[show abstract][hide abstract] ABSTRACT: Objective. Local field potentials (LFPs) that carry information about the subject's motor intention have the potential to serve as a complement or alternative to spike signals for brain-machine interfaces (BMIs). The goal of this study is to assess the utility of LFPs for BMIs by characterizing the largely unknown information coding properties of multichannel LFPs. Approach. Two monkeys were implanted, each with a 16-channel electrode array, in the parietal reach region where both LFPs and spikes are known to encode the subject's intended reach target. We examined how multichannel LFPs recorded during a reach task jointly carry reach target information, and compared the LFP performance to simultaneously recorded multichannel spikes. Main Results. LFPs yielded a higher number of channels that were informative about reach targets than spikes. Single channel LFPs provided more accurate target information than single channel spikes. However, LFPs showed significantly larger signal and noise correlations across channels than spikes. Reach target decoders performed worse when using multichannel LFPs than multichannel spikes. The underperformance of multichannel LFPs was mostly due to their larger noise correlation because noise de-correlated multichannel LFPs produced a decoding accuracy comparable to multichannel spikes. Despite the high noise correlation, decoders using LFPs in addition to spikes outperformed decoders using only spikes. Significance. These results demonstrate that multichannel LFPs could effectively complement spikes for BMI applications by yielding more informative channels. The utility of multichannel LFPs may be further augmented if their high noise correlation can be taken into account by decoders.
Journal of Neural Engineering 06/2013; 10(4):046005. · 3.28 Impact Factor
[show abstract][hide abstract] ABSTRACT: The ability to selectively process visual inputs and to decide between multiple movement options in an adaptive manner is critical for survival. Such decisions are known to be influenced by factors such as reward expectation and visual saliency. The dorsal pulvinar connects to a multitude of cortical areas that are involved in visuospatial memory and integrate information about upcoming eye movements with expected reward values. However, it is unclear whether the dorsal pulvinar is critically involved in spatial memory and reward-based oculomotor decision behavior. To examine this, we reversibly inactivated the dorsal portion of the pulvinar while monkeys performed a delayed memory saccade task that included choices between equally or unequally rewarded options. Pulvinar inactivation resulted in a delay of saccade initiation toward memorized contralesional targets but did not affect spatial memory. Furthermore, pulvinar inactivation caused a pronounced choice bias toward the ipsilesional hemifield when the reward value in the two hemifields was equal. However, this choice bias could be alleviated by placing a high reward target into the contralesional hemifield. The bias was less affected by the manipulation of relative visual saliency between the two competing targets. These results suggest that the dorsal pulvinar is involved in determining the behavioral desirability of movement goals while being less critical for spatial memory and reward processing.
Journal of Cognitive Neuroscience 04/2013; · 4.49 Impact Factor
[show abstract][hide abstract] ABSTRACT: BACKGROUND: The results from recent brain-machine interface (BMI) studies suggest that it may be more efficient to use simple arbitrary relationships between individual neuron activity and BMI movements than the complex relationship observed between neuron activity and natural movements. This idea is based on the assumption that individual neurons can be conditioned independently regardless of their natural movement association. RESULTS: We tested this assumption in the parietal reach region (PRR), an important candidate area for BMIs in which neurons encode the target location for reaching movements. Monkeys could learn to elicit arbitrarily assigned activity patterns, but the seemingly arbitrary patterns always belonged to the response set for natural reaching movements. Moreover, neurons that are free from conditioning showed correlated responses with the conditioned neurons as if they encoded common reach targets. Thus, learning was accomplished by finding reach targets (intrinsic variable of PRR neurons) for which the natural response of reach planning could approximate the arbitrary patterns. CONCLUSIONS: Our results suggest that animals learn to volitionally control single-neuron activity in PRR by preferentially exploring and exploiting their natural movement repertoire. Thus, for optimal performance, BMIs utilizing neural signals in PRR should harness, not disregard, the activity patterns in the natural sensorimotor repertoire.
