Relationships among low-frequency local field potentials, spiking activity, and three-dimensional reach and grasp kinematics in primary motor and ventral premotor cortices
A. K. Bansal and C. E. Vargas-Irwin and W. Truccolo and J. P. Donoghue
J Neurophysiol 105 1603-19 (2011)
A prominent feature of motor cortex field potentials during movement is a distinctive low-frequency local field potential (lf-LFP) (<4 Hz), referred to as the movement event-related potential (mEP). The lf-LFP appears to be a global signal related to regional synaptic input, but its relationship to nearby output signaled by single unit spiking activity (SUA) or to movement remains to be established. Previous studies comparing information in primary motor cortex (MI) lf-LFPs and SUA in the context of planar reaching tasks concluded that lf-LFPs have more information than spikes about movement. However, the relative performance of these signals was based on a small number of simultaneously recorded channels and units, or for data averaged across sessions, which could miss information of larger-scale spiking populations. Here, we simultaneously recorded LFPs and SUA from two 96-microelectrode arrays implanted in two major motor cortical areas, MI and ventral premotor (PMv), while monkeys freely reached for and grasped objects swinging in front of them. We compared arm end point and grip aperture kinematics' decoding accuracy for lf-LFP and SUA ensembles. The results show that lf-LFPs provide enough information to reconstruct kinematics in both areas with little difference in decoding performance between MI and PMv. Individual lf-LFP channels often provided more accurate decoding of single kinematic variables than any one single unit. However, the decoding performance of the best single unit among the large population usually exceeded that of the best single lf-LFP channel. Furthermore, ensembles of SUA outperformed the pool of lf-LFP channels, in disagreement with the previously reported superiority of lf-LFP decoding. Decoding results suggest that information in lf-LFPs recorded from intracortical arrays may allow the reconstruction of reach and grasp for real-time neuroprosthetic applications, thus potentially supplementing the ability to decode these same features from spiking populations.
Encoding of naturalistic stimuli by local field potential spectra in networks of excitatory and inhibitory neurons
A. Mazzoni and S. Panzeri and N. K. Logothetis and N. Brunel
PLoS Comput Biol 4 e1000239 (2008)
Recordings of local field potentials (LFPs) reveal that the sensory cortex displays rhythmic activity and fluctuations over a wide range of frequencies and amplitudes. Yet, the role of this kind of activity in encoding sensory information remains largely unknown. To understand the rules of translation between the structure of sensory stimuli and the fluctuations of cortical responses, we simulated a sparsely connected network of excitatory and inhibitory neurons modeling a local cortical population, and we determined how the LFPs generated by the network encode information about input stimuli. We first considered simple static and periodic stimuli and then naturalistic input stimuli based on electrophysiological recordings from the thalamus of anesthetized monkeys watching natural movie scenes. We found that the simulated network produced stimulus-related LFP changes that were in striking agreement with the LFPs obtained from the primary visual cortex. Moreover, our results demonstrate that the network encoded static input spike rates into gamma-range oscillations generated by inhibitory-excitatory neural interactions and encoded slow dynamic features of the input into slow LFP fluctuations mediated by stimulus-neural interactions. The model cortical network processed dynamic stimuli with naturalistic temporal structure by using low and high response frequencies as independent communication channels, again in agreement with recent reports from visual cortex responses to naturalistic movies. One potential function of this frequency decomposition into independent information channels operated by the cortical network may be that of enhancing the capacity of the cortical column to encode our complex sensory environment.
