Local field potentials in the parietal reach region reveal mechanisms of bimanual coordination.
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ABSTRACT:
SUBMITTER: Mooshagian E
PROVIDER: S-EPMC8096826 | biostudies-literature |
REPOSITORIES: biostudies-literature
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Project description:The precise control of movement execution onset is essential for safe and autonomous cortical motor prosthetics. A recent study from the parietal reach region (PRR) suggested that the local field potentials (LFPs) in this area might be useful for decoding execution time information because of the striking difference in the LFP spectrum between the plan and execution states (Scherberger et al., 2005). More specifically, the LFP power in the 0-10 Hz band sharply rises while the power in the 20-40 Hz band falls as the state transitions from plan to execution. However, a change of visual stimulus immediately preceded reach onset, raising the possibility that the observed spectral change reflected the visual event instead of the reach onset. Here, we tested this possibility and found that the LFP spectrum change was still time locked to the movement onset in the absence of a visual event in self-paced reaches. Furthermore, we successfully trained the macaque subjects to use the LFP spectrum change as a "go" signal in a closed-loop brain-control task in which the animals only modulated the LFP and did not execute a reach. The execution onset was signaled by the change in the LFP spectrum while the target position of the cursor was controlled by the spike firing rates recorded from the same site. The results corroborate that the LFP spectrum change in PRR is a robust indicator for the movement onset and can be used for control of execution onset in a cortical prosthesis.
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Project description:Bimanual coordination is critical for a broad array of behaviors. Drummers, for example, must carefully coordinate movements of their 2 arms, sometimes beating on the same drum and sometimes on different ones. While coordinated behavior is well-studied, the early stages of planning are not well understood. In the parietal reach region (PRR) of the posterior parietal cortex (PPC), the presence of neurons that modulate when either arm moves by itself has been taken as evidence for a role in bimanual coordination. To test this notion, we recorded neurons during both unilateral and bimanual movements. We find that the activity that precedes an ipsilateral arm movement is primarily a sensory response to a target in the neuron's visual receptive field and not a plan to move the ipsilateral arm. In contrast, the activity that precedes a contralateral arm movement is the sum of a movement plan plus a sensory response. Despite not coding ipsilateral arm movements, about half of neurons discriminate between different patterns of bimanual movements. These results provide direct evidence that PRR neurons represent bimanual reach plans, and suggest that bimanual coordination originates in the sensory-to-motor processing stream prior to the motor cortex, within the PPC.
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Project description:Performing a visually guided reach requires the ability to perceive the egocentric distance of a target in three-dimensional space. Previous studies have shown that the parietal reach region (PRR) encodes the two-dimensional location of frontoparallel targets in an eye-centered reference frame. To investigate how a reach target is represented in three dimensions, we recorded the spiking activity of PRR neurons from two rhesus macaques trained to fixate and perform memory reaches to targets at different depths. Reach and fixation targets were configured to explore whether neural activity directly reflects egocentric distance as the amplitude of the required motor command, which is the absolute depth of the target, or rather the relative depth of the target with reference to fixation depth. We show that planning activity in PRR represents the depth of the reach target as a function of disparity and fixation depth, the spatial parameters important for encoding the depth of a reach goal in an eye centered reference frame. The strength of modulation by disparity is maintained across fixation depth. Fixation depth gain modulates disparity tuning while preserving the location of peak tuning features in PRR neurons. The results show that individual PRR neurons code depth with respect to the fixation point, that is, in eye centered coordinates. However, because the activity is gain modulated by vergence angle, the absolute depth can be decoded from the population activity.
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Project description:Although multisensory integration is crucial for sensorimotor function, it is unclear how visual and proprioceptive sensory cues are combined in the brain during motor behaviors. Here we characterized the effects of multisensory interactions on local field potential (LFP) activity obtained from the superior parietal lobule (SPL) as non-human primates performed a reaching task with either unimodal (proprioceptive) or bimodal (visual-proprioceptive) sensory feedback. Based on previous analyses of spiking activity, we hypothesized that evoked LFP responses would be tuned to arm location but would be suppressed on bimodal trials, relative to unimodal trials. We also expected to see a substantial number of recording sites with enhanced beta band spectral power for only one set of feedback conditions (e.g. unimodal or bimodal), as was previously observed for spiking activity. We found that evoked activity and beta band power were tuned to arm location at many individual sites, though this tuning often differed between unimodal and bimodal trials. Across the population, both evoked and beta activity were consistent with feedback-dependent tuning to arm location, while beta band activity also showed evidence of response suppression on bimodal trials. The results suggest that multisensory interactions can alter the tuning and gain of arm position-related LFP activity in the SPL.
