Cortico-spinal modularity in the parieto-frontal system: a new perspective on action control

: Classical neurophysiology suggests that the motor cortex (MI) has a unique role in action control. In contrast, this review presents evidence for multiple parieto-frontal spinal command modules that can bypass MI. Five observations support this modular perspective: (i) the statistics of cortical connectivity demonstrate functionally-related clusters of cortical areas, defining functional modules in the premotor, cingulate, and parietal cortices; (ii) different corticospinal pathways originate from the above areas, each with a distinct range of conduction velocities; (iii) the activation time of each module varies depending on task, and different modules can be activated simultaneously; (iv) a modular architecture with direct motor output is faster and less metabolically expensive than an architecture that relies on MI, given the slow connections between MI and other cortical areas; (v) lesions of the areas composing parieto-frontal modules have different effects from lesions of MI. Here we provide examples of six cortico-spinal modules and functions they subserve: module 1) arm reaching, tool use and object construction; module 2) spatial navigation and locomotion; module 3) grasping and observation of hand and mouth actions; module 4) action initiation, motor sequences, time encoding; module 5) conditional motor association and learning, action plan switching and action inhibition; module 6) planning defensive actions. These modules can serve as a library of tools to be recombined when faced with novel tasks, and MI might serve as a recombinatory hub. In conclusion, the availability of locally-stored information and multiple outflow paths supports the physiological plausibility of the proposed modular perspective

Multiple parietal reach regions in humans: cortical representations for visual and proprioceptive feedback during on-line reaching

Reaching toward a visual target involves at least two sources of information. One is the visual feedback from the hand as it approaches the target. Another is proprioception from the moving limb, which informs the brain of the location of the hand relative to the target even when the hand is not visible. Where these two sources of information are represented in the human brain is unknown. In the present study, we investigated the cortical representations for reaching with or without visual feedback from the moving hand, using functional magnetic resonance imaging. To identify reach-dominant areas, we compared reaching with saccades. Our results show that a reach-dominant region in the anterior precuneus (aPCu), extending into medial intraparietal sulcus, is equally active in visual and nonvisual reaching. A second region, at the superior end of the parieto-occipital sulcus (sPOS), is more active for visual than for nonvisual reaching. These results suggest that aPCu is a sensorimotor area whose sensory input is primarily proprioceptive, while sPOS is a visuomotor area that receives visual feedback during reaching. In addition to the precuneus, medial, anterior intraparietal, and superior parietal cortex were also activated during both visual and nonvisual reaching, with more anterior areas responding to hand movements only and more posterior areas responding to both hand and eye movements. Our results suggest that cortical networks for reaching are differentially activated depending on the sensory conditions during reaching. This indicates the involvement of multiple parietal reach regions in humans, rather than a single homogenous parietal reach region

Cortical Mechanisms for Transsaccadic Perception of Visual Object Features

The cortical correlates for transsaccadic perception (i.e., the ability to perceive, maintain, and update information across rapid eye movements, or saccades; Irwin, 1991) have been little investigated. Previously, Dunkley et al. (2016) found evidence of transsaccadic updating of object orientation in specific intraparietal (i.e., supramarginal gyrus, SMG) and extrastriate occipital (putative V4) regions. Based on these findings, I hypothesized that transsaccadic perception may rely on a single cortical mechanism. In this dissertation, I first investigated whether activation in the previous regions would generalize to another modality (i.e., motor/grasping) for the same feature (orientation) change, using a functional magnetic resonance imaging (fMRI) event-related paradigm that involved participants grasping a three-dimensional rotatable object for either fixations or saccades. The findings from this experiment further support the role of SMG in transsaccadic updating of object orientation, and provide a novel view of traditional reach/grasp-related regions in their ability to update grasp-related signals across saccades. In the second experiment, I investigated whether parietal cortex (e.g., SMG) plays a general role in the transsaccadic perception of other low-level object features, such as spatial frequency. The results point to the engagement of a different, posteromedial extrastriate (i.e., cuneus) region for transsaccadic perception of spatial frequency changes. This indirect assessment of transsaccadic interactions for different object features suggests that feature sensitive mechanisms may exist. In the third experiment, I tested the cortical correlates directly for two object features: orientation and shape. In this experiment, only posteromedial extrastriate cortex was associated with transsaccadic feature updating in the feature discrimination task, as it showed both saccade and feature modulations. Overall, the results of these three neuroimaging studies suggest that transsaccadic perception may be brought about by more than a single, general mechanism and, instead, through multiple, feature-dependent cortical mechanisms. Specifically, the saccade system communicates with inferior parietal cortex for transsaccadic judgements of orientation in an identified object, whereas as a medial occipital system is engaged for feature judgements related to object identity