LFP power spectra in V1 cortex: the graded effect of stimulus contrast
J. A. Henrie and R. Shapley
J Neurophysiol 94 479-90 (2005)
We recorded local field potentials (LFPs) and single-unit activity simultaneously in the macaque primary visual cortex (V1) and studied their responses to drifting sinusoidal gratings that were chosen to be "optimal" for the single units. Over all stimulus conditions, the LFP spectra have much greater power in the low-frequency band (< or = 10 Hz) than higher frequencies and can be described as "1/f." Analysis of the total power limited to the low, gamma (25-90 Hz), or broad (8-240 Hz) frequency bands of the LFP as a function of stimulus contrast indicates that the LFP power gradually increases with stimulus strength across a wide band in a manner roughly comparable to the increase in the simultaneously recorded spike activity. However, the low-frequency band power remains approximately constant across all stimulus contrasts. More specifically the gamma-band LFP power increases differentially more with respect to baseline than either higher or lower bands as stimulus contrast increases. At the highest stimulus contrasts, we report as others have previously, that the power spectrum of the LFP typically contains an obvious peak in the gamma-frequency band. The gamma-band peak emerges from the overall broadband enhancement in LFP power at stimulus contrasts where most single units' responses have begun to saturate. The temporal/spectral structures of the LFP located in the gamma band-which become most evident at the highest contrasts-provide additional constraints on potential mechanisms underlying the stimulus response properties of spiking neurons in V1.
Local field potentials indicate network state and account for neuronal response variability
R. C. Kelly and M. A. Smith and R. E. Kass and T. S. Lee
J Comput Neurosci 29 567-79 (2010)
Multineuronal recordings have revealed that neurons in primary visual cortex (V1) exhibit coordinated fluctuations of spiking activity in the absence and in the presence of visual stimulation. From the perspective of understanding a single cell's spiking activity relative to a behavior or stimulus, these network fluctuations are typically considered to be noise. We show that these events are highly correlated with another commonly recorded signal, the local field potential (LFP), and are also likely related to global network state phenomena which have been observed in a number of neural systems. Moreover, we show that attributing a component of cell firing to these network fluctuations via explicit modeling of the LFP improves the recovery of cell properties. This suggests that the impact of network fluctuations may be estimated using the LFP, and that a portion of this network activity is unrelated to the stimulus and instead reflects ongoing cortical activity. Thus, the LFP acts as an easily accessible bridge between the network state and the spiking activity.
The local and non-local components of the local field potential in awake primate visual cortex
T. J. Gawne
J Comput Neurosci 29 615-23 (2010)
The Local Field Potential (LFP) is the analog signal recorded from a microelectrode inserted into cortex, typically in the frequency band of approximately 1 to 200 Hz. Here visual stimuli were flashed on in the receptive fields of primary visual cortical neurons in awake behaving macaques, and both isolated single units (neurons) and the LFP signal were recorded from the same unipolar microelectrode. The fall-off of single unit activity as a visual stimulus was moved from near the center to near the edge of the receptive field paralleled the fall-off of the stimulus-locked (evoked) LFP response. This suggests that the evoked LFP strongly reflects local neuronal activity. However, the evoked LFP could be significant even when the visual stimulus was completely outside the receptive field and the single unit response had fallen to zero, although this phenomenon was variable. Some of the non-local components of the LFP may be related to the slow distributed, or non-retinotopic, LFP signal previously observed in anesthetized animals. The induced (not time-locked to stimulus onset) component of the LFP showed significant increases only for stimuli within the receptive field of the single units. While the LFP primarily reflects local neuronal activity, it can also reflect neuronal activity at more distant sites, although these non-local components are typically more variable, slower, and weaker than the local components.
Spatial spread of the local field potential and its laminar variation in visual cortex
D. Xing and C.-I. Yeh and R. M. Shapley
J Neurosci 29 11540-9 (2009)
We developed a new method to estimate the spatial extent of summation, the cortical spread, of the local field potential (LFP) throughout all layers of macaque primary visual cortex V1 by taking advantage of the V1 retinotopic map. We mapped multi-unit activity and LFP visual responses with sparse-noise at several cortical sites simultaneously. The cortical magnification factor near the recording sites was precisely estimated by track reconstruction. The new method combined experimental measurements together with a model of signal summation to obtain the cortical spread of the LFP. This new method could be extended to cortical areas that have topographic maps such as S1 or A1, and to cortical areas without functional columnar maps, such as rodent visual cortex. In macaque V1, the LFP was the sum of signals from a very local region, the radius of which was on average 250 microm. The LFP's cortical spread varied across cortical layers, reaching a minimum value of 120 microm in layer 4B. An important functional consequence of the small cortical spread of the LFP is that the visual field maps of LFP and MUA recorded at a single electrode site were very similar. The similar spatial scale of the visual responses, the restricted cortical spread, and their laminar variation led to new insights about the sources and possible applications of the LFP.
