Different Patterns of Cortical Inputs to Subregions of the Primary Motor Cortex Hand Representation in<i>Cebus apella</i>

Dea, Melvin K.; Hamadjida, Adjia; Elgbeili, Guillaume; Quessy, Stephan; Dancause, Numa

doi:10.1093/cercor/bhv324

Cited by 49 publications

(51 citation statements)

References 69 publications

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“…In keeping with all these observations, our approach provides additional evidence that the spatio-temporal dynamics of motor cortex activation is partly determined by the underlying neural connectivity. It also fits with the idea that the motor cortex is not functionally homogeneous but forms a complex network of interacting subregions (Dea et al, 2016). …”

Section: Discussionsupporting

confidence: 81%

Mapping Horizontal Spread of Activity in Monkey Motor Cortex Using Single Pulse Microstimulation

Hao

Riehle

Brochier

2016

Front. Neural Circuits

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Anatomical studies have demonstrated that distant cortical points are interconnected through long range axon collaterals of pyramidal cells. However, the functional properties of these intrinsic synaptic connections, especially their relationship with the cortical representations of body movements, have not been systematically investigated. To address this issue, we used multielectrode arrays chronically implanted in the motor cortex of two rhesus monkeys to analyze the effects of single-pulse intracortical microstimulation (sICMS) applied at one electrode on the neuronal activities recorded at all other electrodes. The temporal and spatial distribution of the evoked responses of single and multiunit activities was quantified to determine the properties of horizontal propagation. The typical responses were characterized by a brief excitatory peak followed by inhibition of longer duration. Significant excitatory responses to sICMS could be evoked up to 4 mm away from the stimulation site, but the strength of the response decreased exponentially and its latency increased linearly with the distance. We then quantified the direction and strength of the propagation in relation to the somatotopic organization of the motor cortex. We observed that following sICMS the propagation of neural activity is mainly directed rostro-caudally near the central sulcus but follows medio-lateral direction at the most anterior electrodes. The fact that these interactions are not entirely symmetrical may characterize a critical functional property of the motor cortex for the control of upper limb movements. Overall, these results support the assumption that the motor cortex is not functionally homogeneous but forms a complex network of interacting subregions.

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Section: Discussionsupporting

confidence: 81%

Mapping Horizontal Spread of Activity in Monkey Motor Cortex Using Single Pulse Microstimulation

Hao

Riehle

Brochier

2016

Front. Neural Circuits

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“…In this regard, the circuitry shown in Figure may begin to bring the connectivity of avian vocal‐motor networks into line with the connectivity of primate motor‐cortical networks (which were detected using similar retrograde tracing methods—Dea, Hamadjida, Elgbeili, Quessy, & Dancause, ; Hamadjida, Dea, Deffeyes, Quessy, & Dancause, ; Stepniewska, Preuss, & Kaas, ). That is, the expanded behavioral repertoire of primates—particularly the hands and digits—is associated with modular and highly parallel patterns of sensorimotor connectivity that transit distinct subregions of premotor and motor cortex, including parallel closed‐loop circuitry between premotor and motor cortex (Dea et al, ; Hamadjida et al, ). The present data suggest that the expanded vocal repertoire of songbirds is associated with similar patterns of premotor and motor connectivity—HVC neurons are organized by connectivity into a number of modular cell groups, patterns of convergent sensorimotor input transit each module in a highly parallel fashion (Figure ), and a parallel closed‐loop circuit connects premotor (HVC) and motor (RA) cortex (Figure ).…”