Current biology: CB 02/2013; · 10.99 Impact Factor
[show abstract][hide abstract] ABSTRACT: Lesions in human posterior parietal cortex can cause optic ataxia (OA), in which reaches but not saccades to visual objects are impaired, suggesting separate visuomotor pathways for the two effectors. In monkeys, one potentially crucial area for reach control is the parietal reach region (PRR), in which neurons respond preferentially during reach planning as compared to saccade planning. However, direct causal evidence linking the monkey PRR to the deficits observed in OA is missing. We thus inactivated part of the macaque PRR, in the medial wall of the intraparietal sulcus, and produced the hallmarks of OA, misreaching for peripheral targets but unimpaired saccades. Furthermore, reach errors were larger for the targets preferred by the neural population local to the injection site. These results demonstrate that PRR is causally involved in reach-specific visuomotor pathways, and reach goal disruption in PRR can be a neural basis of OA.
[show abstract][hide abstract] ABSTRACT: Cortical neural prosthetics extract command signals from the brain with the goal to restore function in paralyzed or amputated patients. Continuous control signals can be extracted from the motor cortical areas, whereas neural activity from posterior parietal cortex (PPC) can be used to decode cognitive variables related to the goals of movement. Because typical activities of daily living comprise both continuous control tasks such as reaching, and tasks benefiting from discrete control such as typing on a keyboard, availability of both signals simultaneously would promise significant increases in performance and versatility. Here, we show that PPC can provide 3D hand trajectory information under natural conditions that would be encountered for prosthetic applications, thus allowing simultaneous extraction of continuous and discrete signals without requiring multisite surgical implants. We found that limb movements can be decoded robustly and with high accuracy from a small population of neural units under free gaze in a complex 3D point-to-point reaching task. Both animals' brain-control performance improved rapidly with practice, resulting in faster target acquisition and increasing accuracy. These findings disprove the notion that the motor cortical areas are the only candidate areas for continuous prosthetic command signals and, rather, suggests that PPC can provide equally useful trajectory signals in addition to discrete, cognitive variables. Hybrid use of continuous and discrete signals from PPC may enable a new generation of neural prostheses providing superior performance and additional flexibility in addressing individual patient needs.
Proceedings of the National Academy of Sciences 10/2012; 109(42):17075-80. · 9.74 Impact Factor
[show abstract][hide abstract] ABSTRACT: Competing models of sensorimotor computation predict different topological constraints in the brain. Some models propose population coding of particular reference frames in anatomically distinct nodes, whereas others require no such dedicated subpopulations and instead predict that regions will simultaneously code in multiple, intermediate, reference frames. Current empirical evidence is conflicting, partly due to difficulties involved in identifying underlying reference frames. Here, we independently varied the locations of hand, gaze, and target over many positions while recording from the dorsal aspect of parietal area 5. We find that the target is represented in a predominantly hand-centered reference frame here, contrasting with the relative code seen in dorsal premotor cortex and the mostly gaze-centered reference frame in the parietal reach region. This supports the hypothesis that different nodes of the sensorimotor circuit contain distinct and systematic representations, and this constrains the types of computational model that are neurobiologically relevant.
[show abstract][hide abstract] ABSTRACT: Impairments of spatial awareness and decision making occur frequently as a consequence of parietal lesions. Here we used event-related functional MRI (fMRI) in monkeys to investigate rapid reorganization of spatial networks during reversible pharmacological inactivation of the lateral intraparietal area (LIP), which plays a role in the selection of eye movement targets. We measured fMRI activity in control and inactivation sessions while monkeys performed memory saccades to either instructed or autonomously chosen spatial locations. Inactivation caused a reduction of contralesional choices. Inactivation effects on fMRI activity were anatomically and functionally specific and mainly consisted of: (i) activity reduction in the upper bank of the superior temporal sulcus (temporal parietal occipital area) for single contralesional targets, especially in the inactivated hemisphere; and (ii) activity increase accompanying contralesional choices between bilateral targets in several frontal and parieto-temporal areas in both hemispheres. There was no overactivation for ipsilesional targets or choices in the intact hemisphere. Task-specific effects of LIP inactivation on blood oxygen level-dependent activity in the temporal parietal occipital area underline the importance of the superior temporal sulcus for spatial processing. Furthermore, our results agree only partially with the influential interhemispheric competition model of spatial neglect and suggest an additional component of interhemispheric cooperation in the compensation of neglect deficits.
