Motor-like neural dynamics in two parietal areas during arm reaching.

The classical view on motor control makes a clear distinction between the role of motor cortex in controlling muscles and parietal cortex in processing movement plans and goals. However, the strong parieto-frontal connections argue against such clear-cut separation of function. Modern dynamical approaches revealed that population activity in motor cortex can be captured by a limited number of patterns, called neural states that are preserved across diverse motor behaviors. Whether such dynamics are also present in parietal cortex is unclear. Here, we studied neural dynamics in the primate parietal cortex during arm movements and found three main states temporally coupled to the planning, execution and target holding epochs. Strikingly, as reported recently in motor cortex, execution was subdivided into distinct, arm acceleration- and deceleration-related, states. These results suggest that dynamics across parieto-frontal areas are highly consistent and hint that parietal population activity largely reflects timing constraints while motor actions unfold.

Decoding of standard and non-standard visuomotor associations from parietal cortex.

OBJECTIVE: Neural signals can be decoded and used to move neural prostheses with the purpose of restoring motor function in patients with mobility impairments. Such patients typically have intact eye movement control and visual function, suggesting that cortical visuospatial signals could be used to guide external devices. Neurons in parietal cortex mediate sensory-motor transformations, encode the spatial coordinates for reaching goals, hand position and movements, and other spatial variables. We studied how spatial information is represented at the population level, and the possibility to decode not only the position of visual targets and the plans to reach them, but also conditional, non-spatial motor responses. APPROACH: The animals first fixated one of nine targets in 3D space and then, after the target changed color, either reached toward it, or performed a non-spatial motor response (lift hand from a button). Spiking activity of parietal neurons was recorded in monkeys during two tasks. We then decoded different task related parameters. MAIN RESULTS: We first show that a maximum-likelihood estimation (MLE) algorithm trained separately in each task transformed neural activity into accurate metric predictions of target location. Furthermore, by combining MLE with a Naïve Bayes classifier, we decoded the monkey's motor intention (reach or hand lift) and the different phases of the tasks. These results show that, although V6A encodes the spatial location of a target during a delay period, the signals they carry are updated around the movement execution in an intention/motor specific way. SIGNIFICANCE: These findings show the presence of multiple levels of information in parietal cortex that could be decoded and used in brain machine interfaces to control both goal-directed movements and more cognitive visuomotor associations.

Reference frames for reaching when decoupling eye and target position in depth and direction.

Spatial representations in cortical areas involved in reaching movements were traditionally studied in a frontoparallel plane where the two-dimensional target location and the movement direction were the only variables to consider in neural computations. No studies so far have characterized the reference frames for reaching considering both depth and directional signals. Here we recorded from single neurons of the medial posterior parietal area V6A during a reaching task where fixation point and reaching targets were decoupled in direction and depth. We found a prevalent mixed encoding of target position, with eye-centered and spatiotopic representations differently balanced in the same neuron. Depth was stronger in defining the reference frame of eye-centered cells, while direction was stronger in defining that of spatiotopic cells. The predominant presence of various typologies of mixed encoding suggests that depth and direction signals are processed on the basis of flexible coordinate systems to ensure optimal motor response.

Common neural substrate for processing depth and direction signals for reaching in the monkey medial posterior parietal cortex.

Many psychophysical studies suggest that target depth and direction during reaches are processed independently, but the neurophysiological support to this view is so far limited. Here, we investigated the representation of reach depth and direction by single neurons in area V6A of the medial posterior parietal cortex (PPC) of macaques, while a fixation-to-reach task in 3-dimensional (3D) space was performed. We found that, in a substantial percentage of V6A neurons, depth and direction signals jointly influenced fixation, planning, and arm movement-related activity. While target depth and direction were equally encoded during fixation, depth tuning became stronger during arm movement planning, execution, and target holding. The spatial tuning of fixation activity was often maintained across epochs, and depth tuning persisted more than directional tuning across epochs. These findings support for the first time the existence of a common neural substrate for the encoding of target depth and direction during reaches in the PPC. Present results also highlight the presence of several types of V6A cells that process independently or jointly signals about eye position and arm movement planning and execution in order to control reaches in 3D space. A conceptual framework for the processing of depth and direction for reaching is proposed.

Body-centered, mixed, but not hand-centered coding of visual targets in the medial posterior parietal cortex during reaches in 3D space.