Sensory information in local field potentials and spikes from visual and auditory cortices: time scales and frequency bands
A. Belitski and S. Panzeri and C. Magri and N. K. Logothetis and C. Kayser
J Comput Neurosci 29 533-45 (2010)
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.
The subthreshold relation between cortical local field potential and neuronal firing unveiled by intracellular recordings in awake rats
M. Okun and A. Naim and I. Lampl
J Neurosci 30 4440-8 (2010)
In most of the in vivo electrophysiological studies of cortical processing, which are extracellular, the spike-triggered local field potential average (LFP STA) is the measure used to estimate the correlation between the synaptic inputs of individual neuron and the local population. To understand how the magnitude and shape of LFP STA reflect the underlying correlation of synaptic activities, the membrane potential of the firing neuron has to be recorded together with the LFP. Using intracellular recordings from the cortex of awake rats, we found that for a large range of firing rates and for different behavioral states, the LFP STA represents both in its waveform and its magnitude the cross-correlation between the membrane potential of the neuron and the LFP. This data, supported by further analysis, suggests that LFP STA does not represent large network events specific to the spike times, but rather the synchrony between the mean synaptic activity of the population and the membrane potential of the single neuron, present both around spike times and in the intervals between spikes. Furthermore, it introduces a novel interpretation of the available data from unit and LFP extracellular recording experiments.
Attention reduces stimulus-driven gamma frequency oscillations and spike field coherence in V1
M. Chalk and J. L. Herrero and M. A. Gieselmann and L. S. Delicato and S. Gotthardt and A. Thiele
Neuron 66 114-25 (2010)
Rhythmic activity of neuronal ensembles has been proposed to play an important role in cognitive functions such as attention, perception, and memory. Here we investigate whether rhythmic activity in V1 of the macaque monkey (macaca mulatta) is affected by top-down visual attention. We measured the local field potential (LFP) and V1 spiking activity while monkeys performed an attention-demanding detection task. We show that gamma oscillations were strongly modulated by the stimulus and by attention. Stimuli that engaged inhibitory mechanisms induced the largest gamma LFP oscillations and the largest spike field coherence. Directing attention toward a visual stimulus at the receptive field of the recorded neurons decreased LFP gamma power and gamma spike field coherence. This decrease could reflect an attention-mediated reduction of surround inhibition. Changes in synchrony in V1 would thus be a byproduct of reduced inhibitory drive, rather than a mechanism that directly aids perceptual processing.
Estimating the contribution of assembly activity to cortical dynamics from spike and population measures
M. Denker and A. Riehle and M. Diesmann and S. Grün
J Comput Neurosci 29 599-613 (2010)
The hypothesis that cortical networks employ the coordinated activity of groups of neurons, termed assemblies, to process information is debated. Results from multiple single-unit recordings are not conclusive because of the dramatic undersampling of the system. However, the local field potential (LFP) is a mesoscopic signal reflecting synchronized network activity. This raises the question whether the LFP can be employed to overcome the problem of undersampling. In a recent study in the motor cortex of the awake behaving monkey based on the locking of coincidences to the LFP we determined a lower bound for the fraction of spike coincidences originating from assembly activation. This quantity together with the locking of single spikes leads to a lower bound for the fraction of spikes originating from any assembly activity. Here we derive a statistical method to estimate the fraction of spike synchrony caused by assemblies-not its lower bound-from the spike data alone. A joint spike and LFP surrogate data model demonstrates consistency of results and the sensitivity of the method. Combining spike and LFP signals, we obtain an estimate of the fraction of spikes resulting from assemblies in the experimental data.