Toward a Full Prehension Decoding from Dorsomedial Area V6A

Neural prosthetics represent a promising approach to restore movements in patients affected by spinal cord lesions. To drive a full capable, brain controlled, prosthetic arm, reaching and grasping components of prehension have to be accurately reconstructed from neural activity. Neurons in the dorsomedial area V6A of macaque show sensitivity to reaching direction accounting also for depth dimension, thus encoding positions in the entire 3D space. Moreover, many neurons are sensible to grips types and wrist orientations. To assess whether these signals are adequate to drive a full capable neural prosthetic arm, we recorded spiking activity of neurons in area V6A, spike counts were used to train machine learning algorithms to reconstruct reaching and grasping. In a first work, two Macaca fascicularis monkeys were trained to perform an instructed-delay reach-to-grasp task in the dark and in the light toward objects of different shapes. The activity of 89 neurons was used to train and validate a Bayes classifier used for decoding objects and grip types. Recognition rates were well above chance level for all the epochs analyzed in this study. In a second work, monkeys were trained to perform reaches to targets located at various depths and directions and the classifier was tested whether it could correctly predict the reach goal position from V6A signals. The reach goal location was reliably decoded with accuracy close to optimal (>90%) throughout the task. Together these results, show a reliable decoding of hand grips and spatial location of reaching goals in the same area, suggesting that V6A is a suitable site to decode the entire prehension action with obvious advantages in terms of implant invasiveness. This new PPC site useful for decoding both reaching and grasping opens new perspectives in the development of human brain-computer interfaces

Alpha- and beta-band oscillations subserve different processes in reactive control of limb movements

The capacity to rapidly suppress a behavioral act in response to sudden instruction to stop is a key cognitive function. This function, called reactive control, is tested in experimental settings using the stop signal task, which requires subjects to generate a movement in response to a go signal or suppress it when a stop signal appears. The ability to inhibit this movement fluctuates over time: sometimes, subjects can stop their response, and at other times, they can not. To determine the neural basis of this fluctuation, we recorded local field potentials (LFPs) in the alpha (6-12 Hz) and beta (13-35 Hz) bands from the dorsal premotor cortex of 2 nonhuman primates that were performing the task. The ability to countermand a movement after a stop signal was predicted by the activity of both bands, each purportedly representing a distinct neural process. The beta band represents the level of movement preparation; higher beta power corresponds to a lower level of movement preparation, whereas the alpha band supports a proper phasic, reactive inhibitory response: movements are inhibited when alpha band power increases immediately after a stop signal. Our findings support the function of LFP bands in generating the signatures of various neural computations that are multiplexed in the brain

Neural Correlates of Reach Planning and Execution

Humans and other primates often interact with the world by reaching and grabbing objects with their hands. This seemingly simple activity is a challenging computational problem that requires the nervous system to transform sensory input into muscle activations that move the hand appropriately through space. This dissertation investigates neural activity in the dorsal premotor cortex of the macaque monkey while simple and complex reaching movements are planned and executed. A novel virtual-reality obstacle-avoidance task is used to decorrelate the direction of the initial segment of the trajectory from the direction of the final target. An unobstructed center-out task is used as a comparison. The firing rates of many neurons are modulated by kinematic factors including hand position and movement direction. During obstacle-avoidance reaching, both the initial segment and final target directions are represented in the firing of dorsal premotor neurons. Population decoders for position, velocity and target direction were built using the indirect optimal linear estimator method, a variant of the population vector algorithm. The decoding model constructed from the direct-reaching task ultimately predicts the direction of movement, not the final target, during the planning period before movement begins. A separate decoding model predicts the target direction when the hand must move elsewhere initially. The time course of neural activity during planning suggests that the two monkeys utilized different preparatory strategies during the obstacle-avoidance task, leading to differences in performance on a subset of trials. A position-based population decoder predicts the hand trajectory during movement, anticipating the real hand position by approximately 200 ms. These findings demonstrate that multiple kinematic parameters of hand movement are represented in dorsal premotor cortex during planning and execution of voluntary reaching behavior. A simple linear decoding scheme based on roughly cosine-tuned spiking activity can extract relevant information from the population of neurons. This work contributes to the overall understanding of the factors that influence dorsal premotor cortical activity during complex reaching movements

Influence of area 5 on primary motor cortex: a paired-pulse TMS investigation in healthy adults

The neural correlates that underpin fine motor control of the hand and their connections with the primary motor cortex (M1) require further investigation. Brodmann’s area 5 located in the superior parietal lobule (SPL) is suggested to be an important cortical area involved in the processing of somatosensory input important for precision movements. Area 5 is present in monkey species capable of opposable thumb movements and it is proposed that this area evolved with the ability to execute manual behaviours such as pinch grip. Further, area 5 is dominated by the representation of the hand and forelimb, and has direct connectivity with M1 implicating its role in the control of hand movements. Few studies have investigated the function of area 5 in humans and none have examined the connectivity between area 5 and ipsilateral M1. This thesis presents a novel approach to study the influence of area 5 on M1 output in healthy and awake humans during the processing of somatosensory inputs and during performance of motor tasks involving the hand. Using paired pulse transcranial magnetic stimulation over left area 5 and ipsilateral M1, the connections between the two cortical loci was probed. It was hypothesized that area 5 would facilitate M1 output at short and long latencies during the processing of tactile inputs and during the performance of motor tasks compared to rest. The current results demonstrate that changes in M1 output are task and temporally specific. Facilitation of the motor evoked potential (MEP) was present at short latency of 6 ms during the processing of somatosensory input whereas inhibition was present during conditions where the hand was performing a task with the thumb and index finger. Further, an inhibitory effect was seen at 40 ms during cutaneous stimulation. In experiments 1 and 2, there was no net influence of area 5 on M1 output observed at rest. The findings presented may have revealed a novel path with which to alter the motor output, and possibly movement of hand muscles