Primate Primary Motor Cortex Research Articles

Where Do Core Thalamocortical Axons Terminate in Mammalian Neocortex When There Is No Cytoarchitecturally Distinct Layer 4?

Although the mammalian cerebral cortex is most often described as a hexalaminar structure, there are cortical areas (primary motor cortex) and species (elephants, cetaceans, and hippopotami), where a cytoarchitecturally indistinct, or absent, layer 4 is noted. Thalamocortical projections from the core, or first order, thalamic system terminate primarily in layers 4/inner 3. We explored the termination sites of core thalamocortical projections in cortical areas and in species where there is no cytoarchitecturally distinct layer 4 using the immunolocalization of vesicular glutamate transporter 2, a known marker of core thalamocortical axon terminals, in 31 mammal species spanning the eutherian radiation. Several variations from the canonical cortical column outline of layer 4 and core thalamocortical inputs were noted. In shrews/microchiropterans, layer 4 was present, but many core thalamocortical projections terminated in layer 1 in addition to layers 4 and inner 3. In primate primary visual cortex, the sublaminated layer 4 was associated with a specialized core thalamocortical projection pattern. In primate primary motor cortex, no cytoarchitecturally distinct layer 4 was evident and the core thalamocortical projections terminated throughout layer 3. In the African elephant, cetaceans, and river hippopotamus, no cytoarchitecturally distinct layer 4 was observed and core thalamocortical projections terminated primarily in inner layer 3 and less densely in outer layer 3. These findings are contextualized in terms of cortical processing, perception, and the evolutionary trajectory leading to an indistinct or absent cortical layer 4.

In vitro characterization of intrinsic properties and local synaptic inputs to pyramidal neurons in macaque primary motor cortex.

Primates (including humans) have a highly developed corticospinal tract, and specialized motor cortical areas which differ in key ways from rodents. Much work on motor cortex has therefore used macaque monkeys as a good animal model for human motor control. However, there is a paucity of data describing the fundamental functional architecture of primate primary motor cortex, which is best addressed with in vitro approaches. In this study we examined the cellular properties and the micro‐circuitry of the adult macaque primary motor cortex by carrying out in‐vitro intracellular recordings. We aimed to characterize the basic properties of the cortical circuitry by studying the intrinsic properties of its pyramidal neurons and their physiological interconnectivity. We studied the passive and active electrophysiological properties of pyramidal neurons in both superficial and deep cortical layers. Both superficial and deep pyramidal neurons exhibited bursting behaviour that could act as powerful excitation for downstream targets. Synaptic connections were lamina specific. Neurons in the deep layers had convergent excitatory inputs from all cortical layers whereas superficial neurons had only significant inputs from superficial layers. This sheds light on the functional architecture of the primate primary motor cortex and how its output is shaped. We also took the unique opportunity in our recording technique to characterize the relationship between intracellular and extracellular spike waveforms, with implications for cell‐type identification in studies in awake behaving monkey. Our results will aid the interpretation of primate studies into motor control involving extracellular spike recordings and electrical stimulation in primary motor cortex.

Decoding 3-D Reach and Grasp Kinematics From High-Frequency Local Field Potentials in Primate Primary Motor Cortex

Intracortical microelectrode array recordings generate a variety of neural signals with potential application as control signals in neural interface systems. Previous studies have focused on single and multiunit activity (MUA), as well as low-frequency local field potentials (LFPs), but have not explored higher frequency (>200 Hz) LFPs. In addition, the potential to decode 3-D reach and grasp kinematics based on LFPs has not been demonstrated. Here, we use mutual information and decoding analyses to probe the information content about 3-D reaching and grasping of seven different LFP frequency bands in the range of 0.3-400 Hz. LFPs were recorded via 96-microelectrode arrays in primary motor cortex (M1) of two monkeys performing free reaching to grasp moving objects. Mutual information analyses revealed that higher frequency bands (e.g., 100-200 and 200-400 Hz) carried the most information about the examined kinematics. Furthermore, Kalman filter decoding revealed that broad-band high frequency LFPs, likely reflecting MUA, provided the best decoding performance as well as substantial accuracy in reconstructing reach kinematics, grasp aperture, and aperture velocity. These results indicate that LFPs, especially high frequency bands, could be useful signals for neural interfaces controlling 3-D reach and grasp kinematics.

Do Electrode Properties Create a Problem in Interpreting Local Field Potential Recordings?

