High accuracy decoding of movement target direction in non-human primates based on common spatial patterns of local field potentials

Background

The current development of brain-machine interface technology is limited, among other factors, by concerns about the long-term stability of single- and multi-unit neural signals. In addition, the understanding of the relation between potentially more stable neural signals, such as local field potentials, and motor behavior is still in its early stages.

Methodology/Principal Findings

We tested the hypothesis that spatial correlation patterns of neural data can be used to decode movement target direction. In particular, we examined local field potentials (LFP), which are thought to be more stable over time than single unit activity (SUA). Using LFP recordings from chronically implanted electrodes in the dorsal premotor and primary motor cortex of non-human primates trained to make arm movements in different directions, we made the following observations: (i) it is possible to decode movement target direction with high fidelity from the spatial correlation patterns of neural activity in both primary motor (M1) and dorsal premotor cortex (PMd); (ii) the decoding accuracy of LFP was similar to the decoding accuracy obtained with the set of SUA recorded simultaneously; (iii) directional information varied with the LFP frequency sub-band, being greater in low (0.3–4 Hz) and high (48–200 Hz) frequency bands than in intermediate bands; (iv) the amount of directional information was similar in M1 and PMd; (v) reliable decoding was achieved well in advance of movement onset; and (vi) LFP were relatively stable over a period of one week.

Conclusions/Significance

The results demonstrate that the spatial correlation patterns of LFP signals can be used to decode movement target direction. This finding suggests that parameters of movement, such as target direction, have a stable spatial distribution within primary motor and dorsal premotor cortex, which may be used for brain-machine interfaces.     

Spike Firing and IPSPs in Layer V Pyramidal Neurons during Beta Oscillations in Rat Primary Motor Cortex (M1) In Vitro

Beta frequency oscillations (10–35 Hz) in motor regions of cerebral cortex play an important role in stabilising and suppressing unwanted movements, and become intensified during the pathological akinesia of Parkinson''s Disease. We have used a cortical slice preparation of rat brain, combined with concurrent intracellular and field recordings from the primary motor cortex (M1), to explore the cellular basis of the persistent beta frequency (27–30 Hz) oscillations manifest in local field potentials (LFP) in layers II and V of M1 produced by continuous perfusion of kainic acid (100 nM) and carbachol (5 µM). Spontaneous depolarizing GABA-ergic IPSPs in layer V cells, intracellularly dialyzed with KCl and IEM1460 (to block glutamatergic EPSCs), were recorded at −80 mV. IPSPs showed a highly significant (P< 0.01) beta frequency component, which was highly significantly coherent with both the Layer II and V LFP oscillation (which were in antiphase to each other). Both IPSPs and the LFP beta oscillations were abolished by the GABA_A antagonist bicuculline. Layer V cells at rest fired spontaneous action potentials at sub-beta frequencies (mean of 7.1+1.2 Hz; n = 27) which were phase-locked to the layer V LFP beta oscillation, preceding the peak of the LFP beta oscillation by some 20 ms. We propose that M1 beta oscillations, in common with other oscillations in other brain regions, can arise from synchronous hyperpolarization of pyramidal cells driven by synaptic inputs from a GABA-ergic interneuronal network (or networks) entrained by recurrent excitation derived from pyramidal cells. This mechanism plays an important role in both the physiology and pathophysiology of control of voluntary movement generation.     

Anterior regions of monkey parietal cortex process visual 3D shape

The intraparietal cortex is involved in the control of visually guided actions, like reach-to-grasp movements, which require extracting the 3D shape and position of objects from 2D retinal images. Using fMRI in behaving monkeys, we investigated the role of the intraparietal cortex in processing stereoscopic information for recovering the depth structure and the position in depth of objects. We found that while several areas (CIP, LIP, and AIP on the lateral bank; PIP and MIP on the medial bank) are activated by stereoscopic stimuli, AIP and an adjoining portion of LIP are sensitive only to depth structure. Furthermore, only these two regions are sensitive to both the depth structure and the 2D shape of small objects. These results indicate that extracting 3D spatial information from stereo involves several intraparietal areas, among which AIP and anterior LIP are more specifically engaged in extracting the 3D shape of objects.     

