Monkey Dorsal Premotor Cortex Research Articles

Microstimulation of dorsal premotor and primary motor cortex delays the volitional commitment to an action choice

Humans and other animals are faced with decisions about actions on a daily basis. These typically include a period of deliberation that ends with the commitment to a choice, which then leads to the overt expression of that choice through action. Previous studies with monkeys have demonstrated that neural activity in sensorimotor areas correlates with the deliberation process and reflects the moment of commitment before movement initiation, but the causal roles of these regions are challenging to establish. Here, we tested whether dorsal premotor (PMd) and primary motor cortex (M1) are causally involved in the volitional commitment to a reaching choice. We found that brief subthreshold microstimulation in PMd or M1 delayed commitment to an action but not the initiation of the action itself. Importantly, microstimulation only had a significant effect when it was delivered close to and before commitment time. These results are consistent with the proposal that PMd and M1 participate in the commitment process, which occurs when a critical firing rate difference is reached between cells voting for the selected option and those voting for the competing one.NEW & NOTEWORTHY The neural substrates of decisions between actions are typically investigated by correlating neural activity and subjects' decision behavior, but this does not establish causality. In a reaching decision task, we demonstrate that subthreshold microstimulation of the monkey dorsal premotor cortex or primary motor cortex delays the deliberation duration if applied shortly before choice commitment. This result suggests a causal role of the sensorimotor cortex in the determination of decisions between actions.

Heterogeneous Attractor Cell Assemblies for Motor Planning in Premotor Cortex

Cognitive functions like motor planning rely on the concerted activity of multiple neuronal assemblies underlying still elusive computational strategies. During reaching tasks, we observed stereotyped sudden transitions (STs) between low and high multiunit activity of monkey dorsal premotor cortex (PMd) predicting forthcoming actions on a single-trial basis. Occurrence of STs was observed even when movement was delayed or successfully canceled after a stop signal, excluding a mere substrate of the motor execution. An attractor model accounts for upward STs and high-frequency modulations of field potentials, indicative of local synaptic reverberation. We found in vivo compelling evidence that motor plans in PMd emerge from the coactivation of such attractor modules, heterogeneous in the strength of local synaptic self-excitation. Modules with strong coupling early reacted with variable times to weak inputs, priming a chain reaction of both upward and downward STs in other modules. Such web of "flip-flops" rapidly converged to a stereotyped distributed representation of the motor program, as prescribed by the long-standing theory of associative networks.

An L 1-regularized logistic model for detecting short-term neuronal interactions

Interactions among neurons are a key component of neural signal processing. Rich neural data sets potentially containing evidence of interactions can now be collected readily in the laboratory, but existing analysis methods are often not sufficiently sensitive and specific to reveal these interactions. Generalized linear models offer a platform for analyzing multi-electrode recordings of neuronal spike train data. Here we suggest an L(1)-regularized logistic regression model (L(1)L method) to detect short-term (order of 3 ms) neuronal interactions. We estimate the parameters in this model using a coordinate descent algorithm, and determine the optimal tuning parameter using a Bayesian Information Criterion. Simulation studies show that in general the L(1)L method has better sensitivities and specificities than those of the traditional shuffle-corrected cross-correlogram (covariogram) method. The L(1)L method is able to detect excitatory interactions with both high sensitivity and specificity with reasonably large recordings, even when the magnitude of the interactions is small; similar results hold for inhibition given sufficiently high baseline firing rates. Our study also suggests that the false positives can be further removed by thresholding, because their magnitudes are typically smaller than true interactions. Simulations also show that the L(1)L method is somewhat robust to partially observed networks. We apply the method to multi-electrode recordings collected in the monkey dorsal premotor cortex (PMd) while the animal prepares to make reaching arm movements. The results show that some neurons interact differently depending on task conditions. The stronger interactions detected with our L(1)L method were also visible using the covariogram method.

The Cortical Timeline for Deciding on Reach Motor Goals

Flexible sensorimotor planning is the basis for goal-directed behavior. We investigated the integration of visuospatial information with context-specific transformation rules during reach planning. We were especially interested in the relative timing of motor-goal decisions in monkey dorsal premotor cortex (PMd) and parietal reach region (PRR). We used a rule-based mapping task with different cueing conditions to compare task-dependent motor-goal latencies. The task allowed us a separation of cue-related from motor-related activity, and a separation of activity related to motor planning from activity related to motor initiation or execution. The results show that selectivity for the visuospatial goal of a pending movement occurred earlier in PMd than PRR whenever the task required spatial remapping. Such remapping was needed if the spatial representation of a cue or of a default motor plan had to be transformed into a spatially incongruent representation of the motor goal. In contrast, we did not find frontoparietal latency differences if the spatial representation of the cue or the default plan was spatially congruent with the motor goal. The fact that frontoparietal latency differences occurred only in conditions with spatial remapping was independent of the subjects' partial a priori knowledge about the pending goal. Importantly, frontoparietal latency differences existed for motor-goal representations during movement planning, without immediate motor execution. We interpret our findings as being in support of the hypothesis that latency differences reflect a dynamic reorganization of network activity in PRR, and suggest that the reorganization is contingent on frontoparietal projections from PMd.

