[Show abstract][Hide abstract] ABSTRACT: Area F5, in the ventral premotor cortex of the macaque monkey, plays a critical role in determining the hand shape appropriate for grasp of a visible object. F5 neurones show increased firing for particular types of grasp, and inactivation of F5 produces deficits in visually guided grasp. But how is F5 activity transformed into the appropriate pattern of hand muscle activity for efficient grasp? Here we investigate the pathways that may be involved by testing the effect of single stimuli delivered through microwires chronically implanted in area F5 and in primary motor cortex (M1) of two macaque monkeys. The EMG responses from M1 test (T) stimulation were recorded from 4-11 contralateral hand, digit and arm muscles during reach-to-grasp of visually presented objects. Conditioning (C) stimulation of F5, at intensities subthreshold for motor effects, caused strong modulation (over twofold) of M1 test (T) responses. The pattern of facilitation was specific. First, facilitation of the T response was particularly evident at short C-T intervals of -1 to 1 ms. Second, this facilitation was only present in some muscles and during reach-to-grasp of a subset of objects; it did not appear to be simply related to the level of EMG activity in the muscles at the moment of cortical stimulation or indeed to the upcoming contribution of that muscle during grasp. At later C-T intervals (1-6 ms), F5 stimulation caused significant suppression of the test M1 response. The results are in keeping with the concept that during visually guided grasp, F5 modulates corticospinal outputs from M1 in a muscle- and grasp-specific manner.
The Journal of Physiology 02/2009; 587(Pt 5):1057-69. DOI:10.1113/jphysiol.2008.165571 · 5.04 Impact Factor
[Show abstract][Hide abstract] ABSTRACT: The selectivity for object-specific grasp in local field potentials (LFPs) was investigated in two awake macaque monkeys trained to observe, reach out, grasp and hold one of six objects presented in a pseudorandom order. Simultaneous, multiple electrode recordings were made from the hand representations of primary motor cortex (M1) and ventral premotor cortex (area F5). LFP activity was well developed during the observation and hold periods of the task, especially in the beta-frequency range (15-30 Hz). Selectivity of LFP activity for upcoming grasp was rare in the observation period, but common during stable grasp. The majority of M1 (90 of 92) and F5 (81 of 97) sites showed selectivity for at least one frequency, which was maximal in the beta range but also present at higher frequencies (30-50 Hz). When the LFP power associated with grasp of a specific object was large in the beta-frequency range, it was usually of low power in the higher 30-50 Hz range, and vice-versa. Simple hook grips involving flexion of one or more fingers were associated with large beta power, whereas more complex grips involving the thumb (e.g., precision grip) were associated with small beta power. At many M1 sites, there was a highly significant inverse relationship between the tuning of spikes (including those of identified pyramidal tract neurons) and beta-range LFP for different grasps, whereas a positive correlation was found at higher frequencies (30-50 Hz). High levels of beta LFP and low pyramidal cell spike rate may reflect a common mechanism used to control motor set during different types of grasp.
The Journal of Neuroscience : The Official Journal of the Society for Neuroscience 11/2008; 28(43):10961-71. DOI:10.1523/JNEUROSCI.1956-08.2008 · 6.34 Impact Factor
[Show abstract][Hide abstract] ABSTRACT: To understand the relative contributions of primary motor cortex (M1) and area F5 of the ventral premotor cortex (PMv) to visually guided grasp, we made simultaneous multiple electrode recordings from the hand representations of these two areas in two adult macaque monkeys. The monkeys were trained to fixate, reach out and grasp one of six objects presented in a pseudorandom order. In M1 326 task-related neurons, 104 of which were identified as pyramidal tract neurons, and 138 F5 neurons were analyzed as separate populations. All three populations showed activity that distinguished the six objects grasped by the monkey. These three populations responded in a manner that generalized across different sets of objects. F5 neurons showed object/grasp related tuning earlier than M1 neurons in the visual presentation and premovement periods. Also F5 neurons generally showed a greater preference for particular objects/grasps than did M1 neurons. F5 neurons remained tuned to a particular grasp throughout both the premovement and reach-to-grasp phases of the task, whereas M1 neurons showed different selectivity during the different phases. We also found that different types of grasp appear to be represented by different overall levels of activity within the F5-M1 circuit. Altogether these properties are consistent with the notion that F5 grasping-related neurons play a role in translating visual information about the physical properties of an object into the motor commands that are appropriate for grasping, and which are elaborated within M1 for delivery to the appropriate spinal machinery controlling hand and digit muscles.