Sensory information in local field potentials and spikes from visual and auditory cortices: time scales and frequency bands

Studies analyzing sensory cortical processing or trying to decode brain activity often rely on a combination of different electrophysiological signals, such as local field potentials (LFPs) and spiking activity. Understanding the relation between these signals and sensory stimuli and between different components of these signals is hence of great interest. We here provide an analysis of LFPs and spiking activity recorded from visual and auditory cortex during stimulation with natural stimuli. In particular, we focus on the time scales on which different components of these signals are informative about the stimulus, and on the dependencies between different components of these signals. Addressing the first question, we find that stimulus information in low frequency bands (<12 Hz) is high, regardless of whether their energy is computed at the scale of milliseconds or seconds. Stimulus information in higher bands (>50 Hz), in contrast, is scale dependent, and is larger when the energy is averaged over several hundreds of milliseconds. Indeed, combined analysis of signal reliability and information revealed that the energy of slow LFP fluctuations is well related to the stimulus even when considering individual or few cycles, while the energy of fast LFP oscillations carries information only when averaged over many cycles. Addressing the second question, we find that stimulus information in different LFP bands, and in different LFP bands and spiking activity, is largely independent regardless of time scale or sensory system. Taken together, these findings suggest that different LFP bands represent dynamic natural stimuli on distinct time scales and together provide a potentially rich source of information for sensory processing or decoding brain activity.     

Frequency Dependence of Signal Power and Spatial Reach of the Local Field Potential

Despite its century-old use, the interpretation of local field potentials (LFPs), the low-frequency part of electrical signals recorded in the brain, is still debated. In cortex the LFP appears to mainly stem from transmembrane neuronal currents following synaptic input, and obvious questions regarding the ‘locality’ of the LFP are: What is the size of the signal-generating region, i.e., the spatial reach, around a recording contact? How far does the LFP signal extend outside a synaptically activated neuronal population? And how do the answers depend on the temporal frequency of the LFP signal? Experimental inquiries have given conflicting results, and we here pursue a modeling approach based on a well-established biophysical forward-modeling scheme incorporating detailed reconstructed neuronal morphologies in precise calculations of population LFPs including thousands of neurons. The two key factors determining the frequency dependence of LFP are the spatial decay of the single-neuron LFP contribution and the conversion of synaptic input correlations into correlations between single-neuron LFP contributions. Both factors are seen to give low-pass filtering of the LFP signal power. For uncorrelated input only the first factor is relevant, and here a modest reduction (<50%) in the spatial reach is observed for higher frequencies (>100 Hz) compared to the near-DC () value of about . Much larger frequency-dependent effects are seen when populations of pyramidal neurons receive correlated and spatially asymmetric inputs: the low-frequency () LFP power can here be an order of magnitude or more larger than at 60 Hz. Moreover, the low-frequency LFP components have larger spatial reach and extend further outside the active population than high-frequency components. Further, the spatial LFP profiles for such populations typically span the full vertical extent of the dendrites of neurons in the population. Our numerical findings are backed up by an intuitive simplified model for the generation of population LFP.     