Correcting the bias of spike field coherence estimators due to a finite number of spikes
D. W. Grasse and K. A. Moxon
J Neurophysiol 104 548-58 (2010)
The coherence between oscillatory activity in local field potentials (LFPs) and single neuron action potentials, or spikes, has been suggested as a neural substrate for the representation of information. The power spectrum of a spike-triggered average (STA) is commonly used to estimate spike field coherence (SFC). However, when a finite number of spikes is used to construct the STA, the coherence estimator is biased. We introduce here a correction for the bias imposed by the limited number of spikes available in experimental conditions. In addition, we present an alternative method for estimating SFC from an STA by using a filter bank approach. This method is shown to be more appropriate in some analyses, such as comparing coherence across frequency bands. The proposed bias correction is a linear transformation derived from an idealized model of spike-field interaction but is shown to hold in more realistic settings. Uncorrected and corrected SFC estimates from both estimation methods are compared across multiple simulated spike-field models and experimentally collected data. The bias correction was shown to reduce the bias of the estimators, but add variance. However, the corrected estimates had a reduced or unchanged mean squared error in the majority of conditions evaluated. The bias correction provides an effective way to reduce bias in an SFC estimator without increasing the mean squared error.
Frequency-dependent attentional modulation of local field potential signals in macaque area MT
P. S. Khayat and R. Niebergall and J. C. Martinez-Trujillo
J Neurosci 30 7037-48 (2010)
Visual attention modulates neuronal responses in primate motion processing area MT. However, whether it modulates the strength local field potentials (LFP-power) within this area remains unexplored, as well as how this modulation relates to the one of the neurons' response. We investigated these issues by simultaneously recording LFPs and neuronal responses evoked by moving random dot patterns of varying direction and contrast in area MT of two male monkeys (Macaca mulatta) during different behavioral conditions. We found that: (1) LFP-power in the gamma (30-120 Hz), but not in the delta (2-4 Hz), (4-8 Hz), alpha (8-12 Hz), beta(1) (12-20 Hz), and beta(2) (20-30 Hz) frequency bands, was tuned for motion direction and contrast, similarly to the neurons' response, (2) shifting attention into a neuron's receptive field (RF) decreased LFP-power in the bands below 30 Hz (except the band), whereas shifting attention to a stimulus motion direction outside the RF had no effect in these bands, (3) LFP-power in the gamma band, however, exhibited both spatial- and motion direction-dependent attentional modulation (increase or decrease), which was highly correlated with the modulation of the neurons' response. These results demonstrate that in area MT, shifting attention into the RFs of neurons in the vicinity of the recording electrode, or to the direction of a moving stimulus located far away from these RFs, distinctively modulates LFP-power in the various frequency bands. They further suggest differences in the neural mechanisms underlying these types of attentional modulation of visual processing.
Intrinsic dendritic filtering gives low-pass power spectra of local field potentials
H. Lindén and K. H. Pettersen and G. T. Einevoll
J Comput Neurosci 29 423-44 (2010)
The local field potential (LFP) is among the most important experimental measures when probing neural population activity, but a proper understanding of the link between the underlying neural activity and the LFP signal is still missing. Here we investigate this link by mathematical modeling of contributions to the LFP from a single layer-5 pyramidal neuron and a single layer-4 stellate neuron receiving synaptic input. An intrinsic dendritic low-pass filtering effect of the LFP signal, previously demonstrated for extracellular signatures of action potentials, is seen to strongly affect the LFP power spectra, even for frequencies as low as 10 Hz for the example pyramidal neuron. Further, the LFP signal is found to depend sensitively on both the recording position and the position of the synaptic input: the LFP power spectra recorded close to the active synapse are typically found to be less low-pass filtered than spectra recorded further away. Some recording positions display striking band-pass characteristics of the LFP. The frequency dependence of the properties of the current dipole moment set up by the synaptic input current is found to qualitatively account for several salient features of the observed LFP. Two approximate schemes for calculating the LFP, the dipole approximation and the two-monopole approximation, are tested and found to be potentially useful for translating results from large-scale neural network models into predictions for results from electroencephalographic (EEG) or electrocorticographic (ECoG) recordings.