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Project description:Neuronal activity within the premotor region HVC is tightly synchronized to, and crucial for, the articulate production of learned song in birds. Characterizations of this neural activity detail patterns of sequential bursting in small, carefully identified subsets of neurons in the HVC population. The dynamics of HVC are well described by these characterizations, but have not been verified beyond this scale of measurement. There is a rich history of using local field potentials (LFP) to extract information about behavior that extends beyond the contribution of individual cells. These signals have the advantage of being stable over longer periods of time, and they have been used to study and decode human speech and other complex motor behaviors. Here we characterize LFP signals presumptively from the HVC of freely behaving male zebra finches during song production to determine if population activity may yield similar insights into the mechanisms underlying complex motor-vocal behavior. Following an initial observation that structured changes in the LFP were distinct to all vocalizations during song, we show that it is possible to extract time-varying features from multiple frequency bands to decode the identity of specific vocalization elements (syllables) and to predict their temporal onsets within the motif. This demonstrates the utility of LFP for studying vocal behavior in songbirds. Surprisingly, the time frequency structure of HVC LFP is qualitatively similar to well-established oscillations found in both human and non-human mammalian motor areas. This physiological similarity, despite distinct anatomical structures, may give insight into common computational principles for learning and/or generating complex motor-vocal behaviors.
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Project description:The intracerebral local field potential (LFP) is a measure of brain activity that reflects the highly dynamic flow of information across neural networks. This is a composite signal that receives contributions from multiple neural sources, yet interpreting its nature and significance may be hindered by several confounding factors and technical limitations. By and large, the main factor defining the amplitude of LFPs is the geometry of the current sources, over and above the degree of synchronization or the properties of the media. As such, similar levels of activity may result in potentials that differ in several orders of magnitude in different populations. The geometry of these sources has been experimentally inaccessible until intracerebral high density recordings enabled the co-activating sources to be revealed. Without this information, it has proven difficult to interpret a century's worth of recordings that used temporal cues alone, such as event or spike related potentials and frequency bands. Meanwhile, a collection of biophysically ill-founded concepts have been considered legitimate, which can now be corrected in the light of recent advances. The relationship of LFPs to their sources is often counterintuitive. For instance, most LFP activity is not local but remote, it may be larger further from rather than close to the source, the polarity does not define its excitatory or inhibitory nature, and the amplitude may increase when source's activity is reduced. As technological developments foster the use of LFPs, the time is now ripe to raise awareness of the need to take into account spatial aspects of these signals and of the errors derived from neglecting to do so.
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Project description:Extracellular recordings are typically analysed by separating them into two distinct signals: local field potentials (LFPs) and spikes. Previous studies have shown that spikes, in the form of single-unit activity (SUA) or multiunit activity (MUA), can be inferred solely from LFPs with moderately good accuracy. SUA and MUA are typically extracted via threshold-based technique which may not be reliable when the recordings exhibit a low signal-to-noise ratio (SNR). Another type of spiking activity, referred to as entire spiking activity (ESA), can be extracted by a threshold-less, fast, and automated technique and has led to better performance in several tasks. However, its relationship with the LFPs has not been investigated. In this study, we aim to address this issue by inferring ESA from LFPs intracortically recorded from the motor cortex area of three monkeys performing different tasks. Results from long-term recording sessions and across subjects revealed that ESA can be inferred from LFPs with good accuracy. On average, the inference performance of ESA was consistently and significantly higher than those of SUA and MUA. In addition, local motor potential (LMP) was found to be the most predictive feature. The overall results indicate that LFPs contain substantial information about spiking activity, particularly ESA. This could be useful for understanding LFP-spike relationship and for the development of LFP-based BMIs.
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Project description:Deep brain stimulation (DBS) devices capable of measuring differential local field potentials ( ∂ LFP) enable neural recordings alongside clinical therapy. Efforts to identify oscillatory correlates of various brain disorders, or disease readouts, are growing but must proceed carefully to ensure readouts are not distorted by brain environment. In this report we identified, characterized, and mitigated a major source of distortion in ∂ LFP that we introduce as mismatch compression (MC). Using in vivo, in silico, and in vitro models of MC, we showed that impedance mismatches in the two recording electrodes can yield incomplete rejection of stimulation artifact and subsequent gain compression that distorts oscillatory power. We then developed and validated an opensource mitigation pipeline that mitigates the distortions arising from MC. This work enables more reliable oscillatory readouts for adaptive DBS applications.
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Project description:Local field potentials (LFPs) and spikes (SPKs) sampled at the thalamocortical recipient layers represent the inputs from the thalamus and outputs to other layers. Previous studies have shown that SPK-constructed receptive fields (RFSPK) of cortical neurons are much smaller than LFP-constructed RFs (RFLFP). The difference in cortical RFLFP and RFSPK is therefore a plausible indication of local networking. The presence of a boarder RFLFP appears due to contamination, to some degree, from remote sites. Our studies of the mouse primary auditory cortex show that the best frequencies and minimum thresholds of RFSPK and RFLFP were similar. We also observed that the RFLFP area was only slightly larger than the RFSPK area, a very different finding from previous reports. The bandwidth of RFLFP was slightly broader than that of RFSPK at all levels. These data do not support the explanation that bioelectrical signals from distant sites impact on cortical LFP through volume conduction. That the cortical LFP represents a local event is further supported by comparisons of RFSPK and RFLFP after cortical inhibition by muscimol and cortical disinhibition by bicuculine. We conclude that the difference between RFSPK (output of cortical neurons) and RFLFP (input of cortical neurons) results from intracortical processing, including cortical lateral inhibition and excitation.
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Project description: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.
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