Frequency-Dependent Modulation of Regional Synchrony in the Human Brain by Eyes Open and Eyes Closed Resting-States

The eyes-open (EO) and eyes-closed (EC) states have differential effects on BOLD-fMRI signal dynamics, affecting both the BOLD oscillation frequency of a single voxel and the regional homogeneity (ReHo) of several neighboring voxels. To explore how the two resting-states modulate the local synchrony through different frequency bands, we decomposed the time series of each voxel into several components that fell into distinct frequency bands. The ReHo in each of the bands was calculated and compared between the EO and EC conditions. The cross-voxel correlations between the mean frequency and the overall ReHo of each voxel’s original BOLD series in different brain areas were also calculated and compared between the two states. Compared with the EC state, ReHo decreased with EO in a wide frequency band of 0.01–0.25 Hz in the bilateral thalamus, sensorimotor network, and superior temporal gyrus, while ReHo increased significantly in the band of 0–0.01 Hz in the primary visual cortex, and in a higher frequency band of 0.02–0.1 Hz in the higher order visual areas. The cross-voxel correlations between the frequency and overall ReHo were negative in all the brain areas but varied from region to region. These correlations were stronger with EO in the visual network and the default mode network. Our results suggested that different frequency bands of ReHo showed different sensitivity to the modulation of EO-EC states. The better spatial consistency between the frequency and overall ReHo maps indicated that the brain might adopt a stricter frequency-dependent configuration with EO than with EC.     

Frequency Dependent Alterations in Regional Homogeneity of Baseline Brain Activity in Schizophrenia

Low frequency oscillations are essential in cognitive function impairment in schizophrenia. While functional connectivity can reveal the synchronization between distant brain regions, the regional abnormalities in task-independent baseline brain activity are less clear, especially in specific frequency bands. Here, we used a regional homogeneity (ReHo) method combined with resting-state functional magnetic resonance imaging to investigate low frequency spontaneous neural activity in the three different frequency bands (slow-5∶0.01–0.027 Hz; slow-4∶0.027–0.08 Hz; and typical band: 0.01–0.08 Hz) in 69 patients with schizophrenia and 62 healthy controls. Compared with controls, schizophrenia patients exhibited decreased ReHo in the precentral gyrus, middle occipital gyrus, and posterior insula, whereas increased ReHo in the medial prefrontal cortex and anterior insula. Significant differences in ReHo between the two bands were found in fusiform gyrus and superior frontal gyrus (slow-4> slow-5), and in basal ganglia, parahippocampus, and dorsal middle prefrontal gyrus (slow-5> slow-4). Importantly, we identified significant interaction between frequency bands and groups in the inferior occipital gyrus and caudate body. This study demonstrates that ReHo changes in schizophrenia are widespread and frequency dependent.     

The grasping side of odours

Background

Research on multisensory integration during natural tasks such as reach-to-grasp is still in its infancy. Crossmodal links between vision, proprioception and audition have been identified, but how olfaction contributes to plan and control reach-to-grasp movements has not been decisively shown. We used kinematics to explicitly test the influence of olfactory stimuli on reach-to-grasp movements.

Methodology/Principal Findings

Subjects were requested to reach towards and grasp a small or a large visual target (i.e., precision grip, involving the opposition of index finger and thumb for a small size target and a power grip, involving the flexion of all digits around the object for a large target) in the absence or in the presence of an odour evoking either a small or a large object that if grasped would require a precision grip and a whole hand grasp, respectively. When the type of grasp evoked by the odour did not coincide with that for the visual target, interference effects were evident on the kinematics of hand shaping and the level of synergies amongst fingers decreased. When the visual target and the object evoked by the odour required the same type of grasp, facilitation emerged and the intrinsic relations amongst individual fingers were maintained.

Conclusions/Significance

This study demonstrates that olfactory information contains highly detailed information able to elicit the planning for a reach-to-grasp movement suited to interact with the evoked object. The findings offer a substantial contribution to the current debate about the multisensory nature of the sensorimotor transformations underlying grasping.     