Directed coupling in local field potentials of macaque v4 during visual short-term memory revealed by multivariate autoregressive models
G. M. Hoerzer and S. Liebe and A. Schloegl and N. K. Logothetis and G. Rainer
Front Comput Neurosci 4 14 (2010)
Processing and storage of sensory information is based on the interaction between different neural populations rather than the isolated activity of single neurons. In order to characterize the dynamic interaction and transient cooperation of sub-circuits within a neural network, multivariate autoregressive (MVAR) models have proven to be an important analysis tool. In this study, we apply directed functional coupling based on MVAR models and describe the temporal and spatial changes of functional coupling between simultaneously recorded local field potentials in extrastriate area V4 during visual memory. Specifically, we compare the strength and directional relations of coupling based on generalized partial directed coherence (GPDC) measures while two rhesus monkeys perform a visual short-term memory task. In both monkeys we find increases in theta power during the memory period that are accompanied by changes in directed coupling. These interactions are most prominent in the low frequency range encompassing the theta band (3-12 Hz) and, more importantly, are asymmetric between pairs of recording sites. Furthermore, we find that the degree of interaction decreases as a function of distance between electrode positions, suggesting that these interactions are a predominantly local phenomenon. Taken together, our results show that directed coupling measures based on MVAR models are able to provide important insights into the spatial and temporal formation of local functionally coupled ensembles during visual memory in V4. Moreover, our findings suggest that visual memory is accompanied not only by a temporary increase of oscillatory activity in the theta band, but by a direction-dependent change in theta coupling, which ultimately represents a change in functional connectivity within the neural circuit.
Which elements of the mammalian central nervous system are excited by low current stimulation with microelectrodes?
F. Rattay and C. Wenger
Neuroscience 170 399-407 (2010)
Low current cortex stimulation produces a sparse and distributed set of activated cells often with distances of several hundred micrometers between cell bodies and the microelectrode. A modeling study based on recently measured densities of high threshold sodium channels Nav1.2 in dendrites and soma and low threshold sodium channels Nav1.6 in the axon shall identify spike initiation sites including a discussion on dendritic spikes. Varying excitability along the neural axis has been observed while studying different electrode positions and configurations. Although the axon initial segment (AIS) and nodes of Ranvier are most excitable, many thin axons and dendrites which are likely to be close to the electrode in the densely packed cortical regions are also proper candidates for spike initiation sites. Cathodic threshold ratio for thin axons and dendrites is about 1:3, whereas 0.2 mum diameter axons passing the electrode tip in 10 mum distance can be activated by 100 mus pulses with 2.6 muA. Direct cathodic excitation of dendrites requires a minimum electrode-fiber distance, which increases with dendrite diameter. Therefore thin dendrites can profit from the stronger electrical field close to the electrode but low current stimulation cannot activate large diameter dendrites, contrary to the inverse recruitment order known from peripheral nerve stimulation. When local depolarization fails to generate a dendritic spike, stimulation is possible via intracellular current flow that initiates an action potential, for example 200 mum distant in the low threshold AIS or in certain cases at the distal dendrite ending. Beside these exceptions, spike initiation site for cathodic low current stimulation appears rather close to the electrode.