Section: Discussionmentioning

confidence: 99%

Orthogonal topography in the parallel input architecture of songbird HVC

Elliott

Bertram

et al. 2017

J of Comparative Neurology

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Neural activity within the cortical premotor nucleus HVC (acronym is name) encodes the learned songs of adult male zebra finches (Taeniopygia guttata). HVC activity is driven and/or modulated by a group of five afferent nuclei (the Medial Magnocellular nucleus of the Anterior Nidopallium, MMAN; Nucleus Interface, NIf; nucleus Avalanche, Av; the Robust nucleus of the Arcopallium, RA; the Uvaeform nucleus, Uva). While earlier evidence suggested that HVC receives a uniformly distributed and nontopographic pattern of afferent input, recent evidence suggests this view is incorrect (Basista et al., ). Here, we used a double-labeling strategy (varying both the distance between and the axial orientation of dual tracer injections into HVC) to reveal a massively parallel and in some cases topographic pattern of afferent input. Afferent neurons target only one rostral or caudal location within medial or lateral HVC, and each HVC location receives convergent input from each afferent nucleus in parallel. Quantifying the distributions of single-labeled cells revealed an orthogonal topography in the organization of afferent input from MMAN and NIf, two cortical nuclei necessary for song learning. MMAN input is organized across the lateral-medial axis whereas NIf input is organized across the rostral-caudal axis. To the extent that HVC activity is influenced by afferent input during the learning, perception, or production of song, functional models of HVC activity may need revision to account for the parallel input architecture of HVC, along with the orthogonal input topography of MMAN and NIf.

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“…The hand area was surrounded by representations of proximal movements (elbow or shoulder), orofacial movements, and non-responsive sites. In particular, only non-responsive sites were found along the rostral wall of the central sulcus (depths of 2,000-4,000 mm), supporting that the hand area of M1 is located on the cortical surface in cebus monkeys [4,8].…”

Section: Physiological Mapping and Injection Of Neuroanatomical Tracersmentioning

confidence: 60%

“…Figure 1 shows representative electrophysiological mapping data from one monkey (CB-7). In M1, digit and wrist/forearm movements formed a contiguous area, which we referred to as the hand area [8,9]. The hand area was surrounded by representations of proximal movements (elbow or shoulder), orofacial movements, and non-responsive sites.…”

Section: Physiological Mapping and Injection Of Neuroanatomical Tracersmentioning

confidence: 99%

Parallel Cortical Networks Formed by Modular Organization of Primary Motor Cortex Outputs

et al. 2016

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In primates, the refinement of motor behaviors, in particular hand use, is associated with the establishment of more direct projections from primary motor cortex (M1) onto cervical motoneurons [1, 2] and the appearance of additional premotor and sensory cortical areas [3]. All of these areas have reciprocal connections with M1 [4-7]. Thus, during the evolution of the sensorimotor network, the number of interlocutors with which M1 interacts has tremendously increased. It is not clear how these additional interconnections are organized in relation to one another within the hand representation of M1. This is important because the organization of connections between M1 and phylogenetically newer and specialized cortical areas is likely to be key to the increased repertoire of hand movements in primates. In cebus monkeys, we used injections of retrograde tracers into the hand representation of different cortical areas of the sensorimotor network (ventral and dorsal premotor areas [PMv and PMd], supplementary motor area [SMA], and posterior parietal cortex [area 5]), and we analyzed the pattern of labeled neurons within the hand representation of M1. Instead of being uniformly dispersed across M1, neurons sending projections to each distant cortical area were largely segregated in different subregions of M1. These data support the view that primates split the cortical real estate of M1 into modules, each preferentially interconnected with a particular cortical area within the sensorimotor network. This modular organization could sustain parallel processing of interactions with multiple specialized cortical areas to increase the behavioral repertoire of the hand.

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Different Patterns of Cortical Inputs to Subregions of the Primary Motor Cortex Hand Representation inCebus apella

Cited by 49 publications

References 69 publications

Mapping Horizontal Spread of Activity in Monkey Motor Cortex Using Single Pulse Microstimulation

Mapping Horizontal Spread of Activity in Monkey Motor Cortex Using Single Pulse Microstimulation

Orthogonal topography in the parallel input architecture of songbird HVC

Parallel Cortical Networks Formed by Modular Organization of Primary Motor Cortex Outputs

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