Proceedings of the National Academy of Sciences 05/2012; 109(21):8274-9. · 9.74 Impact Factor
[show abstract][hide abstract] ABSTRACT: Previous findings suggest the posterior parietal cortex (PPC) contributes to arm movement planning by transforming target and limb position signals into a desired reach vector. However, the neural mechanisms underlying this transformation remain unclear. In the present study we examined the responses of 109 PPC neurons as movements were planned and executed to visual targets presented over a large portion of the reaching workspace. In contrast to previous studies, movements were made without concurrent visual and somatic cues about the starting position of the hand. For comparison, a subset of neurons was also examined with concurrent visual and somatic hand position cues. We found that single cells integrated target and limb position information in a very consistent manner across the reaching workspace. Approximately two-thirds of the neurons with significantly tuned activity (42/61 and 30/46 for left and right workspaces, respectively) coded targets and initial hand positions separably, indicating no hand-centered encoding, whereas the remaining one-third coded targets and hand positions inseparably, in a manner more consistent with the influence of hand-centered coordinates. The responses of both types of neurons were largely invariant with respect to the presence or absence of visual hand position cues, suggesting their corresponding coordinate frames and gain effects were unaffected by cue integration. The results suggest that the PPC uses a consistent scheme for computing reach vectors in different parts of the workspace that is robust to changes in the availability of somatic and visual cues about hand position.
Journal of Neurophysiology 03/2012; 108(1):187-99. · 3.30 Impact Factor
[show abstract][hide abstract] ABSTRACT: Neurons in the orbitofrontal cortex (OFC) have been shown to encode subjective values, suggesting a role in preference-based decision-making, although the precise relation to choice behavior is unclear. In a repeated two-choice task, subjective values of each choice can account for aggregate choice behavior, which is the overall likelihood of choosing one option over the other. Individual choices, however, are impossible to predict with knowledge of relative subjective values alone. In this study we investigated the role of internal factors in choice behavior with a simple but novel free-choice task and simultaneous recording from individual neurons in nonhuman primate OFC. We found that, first, the observed sequences of choice behavior included periods of exceptionally long runs of each of two available options and periods of frequent switching. Neither a satiety-based mechanism nor a random selection process could explain the observed choice behavior. Second, OFC neurons encode important features of the choice behavior. These features include activity selective for exceptionally long runs of a given choice (stay selectivity) as well as activity selective for switches between choices (switch selectivity). These results suggest that OFC neural activity, in addition to encoding subjective values on a long timescale that is sensitive to satiety, also encodes a signal that fluctuates on a shorter timescale and thereby reflects some of the statistically improbable aspects of free-choice behavior.
Journal of Neurophysiology 03/2012; 107(12):3246-55. · 3.30 Impact Factor
[show abstract][hide abstract] ABSTRACT: The goal of the Caltech group is to gain insight into the processes that occur within the primate nervous system during dexterous reaching and grasping and to see whether natural recovery from local brain damage can be accelerated by artificial means. We will create computational models of the nervous system embodying this insight and explain a variety of clinically observed neurological deficits in human subjects using these models.
[show abstract][hide abstract] ABSTRACT: Traditional theories have considered decision making as a separate neural process occurring before action planning. However, recent neurophysiological studies of spatial target selection have suggested that decision making and motor planning may be performed in an integrated manner. It was proposed that multiple potential plans are concurrently formed and the ultimately selected action simultaneously emerges within the same circuits (Shadlen and Newsome, 2001; Cisek and Kalaska, 2010). In the present study, we recorded from the parietal reach region (PRR) and dorsal area 5 (area 5d) in the posterior parietal cortex (PPC) while monkeys performed a nonspatial effector (saccade vs reach) choice task. The results show that PRR encodes potential and selected reach plans whereas area 5d encodes only selected reach plans, suggesting a serial visuomotor cortical circuitry for nonspatial effector decisions. Thus, there appears to be a different flow of processing for decisions and planning for spatial target selection, which is more integrated, and nonspatial effector decisions between eye and limb movements, which are more serial.