Journal of Neurophysiology 08/2007; 98(1):488-501. DOI:10.1152/jn.01094.2006 · 2.89 Impact Factor
[Show abstract][Hide abstract] ABSTRACT: During object grasp, a coordinated activation of distal muscles is required to shape the hand in relation to the physical properties of the object. Despite the fundamental importance of the grasping action, little is known of the muscular activation patterns that allow objects of different sizes and shapes to be grasped. In a study of two adult macaque monkeys, we investigated whether we could distinguish between EMG activation patterns associated with grasp of 12 differently shaped objects, chosen to evoke a wide range of grasping postures. Each object was mounted on a horizontal shuttle held by a weak spring (load force 1-2 N). Objects were located in separate sectors of a "carousel," and inter-trial rotation of the carousel allowed sequential presentation of the objects in pseudorandom order. EMG activity from 10 to 12 digit, hand, and arm muscles was recorded using chronically implanted electrodes. We show that the grasp of different objects was characterized by complex but distinctive patterns of EMG activation. Cluster analysis shows that these object-related EMG patterns were specific and consistent enough to identify the object unequivocally from the EMG recordings alone. EMG-based object identification required a minimum of six EMGs from simultaneously recorded muscles. EMG patterns were consistent across recording sessions in a given monkey but showed some differences between animals. These results identify the specific patterns of activity required to achieve distinct hand postures for grasping, and they open the way to our understanding of how these patterns are generated by the central motor network.
Journal of Neurophysiology 10/2004; 92(3):1770-82. DOI:10.1152/jn.00976.2003 · 2.89 Impact Factor
[Show abstract][Hide abstract] ABSTRACT: In studies using single neuron recordings from awake, behaving monkeys, it is necessary to make repeated transdural penetrations using fragile microelectrodes. The tough connective tissue that accumulates after the dura mater is first exposed is often problematic because of electrode breakage and the mechanical stress to the underlying brain tissue caused by excessive dimpling during penetration. We describe the use of an antimitotic compound, 5-fluorouracil (5FU) to control the growth of this connective tissue. 5FU can be safely applied for short periods to the exposed dural tissue on a regular basis provided that it is thoroughly rinsed after application. The advantages of using 5FU are fourfold: first, it depresses fibroblast division and minimizes dural growth and scar tissue formation so that penetrations are easier with less electrode damage or breakage. Second, the frequency of surgical procedures required to remove this tissue are greatly reduced, which benefits both the experiment animal and the experiment. Third, 5FU reduces vascularization of the tissue so that its removal is far easier and without significant blood loss. Finally, 5FU seems to inhibit bacterial infections within the recording chamber. In macaque motor cortex, we performed a quantitative study of electrophysiological data recorded from monkeys with and without 5FU treatment. No significant deleterious side effects produced by 5FU could be detected. Likewise, histological examination of cortical tissue underlying treated dura did not reveal any obvious signs of damage by 5FU. We recommend this approach, with the appropriate safety precautions, to all those neurophysiologists using transdural microelectrode methods in chronically prepared experimental animals. It is also possible that this technique may be useful in other situations where there is dural scarring after surgical intervention or injury.
Journal of Neurophysiology 09/2003; 90(2):1324-32. DOI:10.1152/jn.00169.2003 · 2.89 Impact Factor
[Show abstract][Hide abstract] ABSTRACT: We investigated whether stimulation of the pyramidal tract (PT) could reset the phase of 15-30 Hz beta oscillations observed in the macaque motor cortex. We recorded local field potentials (LFPs) and multiple single-unit activity from two conscious macaque monkeys performing a precision grip task. EMG activity was also recorded from the second animal. Single PT stimuli were delivered during the hold period of the task, when oscillations in the LFP were most prominent. Stimulus-triggered averaging of the LFP showed a phase-locked oscillatory response to PT stimulation. Frequency domain analysis revealed two components within the response: a 15-30 Hz component, which represented resetting of on-going beta rhythms, and a lower frequency 10 Hz response. Only the higher frequency could be observed in the EMG activity, at stronger stimulus intensities than were required for resetting the cortical rhythm. Stimulation of the PT during movement elicited a greatly reduced oscillatory response. Analysis of single-unit discharge confirmed that PT stimulation was capable of resetting periodic activity in motor cortex. The firing patterns of pyramidal tract neurones (PTNs) and unidentified neurones exhibited successive cycles of suppression and facilitation, time locked to the stimulus. We conclude that PTN activity directly influences the generation of the 15-30 Hz rhythm. These PTNs facilitate EMG activity in upper limb muscles, contributing to corticomuscular coherence at this same frequency. Since the earliest oscillatory effect observed following stimulation was a suppression of firing, we speculate that inhibitory feedback may be the key mechanism generating such oscillations in the motor cortex.