Local field potential (LFP) recordings within the brain have become an important tool used by neuroscientists to make inferences about the activity of a population of cells near an electrode. Each passing year analysis of LFPs in neuroscience seems to bring important new insights on the possible workings of networks in the brain to produce behavior (Buschman and Miller 2007; Canolty et al. 2006; Gregoriou et al. 2009; Liu and Newsome 2006; Lubenov and Siapas 2009; Pesaran et al. 2008; Womelsdorf et al. 2006). Indeed LFPs have become a near-ubiquitous tool in neurophysiology seemingly in use anywhere extracellular spikes are also recorded.

Congenitally altered motor experience alters somatotopic organization of human primary motor cortex.

Human motor development is thought to result from a complex interaction between genes and experience. The well-known somatotopic organization of the primate primary motor cortex (M1) emerges postnatally. Although adaptive changes in response to learning and use occur throughout life, somatotopy is maintained as reorganization is restricted to modifications within major body part representations. We report of a unique opportunity to evaluate the influence of experience on the genetically determined somatotopic organization of motor cortex in humans. We examined the motor "foot" representation in subjects with congenitally compromised hand function and compensatory skillful foot use. Functional magnetic resonance imaging (fMRI) and transcranial magnetic stimulation (TMS) of M1 revealed that the foot was represented in the classical medial foot area of M1 and was several centimetres away in nonadjacent cortex in the vicinity of the lateral "hand" area. Both areas had direct output to the spinal motor neurons innervating foot muscles and were behaviorally relevant because experimental disruption of either area by TMS altered reaction times. We demonstrate a unique, nonsomatotopically organized M1 in humans, which emerged as a function of grossly altered motor behavior from the earliest stages of development. Our results imply that during early motor development experience may play a more critical role in the shaping of genetically determined neural networks than previously assumed.

Coding of movement‐ and force‐related information in primate primary motor cortex: a computational approach

Coordinated movements result from descending commands transmitted by central motor systems to the muscles. Although the resulting effect of the commands has the dimension of a muscular force, it is unclear whether the information transmitted by the commands concerns movement kinematics (e.g. position, velocity) or movement dynamics (e.g. force, torque). To address this issue, we used an optimal control model of movement production that calculates inputs to motoneurons that are appropriate to drive an articulated limb toward a goal. The model quantitatively accounted for kinematic, kinetic and muscular properties of planar, shoulder/elbow arm-reaching movements of monkeys, and reproduced detailed features of neuronal correlates of these movements in primate motor cortex. The model also reproduced qualitative spatio-temporal characteristics of movement- and force-related single neuron discharges in non-planar reaching and isometric force production tasks. The results suggest that the nervous system of the primate controls movements through a muscle-based controller that could be located in the motor cortex.

Reliability of signals from a chronically implanted, silicon-based electrode array in non-human primate primary motor cortex

Multiple-electrode arrays are valuable both as a research tool and as a sensor for neuromotor prosthetic devices, which could potentially restore voluntary motion and functional independence to paralyzed humans. Long-term array reliability is an important requirement for these applications. Here, we demonstrate the reliability of a regular array of 100 microelectrodes to obtain neural recordings from primary motor cortex (MI) of monkeys for at least three months and up to 1.5 years. We implanted Bionic (Cyberkinetics, Inc., Foxboro, MA) silicon probe arrays in MI of three Macaque monkeys. Neural signals were recorded during performance of an eight-direction, push-button task. Recording reliability was evaluated for 18, 35, or 51 sessions distributed over 83, 179, and 569 days after implantation, respectively, using qualitative and quantitative measures. A four-point signal quality scale was defined based on the waveform amplitude relative to noise. A single observer applied this scale to score signal quality for each electrode. A mean of 120 (+/- 17.6 SD), 146 (+/- 7.3), and 119 (+/- 16.9) neural-like waveforms were observed from 65-85 electrodes across subjects for all recording sessions of which over 80% were of high quality. Quantitative measures demonstrated that waveforms had signal-to-noise ratio (SNR) up to 20 with maximum peak-to-peak amplitude of over 1200 microv with a mean SNR of 4.8 for signals ranked as high quality. Mean signal quality did not change over the duration of the evaluation period (slope 0.001, 0.0068 and 0.03; NS). By contrast, neural waveform shape varied between, but not within days in all animals, suggesting a shifting population of recorded neurons over time. Arm-movement related modulation was common and 66% of all recorded neurons were tuned to reach direction. The ability for the array to record neural signals from parietal cortex was also established. These results demonstrate that neural recordings that can provide movement related signals for neural prostheses, as well as for fundamental research applications, can be reliably obtained for long time periods using a monolithic microelectrode array in primate MI and potentially from other cortical areas as well.