Journal of Neuroscience 12/2011; 31(49):18130-6. · 6.91 Impact Factor
[show abstract][hide abstract] ABSTRACT: The spiking activity in the parietal reach region (PRR) represents the spatial goal of an impending reach when the reach is directed toward or away from a visual object. The local field potentials (LFPs) in this region also represent the reach goal when the reach is directed to a visual object. Thus PRR is a candidate area for reading out a patient's intended reach goals for neural prosthetic applications. For natural behaviors, reach goals are not always based on the location of a visual object, e.g., playing the piano following sheet music or moving following verbal directions. So far it has not been directly tested whether and how PRR represents reach goals in such cognitive, nonlocational conditions, and knowing the encoding properties in various task conditions would help in designing a reach goal decoder for prosthetic applications. To address this issue, we examined the macaque PRR under two reach conditions: reach goal determined by the stimulus location (direct) or shape (symbolic). For the same goal, the spiking activity near reach onset was indistinguishable between the two tasks, and thus a reach goal decoder trained with spiking activity in one task performed perfectly in the other. In contrast, the LFP activity at 20-40 Hz showed small but significantly enhanced reach goal tuning in the symbolic task, but its spatial preference remained the same. Consequently, a decoder trained with LFP activity performed worse in the other task than in the same task. These results suggest that LFP decoders in PRR should take into account the task context (e.g., locational vs. nonlocational) to be accurate, while spike decoders can robustly provide reach goal information regardless of the task context in various prosthetic applications.
Journal of Neurophysiology 11/2011; 107(3):836-49. · 3.30 Impact Factor
[show abstract][hide abstract] ABSTRACT: Local field potentials (LFPs) have shown diverse relations to the spikes across different brain areas and stimulus features, suggesting that LFP-spike relationships are highly specific to the underlying connectivity of a local network. If so, the LFP-spike relationship may vary even within one brain area under the same task condition if neurons have heterogeneous connectivity with the active input sources during the task. Here, we tested this hypothesis in the parietal reach region (PRR), which includes two distinct classes of motor goal planning neurons with different connectivity to the visual input, i.e., visuomotor neurons receive stronger visual input than motor neurons. We predicted that the visual stimulation would render both the spike response and the LFP-spike relationship different between the two neuronal subpopulations. Thus we examined how visual stimulations affect spikes, LFPs, and LFP-spike relationships in PRR by comparing their planning (delay) period activity between two conditions: with or without a visual stimulus at the reach target. Neurons were classified as visuomotor if the visual stimulation increased their firing rate, or as motor otherwise. We found that the visual stimulation increased LFP power in gamma bands >40 Hz for both classes. Moreover, confirming our prediction, the correlation between the LFP gamma power and the firing rate became higher for the visuomotor than motor neurons in the presence of visual stimulation. We conclude that LFPs vary with the stimulation condition and that the LFP-spike relationship depends on a given neuron's connectivity to the dominant input sources in a particular stimulation condition.
Journal of Neurophysiology 02/2011; 105(4):1850-60. · 3.30 Impact Factor
[show abstract][hide abstract] ABSTRACT: In the study of the neural basis of sensorimotor transformations, it has become clear that the brain does not always wait to sense external events and afterward select the appropriate responses. If there are predictable regularities in the environment, the brain begins to anticipate the timing of instructional cues and the signals to execute a response, revealing an internal representation of the sequential behavioral states of the task being performed. To investigate neural mechanisms that could represent the sequential states of a task, we recorded neural activity from two oculomotor structures implicated in behavioral timing--the supplementary eye fields (SEF) and the lateral intraparietal area (LIP)--while rhesus monkeys performed a memory-guided saccade task. The neurons of the SEF were found to collectively encode the progression of the task with individual neurons predicting and/or detecting states or transitions between states. LIP neurons, while also encoding information about the current temporal interval, were limited with respect to SEF neurons in two ways. First, LIP neurons tended to be active when the monkey was planning a saccade but not in the precue or intertrial intervals, whereas SEF neurons tended to have activity modulation in all intervals. Second, the LIP neurons were more likely to be spatially tuned than SEF neurons. SEF neurons also show anticipatory activity. The state-selective and anticipatory responses of SEF neurons support two complementary models of behavioral timing, state dependent and accumulator models, and suggest that each model describes a contribution SEF makes to timing at different temporal resolutions.