Frequency Specificity of Regional Homogeneity in the Resting-State Human Brain

Resting state-fMRI studies have found that the inter-areal correlations in cortical networks concentrate within ultra-low frequencies (0.01–0.04 Hz) while long-distance connections within subcortical networks distribute over a wider frequency range (0.01–0.14 Hz). However, the frequency characteristics of regional homogeneity (ReHo) in different areas are still unclear. To examine the ReHo properties in different frequency bands, a data-driven method, Empirical Mode Decomposition (EMD), was adopted to decompose the time series of each voxel into several components with distinct frequency bands. ReHo values in each of the components were then calculated. Our results showed that ReHo in cortical areas were higher and more frequency-dependent than those in the subcortical regions. BOLD oscillations of 0.02–0.04 Hz mainly contributed to the cortical ReHo, whereas the ReHo in limbic areas involved a wider frequency range and were dominated by higher-frequency BOLD oscillations (>0.08 Hz). The frequency characteristics of ReHo are distinct between different parts of the striatum, with the frequency band of 0.04–0.1 Hz contributing the most to ReHo in caudate nucleus, and oscillations lower than 0.02 Hz contributing more to ReHo in putamen. The distinct frequency-specific ReHo properties of different brain areas may arise from the assorted cytoarchitecture or synaptic types in these areas. Our work may advance the understanding of the neural-physiological basis of local BOLD activities and the functional specificity of different brain regions.     

Localizing Movement-Related Primary Sensorimotor Cortices with Multi-Band EEG Frequency Changes and Functional MRI

Electroencephalographic (EEG) oscillations in multiple frequency bands can be observed during functional activity of the cerebral cortex. An important question is whether activity of focal areas of cortex, such as during finger movements, is tracked by focal oscillatory EEG changes. Although a number of studies have compared EEG changes to functional MRI hemodynamic responses, we can find no previous research that relates the fMRI hemodynamic activity to localization of the multiple EEG frequency changes observed in motor tasks. In the present study, five participants performed similar thumb and finger movement tasks in parallel EEG and functional MRI studies. We examined changes in five frequency bands (from 5–120 Hz) and localized them using 256 dense-array EEG (dEEG) recordings and high-resolution individual head models. These localizations were compared with fMRI localizations in the same participants. Results showed that beta-band (14–30 Hz) desynchronizations (power decreases) were the most robust effects, appearing in all individuals, consistently localized to the hand region of the primary motor cortex, and consistently aligned with fMRI localizations.     

Modulations of EEG Beta Power during Planning and Execution of Grasping Movements

Although beta oscillations (≈ 13–35 Hz) are often considered as a sensorimotor rhythm, their functional role remains debated. In particular, the modulations of beta power during preparation and execution of complex movements in different contexts were barely investigated. Here, we analysed the beta oscillations recorded with electroencephalography (EEG) in a precued grasping task in which we manipulated two critical parameters: the grip type (precision vs. side grip) and the force (high vs. low force) required to pull an object along a horizontal axis. A cue was presented 3 s before a GO signal and provided full, partial or no information about the two movement parameters. We measured beta power over the centro-parietal areas during movement preparation and execution as well as during object hold. We explored the modulations of power in relation to the amount and type of prior information provided by the cue. We also investigated how beta power was affected by the grip and force parameters.We observed an increase in beta power around the cue onset followed by a decrease during movement preparation and execution. These modulations were followed by a transient power increase during object hold. This pattern of modulations did not differ between the 4 movement types (2 grips ×2 forces). However, the amount and type of prior information provided by the cue had a significant effect on the beta power during the preparatory delay. We discuss how these results fit with current hypotheses on the functional role of beta oscillations.     

The Effects of Visual Control and Distance in Modulating Peripersonal Spatial Representation

In the presence of vision, finalized motor acts can trigger spatial remapping, i.e., reference frames transformations to allow for a better interaction with targets. However, it is yet unclear how the peripersonal space is encoded and remapped depending on the availability of visual feedback and on the target position within the individual’s reachable space, and which cerebral areas subserve such processes. Here, functional magnetic resonance imaging (fMRI) was used to examine neural activity while healthy young participants performed reach-to-grasp movements with and without visual feedback and at different distances of the target from the effector (near to the hand–about 15 cm from the starting position–vs. far from the hand–about 30 cm from the starting position). Brain response in the superior parietal lobule bilaterally, in the right dorsal premotor cortex, and in the anterior part of the right inferior parietal lobule was significantly greater during visually-guided grasping of targets located at the far distance compared to grasping of targets located near to the hand. In the absence of visual feedback, the inferior parietal lobule exhibited a greater activity during grasping of targets at the near compared to the far distance. Results suggest that in the presence of visual feedback, a visuo-motor circuit integrates visuo-motor information when targets are located farther away. Conversely in the absence of visual feedback, encoding of space may demand multisensory remapping processes, even in the case of more proximal targets.     