A high-performance brain–computer interface

Recent studies have demonstrated that monkeys and humans can use signals from the brain to guide computer cursors. Brain-computer interfaces (BCIs) may one day assist patients suffering from neurological injury or disease, but relatively low system performance remains a major obstacle. In fact, the speed and accuracy with which keys can be selected using BCIs is still far lower than for systems relying on eye movements. This is true whether BCIs use recordings from populations of individual neurons using invasive electrode techniques or electroencephalogram recordings using less- or non-invasive techniques. Here we present the design and demonstration, using electrode arrays implanted in monkey dorsal premotor cortex, of a manyfold higher performance BCI than previously reported. These results indicate that a fast and accurate key selection system, capable of operating with a range of keyboard sizes, is possible (up to 6.5 bits per second, or approximately 15 words per minute, with 96 electrodes). The highest information throughput is achieved with unprecedentedly brief neural recordings, even as recording quality degrades over time. These performance results and their implications for system design should substantially increase the clinical viability of BCIs in humans.

Callosal connections of dorso-lateral premotor cortex.

This study investigated the organization of the callosal connections of the two subdivisions of the monkey dorsal premotor cortex (PMd), dorso-rostral (F7) and dorso-caudal (F2). In one animal, Fast blue and Diamidino yellow were injected in F7 and F2, respectively; in a second animal, the pattern of injections was reversed. F7 and F2 receive a major callosal input from their homotopic counterpart. The heterotopic connections of F7 originate mainly from F2, with smaller contingent from pre-supplementary motor area (pre-SMA, F6), area 8 (frontal eye fields), and prefrontal cortex (area 46), while those of F2 originate from F7, with smaller contributions from ventral premotor areas (F5, F4), SMA-proper (F3), and primary motor cortex (M1). Callosal cells projecting homotopically are mostly located in layers II-III, those projecting heterotopically occupy layers II-III and V-VI. A spectral analysis was used to characterize the spatial fluctuations of the distribution of callosal neurons, in both F7 and F2, as well as in adjacent cortical areas. The results revealed two main periodic components. The first, in the domain of the low spatial frequencies, corresponds to periodicities of cell density with peak-to-peak distances of approximately 10 mm, and suggests an arrangement of callosal cells in the form of 5-mm wide bands. The second corresponds to periodicities of approximately 2 mm, and probably reflects a 1-mm columnar-like arrangement. Coherency and phase analyses showed that, although similar in their spatial arrangements, callosal cells projecting to dorsal premotor areas are segregated in the tangential cortical domain.

Modest gaze-related discharge modulation in monkey dorsal premotor cortex during a reaching task performed with free fixation.

Recent studies have shown that gaze angle modulates reach-related neural activity in many cortical areas, including the dorsal premotor cortex (PMd), when gaze direction is experimentally controlled by lengthy periods of imposed fixation. We looked for gaze-related modulation in PMd during the brief fixations that occur when a monkey is allowed to look around freely without experimentally imposed gaze control while performing a center-out delayed arm-reaching task. During the course of the instructed-delay period, we found significant effects of gaze angle in 27-51% of PMd cells. However, for 90-95% of cells, these effects accounted for <20% of the observed discharge variance. The effect of gaze was significantly weaker than the effect of reach-related variables. In particular, cell activity during the delay period was more strongly related to the intended movement expressed in arm-related coordinates than in gaze-related coordinates. Under the same experimental conditions, many cells in medial parietal cortex exhibited much stronger gaze-related modulation and expressed intended movement in gaze-related coordinates. In summary, gaze direction-related modulation of cell activity is indeed expressed in PMd during the brief fixations that occur in natural oculomotor behavior, but its overall effect on cell activity is modest.

Neuronal processes that link object vision with motor preparation in the monkey dorsal premotor cortex

To investigate the difficulty that patients with Parkinson’s disease (PD) have in performing fast movements, we used H215O PET to study regional cerebral blood flow (rCBF) associated with performance of a simple predictive visuomanual tracking task at three different velocities. Tracking movements in PD patients (versus tracking with the eyes alone) were associated with a general underactivation of the areas normally activated by the task (sensorimotor cortex contralateral to the moving arm, bilateral dorsal premotor cortices, and ipsilateral cerebellum). Presupplementary motor cortex (pre-SMA) ipsilateral to the moving arm had greater than normal movement-related activations. Increasing movement velocity led to increased rCBF in multiple premotor and parietal cortical areas and basal ganglia in the patients as opposed to the few cerebral locations that are normally velocity-related. The functional correlates of PD bradykinesia are: (1) impaired recruitment of cortical and subcortical systems that normally regulate kinematic parameters of movement such as velocity; and (2) increased recruitment of multiple premotor areas including both regions specialized for visuomotor control (ventral premotor and parietal cortices) and some that are not (pre-SMA). The overactivation of cortical regions observed in patients may be functional correlates of compensatory mechanisms and/or impaired suppression as a facet of the primary pathophysiology of PD.

Neuronal process for increasing the “fineness” of force-coding in the monkey dorsal premotor cortex

Neuronal process for increasing the “fineness” of force-coding in the monkey dorsal premotor cortex

1568 Neuronal process for increasing the “fineness” of force-coding in the monkey dorsal premotor cortex

1568 Neuronal process for increasing the “fineness” of force-coding in the monkey dorsal premotor cortex