Journal of Neurophysiology 11/2010; 104(5):2831-49. · 3.30 Impact Factor
[show abstract][hide abstract] ABSTRACT: This study demonstrates that the spiking and local field potential (LFP) activity in the parietal reach region (PRR) of the macaque monkey can be jointly used to control the location of the computer cursor when the correct target location must be inferred symbolically, e.g., leftward arrow for the leftward target, etc. The average correct target acquisition rate during this brain machine control task without actual movements was 86% for the six discrete target locations when using spikes and LFPs from 16 electrodes. This performance was significantly better than using spikes or LFPs alone. These results, together with our previous findings, suggest that a single decoder based on both spikes and LFPs in PRR can robustly provide the subjects' motor intent under varying contexts for neural prosthetic applications.
Engineering in Medicine and Biology Society (EMBC), 2010 Annual International Conference of the IEEE; 10/2010
[show abstract][hide abstract] ABSTRACT: Visual signals generated by self-motion are initially represented in retinal coordinates in the early parts of the visual system. Because this information can be used by an observer to navigate through the environment, it must be transformed into body or world coordinates at later stations of the visual-motor pathway. Neurons in the dorsal aspect of the medial superior temporal area (MSTd) are tuned to the focus of expansion (FOE) of the visual image. We performed experiments to determine whether focus tuning curves in area MSTd are represented in eye coordinates or in screen coordinates (which could be head, body, or world-centered in the head-fixed paradigm used). Because MSTd neurons adjust their FOE tuning curves during pursuit eye movements to compensate for changes in pursuit and translation speed that distort the visual image, the coordinate frame was determined while the eyes were stationary (fixed gaze or simulated pursuit conditions) and while the eyes were moving (real pursuit condition). We recorded extracellular responses from 80 MSTd neurons in two rhesus monkeys (Macaca mulatta). We found that the FOE tuning curves of the overwhelming majority of neurons were aligned in an eye-centered coordinate frame in each of the experimental conditions [fixed gaze: 77/80 (96%); real pursuit: 77/80 (96%); simulated pursuit 74/80 (93%); t-test, P < 0.05]. These results indicate that MSTd neurons represent heading in an eye-centered coordinate frame both when the eyes are stationary and when they are moving. We also found that area MSTd demonstrates significant eye position gain modulation of response fields much like its posterior parietal neighbors.
Journal of Neurophysiology 10/2010; 105(1):60-8. · 3.30 Impact Factor
[show abstract][hide abstract] ABSTRACT: In this time-resolved functional magnetic resonance imaging (fMRI) study, we aimed to trace the neuronal correlates of covert planning processes that precede visually guided motor behavior. Specifically, we asked whether human posterior parietal cortex has prospective planning activity that can be distinguished from activity related to retrospective visual memory and attention. Although various electrophysiological studies in monkeys have demonstrated such motor planning at the level of parietal neurons, comparatively little support is provided by recent human imaging experiments. Rather, a majority of experiments highlights a role of human posterior parietal cortex in visual working memory and attention. We thus sought to establish a clear separation of visual memory and attention from processes related to the planning of goal-directed motor behaviors. To this end, we compared delayed-response tasks with identical mnemonic and attentional demands but varying degrees of motor planning. Subjects memorized multiple target locations, and in a random subset of trials targets additionally instructed (1) desired goals or (2) undesired goals for upcoming finger reaches. Compared with the memory/attention-only conditions, both latter situations led to a specific increase of preparatory fMRI activity in posterior parietal and dorsal premotor cortex. Thus, posterior parietal cortex has prospective plans for upcoming behaviors while considering both types of targets relevant for action: those to be acquired and those to be avoided.