Oscillatory Activity in the Medial Prefrontal Cortex and Nucleus Accumbens Correlates with Impulsivity and Reward Outcome

Actions expressed prematurely without regard for their consequences are considered impulsive. Such behaviour is governed by a network of brain regions including the prefrontal cortex (PFC) and nucleus accumbens (NAcb) and is prevalent in disorders including attention deficit hyperactivity disorder (ADHD) and drug addiction. However, little is known of the relationship between neural activity in these regions and specific forms of impulsive behaviour. In the present study we investigated local field potential (LFP) oscillations in distinct sub-regions of the PFC and NAcb on a 5-choice serial reaction time task (5-CSRTT), which measures sustained, spatially-divided visual attention and action restraint. The main findings show that power in gamma frequency (50–60 Hz) LFP oscillations transiently increases in the PFC and NAcb during both the anticipation of a cue signalling the spatial location of a nose-poke response and again following correct responses. Gamma oscillations were coupled to low-frequency delta oscillations in both regions; this coupling strengthened specifically when an error response was made. Theta (7–9 Hz) LFP power in the PFC and NAcb increased during the waiting period and was also related to response outcome. Additionally, both gamma and theta power were significantly affected by upcoming premature responses as rats waited for the visual cue to respond. In a subgroup of rats showing persistently high levels of impulsivity we found that impulsivity was associated with increased error signals following a nose-poke response, as well as reduced signals of previous trial outcome during the waiting period. Collectively, these in-vivo neurophysiological findings further implicate the PFC and NAcb in anticipatory impulsive responses and provide evidence that abnormalities in the encoding of rewarding outcomes may underlie trait-like impulsive behaviour.     

Eye-Head Coordination for Visual Cognitive Processing

We investigated coordinated movements between the eyes and head (“eye-head coordination”) in relation to vision for action. Several studies have measured eye and head movements during a single gaze shift, focusing on the mechanisms of motor control during eye-head coordination. However, in everyday life, gaze shifts occur sequentially and are accompanied by movements of the head and body. Under such conditions, visual cognitive processing influences eye movements and might also influence eye-head coordination because sequential gaze shifts include cycles of visual processing (fixation) and data acquisition (gaze shifts). In the present study, we examined how the eyes and head move in coordination during visual search in a large visual field. Subjects moved their eyes, head, and body without restriction inside a 360° visual display system. We found patterns of eye-head coordination that differed those observed in single gaze-shift studies. First, we frequently observed multiple saccades during one continuous head movement, and the contribution of head movement to gaze shifts increased as the number of saccades increased. This relationship between head movements and sequential gaze shifts suggests eye-head coordination over several saccade-fixation sequences; this could be related to cognitive processing because saccade-fixation cycles are the result of visual cognitive processing. Second, distribution bias of eye position during gaze fixation was highly correlated with head orientation. The distribution peak of eye position was biased in the same direction as head orientation. This influence of head orientation suggests that eye-head coordination is involved in gaze fixation, when the visual system processes retinal information. This further supports the role of eye-head coordination in visual cognitive processing.     

iTBS-Induced LTP-Like Plasticity Parallels Oscillatory Activity Changes in the Primary Sensory and Motor Areas of Macaque Monkeys