The Journal of Physiology 07/2002; 541(Pt 3):685-99. DOI:10.1113/jphysiol.2001.015099 · 5.04 Impact Factor
[Show abstract][Hide abstract] ABSTRACT: Diffusion tensor imaging (DTI), a magnetic resonance imaging technique, is used to infer major axonal projections in the macaque and human brain. This study investigates the feasibility of using known macaque anatomical connectivity as a "gold-standard" for the evaluation of DTI tractography methods. Connectivity information is determined from the DTI data using fast marching tractography (FMT), a novel tract-tracing (tractography) method. We show for the first time that it is possible to determine, in an entirely noninvasive manner, anatomical connection pathways and maps of an anatomical connectivity metric in the macaque brain using a standard clinical scanner and that these pathways are consistent with known anatomy. Analogous human anatomical connectivity is also presented for the first time using the FMT method, and the results are compared. The current limitations of the methodology and possibilities available for further studies are discussed.
[Show abstract][Hide abstract] ABSTRACT: Neural synchronization in the cortex, and its potential role in information coding, has attracted much recent attention. In this study, we have recorded long spike trains (mean, 33,000 spikes) simultaneously from multiple single neurons in the primary motor cortex (M1) of two conscious macaque monkeys performing a precision grip task. The task required the monkey to use its index finger and thumb to move two spring-loaded levers into a target, hold them there for 1 s, and release for a food reward. Synchrony was analyzed using a time-resolved cross-correlation method, normalized using an estimate of the instantaneous firing rate of the cell. This was shown to be more reliable than methods using trial-averaged firing rate. A total of 375 neurons was recorded from the M1 hand area; 235 were identified as pyramidal tract neurons. Synchrony was weak [mean k' = 1.05 +/- 0.04 (SD)] but widespread among pairs of M1 neurons (218/1359 pairs with above-chance synchrony), including output neurons. Synchrony usually took the form of a broad central peak [average width, 18.7 +/- 8.7 (SD) ms]. There were marked changes during different phases of the task. As a population, synchrony was greatest during the steady hold period in striking contrast to the averaged cell firing rate, which was maximal when the animal was moving the levers into target. However, the modulation of synchrony during task performance showed considerable variation across individual cell pairs. Two types of synchrony were identified: oscillatory (with periodic side lobes in the cross-correlation) and nonoscillatory. Their relative contributions were quantified by filtering the cross-correlations to exclude either frequencies from 18 to 37 Hz or all higher and lower frequencies. At the peak of population synchrony during the hold period, about half (51.7% in one monkey, 56.2% in the other) of the synchronization was within this oscillatory bandwidth. This study provides strong support for assemblies of neurons being synchronized during specific phases of a complex task with potentially important consequences for both information processing within M1 and for the impact of M1 commands on target motoneurons.
Journal of Neurophysiology 03/2001; 85(2):869-85. · 2.89 Impact Factor
[Show abstract][Hide abstract] ABSTRACT: Simultaneous recording from multiple single neurones presents many technical difficulties. However, obtaining such data has many advantages, which make it highly worthwhile to overcome the technical problems. This report describes methods which we have developed to permit recordings in awake behaving monkeys using the 'Eckhorn' 16 electrode microdrive. Structural magnetic resonance images are collected to guide electrode placement. Head fixation is achieved using a specially designed headpiece, modified for the multiple electrode approach, and access to the cortex is provided via a novel recording chamber. Growth of scar tissue over the exposed dura mater is reduced using an anti-mitotic compound. Control of the microdrive is achieved by a computerised system which permits several experimenters to move different electrodes simultaneously, considerably reducing the load on an individual operator. Neurones are identified as pyramidal tract neurones by antidromic stimulation through chronically implanted electrodes; stimulus control is integrated into the computerised system. Finally, analysis of multiple single unit recordings requires accurate methods to correct for non-stationarity in unit firing. A novel technique for such correction is discussed.