Journal of Neuroscience 09/2010; 30(35):11715-25. · 6.91 Impact Factor
[show abstract][hide abstract] ABSTRACT: Spatial computations underlying the coordination of the hand and eye present formidable geometric challenges. One way for the nervous system to simplify these computations is to directly encode the relative position of the hand and the center of gaze. Neurons in the dorsal premotor cortex (PMd), which is critical for the guidance of arm-reaching movements, encode the relative position of the hand, gaze, and goal of reaching movements. This suggests that PMd can coordinate reaching movements with eye movements. Here, we examine saccade-related signals in PMd to determine whether they also point to a role for PMd in coordinating visual-motor behavior. We first compared the activity of a population of PMd neurons with a population of parietal reach region (PRR) neurons. During center-out reaching and saccade tasks, PMd neurons responded more strongly before saccades than PRR neurons, and PMd contained a larger proportion of exclusively saccade-tuned cells than PRR. During a saccade relative position-coding task, PMd neurons encoded saccade targets in a relative position code that depended on the relative position of gaze, the hand, and the goal of a saccadic eye movement. This relative position code for saccades is similar to the way that PMd neurons encode reach targets. We propose that eye movement and eye position signals in PMd do not drive eye movements, but rather provide spatial information that links the control of eye and arm movements to support coordinated visual-motor behavior.
Journal of Neuroscience 05/2010; 30(19):6527-37. · 6.91 Impact Factor
[show abstract][hide abstract] ABSTRACT: Contralateral hemispheric representation of sensory inputs (the right visual hemifield in the left hemisphere and vice versa) is a fundamental feature of primate sensorimotor organization, in particular the visuomotor system. However, many higher-order cognitive functions in humans show an asymmetric hemispheric lateralization--e.g., right brain specialization for spatial processing--necessitating a convergence of information from both hemifields. Electrophysiological studies in monkeys and functional imaging in humans have investigated space and action representations at different stages of visuospatial processing, but the transition from contralateral to unified global spatial encoding and the relationship between these encoding schemes and functional lateralization are not fully understood. Moreover, the integration of data across monkeys and humans and elucidation of interspecies homologies is hindered, because divergent findings may reflect actual species differences or arise from discrepancies in techniques and measured signals (electrophysiology vs. imaging). Here, we directly compared spatial cue and memory representations for action planning in monkeys and humans using event-related functional MRI during a working-memory oculomotor task. In monkeys, cue and memory-delay period activity in the frontal, parietal, and temporal regions was strongly contralateral. In putative human functional homologs, the contralaterality was significantly weaker, and the asymmetry between the hemispheres was stronger. These results suggest an inverse relationship between contralaterality and lateralization and elucidate similarities and differences in human and macaque cortical circuits subserving spatial awareness and oculomotor goal-directed actions.
Proceedings of the National Academy of Sciences 04/2010; 107(17):7933-8. · 9.74 Impact Factor
[show abstract][hide abstract] ABSTRACT: We studied spike responses of V1 superficial layer neurons in a perceptual decision task.
A rhesus monkey was trained to hold fixation during presentations of a three-dimensional
(structure-from-motion) object and to make a perceptual decisions in an alternative
choice paradigm while extracellular responses were obtained by single electrode
penetrations. The disparity of constituent dots was varied from trial-to-trial to render
perceptually ambiguous or unambiguous objects. Neurons with modulated disparity
responses were selected. We estimated the certainty at which the firing rate of a given V1
neuron would allow an ideal observer to predict the monkey's perceptual choice in the
task. Neuronal responses to zero-disparity (ambiguous) objects were sorted according to
the perceptual decision and the choice probability was determined for each neuron
(Britten et al., 1996). Based on the sample of n>100 neurons the firing rate ROC curves
showed significant bias from chance starting at 500 msec after the stimulus onset. The
choice probability was different from 0.5 for the significant majority of cells. The long
latency of the perceptual bias in the V1 responses suggests a feed-back from higher visual
cortical areas including MT/MST that further raises the question of V1's involvement in
perceptual awareness. (Supported by NEI and J.G. Boswell Professorship)
Acknowledgments: We thank to Christof Koch and Melissa Saenz for useful discussions