Recently, neuromodulation techniques based on the use of repetitive transcranial magnetic stimulation (rTMS) have been proposed as a non-invasive and efficient method to induce in vivo long-term potentiation (LTP)-like aftereffects. However, the exact impact of rTMS-induced perturbations on the dynamics of neuronal population activity is not well understood. Here, in two monkeys, we examine changes in the oscillatory activity of the sensorimotor cortex following an intermittent theta burst stimulation (iTBS) protocol. We first probed iTBS modulatory effects by testing the iTBS-induced facilitation of somatosensory evoked potentials (SEP). Then, we examined the frequency information of the electrocorticographic signal, obtained using a custom-made miniaturised multi-electrode array for electrocorticography, after real or sham iTBS. We observed that iTBS induced facilitation of SEPs and influenced spectral components of the signal, in both animals. The latter effect was more prominent on the θ band (4–8 Hz) and the high γ band (55–90 Hz), de-potentiated and potentiated respectively. We additionally found that the multi-electrode array uniformity of β (13–26 Hz) and high γ bands were also afflicted by iTBS. Our study suggests that enhanced cortical excitability promoted by iTBS parallels a dynamic reorganisation of the interested neural network. The effect in the γ band suggests a transient local modulation, possibly at the level of synaptic strength in interneurons. The effect in the θ band suggests the disruption of temporal coordination on larger spatial scales.     

Information coding in a laminar computational model of cat primary visual cortex

Neural populations across cortical layers perform different computational tasks. However, it is not known whether information in different layers is encoded using a common neural code or whether it depends on the specific layer. Here we studied the laminar distribution of information in a large-scale computational model of cat primary visual cortex. We analyzed the amount of information about the input stimulus conveyed by the different representations of the cortical responses. In particular, we compared the information encoded in four possible neural codes: (1) the information carried by the firing rate of individual neurons; (2) the information carried by spike patterns within a time window; (3) the rate-and-phase information carried by the firing rate labelled by the phase of the Local Field Potentials (LFP); (4) the pattern-and-phase information carried by the spike patterns tagged with the LFP phase. We found that there is substantially more information in the rate-and-phase code compared with the firing rate alone for low LFP frequency bands (less than 30 Hz). When comparing how information is encoded across layers, we found that the extra information contained in a rate-and-phase code may reach 90 % in Layer 4, while in other layers it reaches only 60 %, compared to the information carried by the firing rate alone. These results suggest that information processing in primary sensory cortices could rely on different coding strategies across different layers.     

EEG Source Reconstruction Reveals Frontal-Parietal Dynamics of Spatial Conflict Processing

Cognitive control requires the suppression of distracting information in order to focus on task-relevant information. We applied EEG source reconstruction via time-frequency linear constrained minimum variance beamforming to help elucidate the neural mechanisms involved in spatial conflict processing. Human subjects performed a Simon task, in which conflict was induced by incongruence between spatial location and response hand. We found an early (∼200 ms post-stimulus) conflict modulation in stimulus-contralateral parietal gamma (30–50 Hz), followed by a later alpha-band (8–12 Hz) conflict modulation, suggesting an early detection of spatial conflict and inhibition of spatial location processing. Inter-regional connectivity analyses assessed via cross-frequency coupling of theta (4–8 Hz), alpha, and gamma power revealed conflict-induced shifts in cortical network interactions: Congruent trials (relative to incongruent trials) had stronger coupling between frontal theta and stimulus-contrahemifield parietal alpha/gamma power, whereas incongruent trials had increased theta coupling between medial frontal and lateral frontal regions. These findings shed new light into the large-scale network dynamics of spatial conflict processing, and how those networks are shaped by oscillatory interactions.     

