurology

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High‐resolution anterograde tracers and stereology were used to study the terminal organization of the corticospinal projection (CSP) from the rostral portion of the primary motor cortex (M1r) to spinal levels C5–T1. Most of this projection (90%) terminated contralaterally within laminae V–IX, with the densest distribution in lamina VII. Moderate bouton numbers occurred in laminae VI, VIII, and IX with few in lamina V. Within lamina VII, labeling occurred over the distal‐related dorsolateral subsectors and proximal‐related ventromedial subsectors. Within motoneuron lamina IX, most terminations occurred in the proximal‐related dorsomedial quadrant, followed by the distal‐related dorsolateral quadrant. Segmentally, the contralateral lamina VII CSP gradually declined from C5–T1 but was consistently distributed at C5–C7 in lamina IX. The ipsilateral CSP ended in axial‐related lamina VIII and adjacent ventromedial region of lamina VII. These findings demonstrate the M1r CSP influences distal and proximal/axial‐related spinal targets. Thus, the M1r CSP represents a transitional CSP, positioned between the caudal M1 (M1c) CSP, which is 98% contralateral and optimally organized to mediate distal upper extremity movements (Morecraft et al., 2013), and dorsolateral premotor (LPMCd) CSP being 79% contralateral and optimally organized to mediate proximal/axial movements (Morecraft et al., 2019). This distal to proximal CSP gradient corresponds to the clinical deficits accompanying caudal to rostral motor cortex injury. The lamina IX CSP is considered in the light of anatomical and neurophysiological evidence which suggests M1c gives rise to the major proportion of the cortico‐motoneuronal (CM) projection, while there is a limited M1r CM projection.

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Corticobulbar projections from distinct motor cortical areas to the reticular formation in macaque monkeys

Cited by 78 publications

References 86 publications

Ipsilateral corticotectal projections from the primary, premotor and supplementary motor cortical areas in adult macaque monkeys: a quantitative anterograde tracing study

Ipsilateral corticotectal projections from the primary, premotor and supplementary motor cortical areas in adult macaque monkeys: a quantitative anterograde tracing study

Extensive somatosensory and motor corticospinal sprouting occurs following a central dorsal column lesion in monkeys

Terminal organization of the corticospinal projection from the arm/hand region of the rostral primary motor cortex (M1r or old M1) to the cervical enlargement (C5–T1) in rhesus monkey

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