The frames of reference used by neurons in posterior parietal cortex (PPC) to encode spatial locations during arm reaching movements is a debated topic in modern neurophysiology. Traditionally, target location, encoded in retinocentric reference frame (RF) in caudal PPC, was assumed to be serially transformed to body-centered and then hand-centered coordinates rostrally. However, recent studies suggest that these transformations occur within a single area. The caudal PPC area V6A has been shown to represent reach targets in eye-centered, body-centered, and a combination of both RFs, but the presence of hand-centered coding has not been yet investigated. To examine this issue, 141 single neurons were recorded from V6A in 2 Macaca fascicularis monkeys while they performed a foveated reaching task in darkness. The targets were presented at different distances and lateralities from the body and were reached from initial hand positions located at different depths. Most V6A cells used body-centered, or mixed body- and hand-centered coordinates. Only a few neurons used pure hand-centered coordinates, thus clearly distinguishing V6A from nearby PPC regions. Our findings support the view of a gradual RF transformation in PPC and also highlight the impact of mixed frames of reference.

Three-dimensional eye position signals shape both peripersonal space and arm movement activity in the medial posterior parietal cortex.

Research conducted over the last decades has established that the medial part of posterior parietal cortex (PPC) is crucial for controlling visually guided actions in human and non-human primates. Within this cortical sector there is area V6A, a crucial node of the parietofrontal network involved in arm movement control in both monkeys and humans. However, the encoding of action-in-depth by V6A cells had been not studied till recently. Recent neurophysiological studies show the existence in V6A neurons of signals related to the distance of targets from the eyes. These signals are integrated, often at the level of single cells, with information about the direction of gaze, thus encoding spatial location in 3D space. Moreover, 3D eye position signals seem to be further exploited at two additional levels of neural processing: (a) in determining whether targets are located in the peripersonal space or not, and (b) in shaping the spatial tuning of arm movement related activity toward reachable targets. These findings are in line with studies in putative homolog regions in humans and together point to a role of medial PPC in encoding both the vergence angle of the eyes and peripersonal space. Besides its role in spatial encoding also in depth, several findings demonstrate the involvement of this cortical sector in non-spatial processes.

Eye position modulates the electromyographic responses of neck muscles to electrical stimulation of the superior colliculus in the alert cat.

Rapid gaze shifts are often accomplished with coordinated movements of the eyes and head, the relative amplitude of which depends on the starting position of the eyes. The size of gaze shifts is determined by the superior colliculus (SC) but additional processing in the lower brain stem is needed to determine the relative contributions of eye and head components. Models of eye-head coordination often assume that the strength of the command sent to the head controllers is modified by a signal indicative of the eye position. Evidence in favor of this hypothesis has been recently obtained in a study of phasic electromyographic (EMG) responses to stimulation of the SC in head-restrained monkeys (Corneil et al. in J Neurophysiol 88:2000-2018, 2002b). Bearing in mind that the patterns of eye-head coordination are not the same in all species and because the eye position sensitivity of phasic EMG responses has not been systematically investigated in cats, in the present study we used cats to address this issue. We stimulated electrically the intermediate and deep layers of the caudal SC in alert cats and recorded the EMG responses of neck muscles with horizontal and vertical pulling directions. Our data demonstrate that phasic, short latency EMG responses can be modulated by the eye position such that they increase as the eye occupies more and more eccentric positions in the pulling direction of the muscle tested. However, the influence of the eye position is rather modest, typically accounting for only 10-50% of the variance of EMG response amplitude. Responses evoked from several SC sites were not modulated by the eye position.

Oculomotor areas of the primate frontal lobes: a transneuronal transfer of rabies virus and [14C]-2-deoxyglucose functional imaging study.

We used the [14C]-2-deoxyglucose method to study the location and extent of primate frontal lobe areas activated for saccades and fixation and the retrograde transneuronal transfer of rabies virus to determine whether these regions are oligosynaptically connected with extraocular motoneurons. Fixation-related increases of local cerebral glucose utilization (LCGU) values were found around the fundus of the inferior limb of the arcuate sulcus (AS) just ventral to its genu, in the dorsomedial frontal cortex (DMFC), cingulate cortex, and orbitofrontal cortex. Significant increases of LCGU values were found in and around both banks of the AS, DMFC, and caudal principal, cingulate, and orbitofrontal cortices of monkeys executing visually guided saccades. All of these areas are oligosynaptically connected to extraocular motoneurons, as shown by the presence of retrogradely transneuronally labeled cells after injection of rabies virus in the lateral rectus muscle. Our data demonstrate that the arcuate oculomotor cortex occupies a region considerably larger than the classic, electrical stimulation-defined, frontal eye field. Besides a large part of the anterior bank of the AS, it includes the caudal prearcuate convexity and part of the premotor cortex in the posterior bank of the AS. They also demonstrate that the oculomotor DMFC occupies a small area straddling the ridge of the brain medial to the superior ramus of the AS. Our results support the notion that a network of several interconnected frontal lobe regions is activated during rapid, visually guided eye movements and that their output is conveyed in parallel to subcortical structures projecting to extraocular motoneurons.