Systematic changes in motor cortex cell activity with arm posture during directional isometric force generation.

We report here the activity of 96 cells in primate primary motor cortex (MI) during exertion of isometric forces at the hand in constant spatial directions, while the hand was at five to nine different spatial locations on a plane. The discharge of nearly all cells varied significantly with both hand location and the direction of isometric force before and during force-ramp generation as well as during static force-hold. In addition, nearly all cells displayed changes in the variation of their activity with force direction at different hand locations. This change in relationship was often expressed in part as a change in the cell's directional tuning at different hand locations. Cell directional tuning tended to shift systematically with hand location even though the direction of static force output at the hand remained constant. These directional effects were less pronounced before the onset of force output than after force onset. Cells also often showed planar modulations of discharge level with hand location. Sixteen proximal arm muscles showed similar effects, reflecting how hand location-dependent biomechanical factors altered their task-related activity. These findings indicate that MI single-cell activity does not covary exclusively with the level and direction of net force output at the hand and provides further evidence that MI contributes to the transformation between extrinsic and intrinsic representations of motor output during isometric force production.

Neuronal activity patterns in primate primary motor cortex related to trained or semiautomatic jaw and tongue movements.

The present study was undertaken to determine the firing patterns and the mechanoreceptive field (RF) properties of neurons within the face primary motor cortex (face-MI) in relation to chewing and other orofacial movements in the awake monkey. Of a total of 107 face-MI neurons recorded, 73 of 74 tested had activity related to chewing and 47 of 66 neurons tested showed activity related to a trained tongue task. Of the 73 chewing-related neurons, 52 (71.2%) showed clear rhythmic activity during rhythmic chewing. A total of 32 (43.8%) also showed significant alterations in activity in relation to the swallowing of a solid food (apple) bolus. Many of the chewing-related neurons (81.8% of 55 tested) had an orofacial RF, which for most was on the tongue dorsum. Tongue protrusion was evoked by intracortical microstimulation (ICMS) at most (63.6%) of the recording sites where neurons fired during the rhythmic jaw-opening phase, whereas tongue retraction was evoked by ICMS at most (66.7%) sites at which the neurons firing during the rhythmic jaw-closing phase were recorded. Of the 47 task-related neurons, 21 of 22 (95.5%) examined also showed chewing-related activity and 29 (61.7%) demonstrated significant alteration in activity in relation to the swallowing of a juice reward. There were no significant differences in the peak firing frequency among neuronal activities related to chewing, swallowing, or the task. These findings provide further evidence that face-MI may play an important role not only in trained orofacial movements but also in chewing as well as swallowing, including the control of tongue and jaw movements that occur during the masticatory sequence.

Lesions of the precentral gyrus in nonhuman primates: A pre-medline bibliography

Many contemporary investigators are unaware of the important papers involving lesions of the primate primary motor cortex published prior to those revealed by a computer search of the literature (i.e., papers published prior to about 1966). In order to increase awareness of these reports, we present here an annotated bibliography of these papers beginning with that of Ferrier and Yeo (1884). We provide evidence that these papers can provide valuable information on the function of the primate motor cortex and on recovery of behavior after brain lesions, and are also useful for sharpening the questions posed by more refined modern studies.

Reorganization in Primary Motor Cortex of Primates with Long-Standing Therapeutic Amputations

Intracortical microstimulation was used to investigate the organization of primate primary motor cortex (M1) in three squirrel monkeys and two galagos years after the therapeutic amputation of an injured forelimb or hindlimb. In two squirrel monkeys with forelimb amputation, physiological results were correlated with the distribution of corticospinal neurons after injections of tracers into the lower cervical segments of the spinal cord. Distributions of labeled corticospinal neurons helped identify the locations of the former forelimb cortex in M1. Evoked movements from M1 ipsilateral to the missing limb were not obviously different from M1 of normal controls. Stimulation in the deefferented part of M1 contralateral to the missing limb elicited movements of the remaining proximal muscles as well as movements from adjacent body representations in all cases. Stimulation in the deefferented forelimb cortex evoked shoulder stump, trunk, and orofacial movements, whereas stimulation in the deefferented hindlimb cortex evoked hip stump, trunk, and tail movements. Movements were evoked from all sites in the deprived cortex, so that there were no unresponsive zones. Minimal levels of current necessary to evoke these movements varied from those in the normal range to those of much higher levels, with the average threshold higher than normal. Finally, multiunit recording from the two galagos revealed that the deprived portions of S1 were responsive to touch or taps on the stump and neighboring body parts.

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