Visual gaze control during peering flight manoeuvres in honeybees

As animals travel through the environment, powerful reflexes help stabilize their gaze by actively maintaining head and eyes in a level orientation. Gaze stabilization reduces motion blur and prevents image rotations. It also assists in depth perception based on translational optic flow. Here we describe side-to-side flight manoeuvres in honeybees and investigate how the bees’ gaze is stabilized against rotations during these movements. We used high-speed video equipment to record flight paths and head movements in honeybees visiting a feeder. We show that during their approach, bees generate lateral movements with a median amplitude of about 20 mm. These movements occur with a frequency of up to 7 Hz and are generated by periodic roll movements of the thorax with amplitudes of up to ±60°. During such thorax roll oscillations, the head is held close to horizontal, thereby minimizing rotational optic flow. By having bees fly through an oscillating, patterned drum, we show that head stabilization is based mainly on visual motion cues. Bees exposed to a continuously rotating drum, however, hold their head fixed at an oblique angle. This result shows that although gaze stabilization is driven by visual motion cues, it is limited by other mechanisms, such as the dorsal light response or gravity reception.     

Estimating Extracellular Spike Waveforms from CA1 Pyramidal Cells with Multichannel Electrodes

Extracellular (EC) recordings of action potentials from the intact brain are embedded in background voltage fluctuations known as the “local field potential” (LFP). In order to use EC spike recordings for studying biophysical properties of neurons, the spike waveforms must be separated from the LFP. Linear low-pass and high-pass filters are usually insufficient to separate spike waveforms from LFP, because they have overlapping frequency bands. Broad-band recordings of LFP and spikes were obtained with a 16-channel laminar electrode array (silicone probe). We developed an algorithm whereby local LFP signals from spike-containing channel were modeled using locally weighted polynomial regression analysis of adjoining channels without spikes. The modeled LFP signal was subtracted from the recording to estimate the embedded spike waveforms. We tested the method both on defined spike waveforms added to LFP recordings, and on in vivo-recorded extracellular spikes from hippocampal CA1 pyramidal cells in anaesthetized mice. We show that the algorithm can correctly extract the spike waveforms embedded in the LFP. In contrast, traditional high-pass filters failed to recover correct spike shapes, albeit produceing smaller standard errors. We found that high-pass RC or 2-pole Butterworth filters with cut-off frequencies below 12.5 Hz, are required to retrieve waveforms comparable to our method. The method was also compared to spike-triggered averages of the broad-band signal, and yielded waveforms with smaller standard errors and less distortion before and after the spike.     

Sixty Hertz Neurostimulation Amplifies Subthalamic Neural Synchrony in Parkinson’s Disease

High frequency subthalamic nucleus (STN) deep brain stimulation (DBS) improves the cardinal motor signs of Parkinson’s disease (PD) and attenuates STN alpha/beta band neural synchrony in a voltage-dependent manner. While there is a growing interest in the behavioral effects of lower frequency (60 Hz) DBS, little is known about its effect on STN neural synchrony. Here we demonstrate for the first time that during intra-operative 60 Hz STN DBS, one or more bands of resting state neural synchrony were amplified in the STN in PD. We recorded intra-operative STN resting state local field potentials (LFPs) from twenty-eight STNs in seventeen PD subjects after placement of the DBS lead (model 3389, Medtronic, Inc.) before and during three randomized neurostimulation sets (130 Hz/1.35V, 130 Hz/2V, 60 Hz/2V). During 130 Hz/2V DBS, baseline (no DBS) STN alpha (8 – 12 Hz) and beta (13 – 35 Hz) band power decreased (N=14, P < 0.001 for both), whereas during 60 Hz/2V DBS, alpha band and peak frequency power increased (P = 0.012, P = 0.007, respectively). The effect of 60 Hz/2V DBS opposed that of power-equivalent (130 Hz/1.35V) DBS (alpha: P < 0.001, beta: P = 0.006). These results show that intra-operative 60 Hz STN DBS amplified whereas 130 Hz STN DBS attenuated resting state neural synchrony in PD; the effects were frequency-specific. We demonstrate that neurostimulation may be useful as a tool to selectively modulate resting state resonant bands of neural synchrony and to investigate its influence on motor and non-motor behaviors in PD and other neuropsychiatric diseases.