Performance monitoring local field potentials in the medial frontal cortex of primates: supplementary eye field
E. E. Emeric and M. Leslie and P. Pouget and J. D. Schall
J Neurophysiol 104 1523-37 (2010)
We describe intracranial local field potentials (LFPs) recorded in the supplementary eye field (SEF) of macaque monkeys performing a saccade countermanding task. The most prominent feature at 90\% of the sites was a negative-going polarization evoked by a contralateral visual target. At roughly 50\% of sites a negative-going polarization was observed preceding saccades, but in stop signal trials this polarization was not modulated in a manner sufficient to control saccade initiation. When saccades were canceled in stop signal trials, LFP modulation increased with the inferred magnitude of response conflict derived from the coactivation of gaze-shifting and gaze-holding neurons. At 30\% of sites, a pronounced negative-going polarization occurred after errors. This negative polarity did not appear in unrewarded correct trials. Variations of response time with trial history were not related to any features of the LFP. The results provide new evidence that error-related and conflict-related but not feedback-related signals are conveyed by the LFP in the macaque SEF and are important for identifying the generator of the error-related negativity.
Simultaneous recording of ECoG and intracortical neuronal activity using a flexible multichannel electrode-mesh in visual cortex
H. Toda and T. Suzuki and H. Sawahata and K. Majima and Y. Kamitani and I. Hasegawa
Neuroimage 54 203-12 (2011)
Electrocorticogram (ECoG) is a well-balanced methodology for stably mapping brain surface local field potentials (LFPs) over a wide cortical region with high signal fidelity and minimal invasiveness to the brain tissue. To directly compare surface ECoG signals with intracortical neuronal activity immediately underneath, we fabricated a flexible multichannel electrode array with mesh-form structure using micro-electro-mechanical systems. A Parylene-C-based "electrode-mesh" for rats contained a 6×6 gold electrode array with 1-mm interval. Specifically, the probe had 800×800 μm(2) fenestrae in interelectrode spaces, through which simultaneous penetration of microelectrode was capable. This electrode-mesh was placed acutely or chronically on the dural/pial surface of the visual cortex of Long-Evans rats for up to 2 weeks. We obtained reliable trial-wise profiles of visually evoked ECoG signals through individual eye stimulation. Visually evoked ECoG signals from the electrode-mesh exhibited as well or larger signal amplitudes as intracortical LFPs and less across-trial variability than conventional silver-ball ECoG. Ocular selectivity of ECoG responses was correlated with that of intracortical spike/LFP activities. Moreover, single-trial ECoG signals carried sufficient information for predicting the stimulated eye with a correct performance approaching 90\%, and the decoding was significantly generalized across sessions over 6 hours. Electrode impedance or signal quality did not obviously deteriorate for 2 weeks following implantation. These findings open up a methodology to directly explore ECoG signals with reference to intracortical neuronal sources and would provide a key to developing minimally invasive next-generation brain-machine interfaces.
Evoked potentials in motor cortical local field potentials reflect task timing and behavioral performance
B. E. Kilavik and J. Confais and A. Ponce-Alvarez and M. Diesmann and A. Riehle
J Neurophysiol 104 2338-51 (2010)
Evoked potentials (EPs) are observed in motor cortical local field potentials (LFPs) during movement execution (movement-related potentials [MRPs]) and in response to relevant visual cues (visual evoked potentials [VEPs]). Motor cortical EPs may be directionally selective, but little is known concerning their relation to other aspects of motor behavior, such as task timing and performance. We recorded LFPs in motor cortex of two monkeys during performance of a precued arm-reaching task. A time cue at the start of each trial signaled delay duration and thereby the pace of the task and the available time for movement preparation. VEPs and MRPs were strongly modulated by the delay duration, VEPs being systematically larger in short-delay trials and MRPs larger in long-delay trials. Despite these systematic modulations related to the task timing, directional selectivity was similar in short and long trials. The behavioral reaction time was positively correlated with MRP size and negatively correlated with VEP size, within sessions. In addition, the behavioral performance improved across sessions, in parallel with a slow decrease in the size of VEPs and MRPs. Our results clearly show the strong influence of the behavioral context and performance on motor cortical population activity during movement preparation and execution.
Decoding stimulus-reward pairing from local field potentials recorded from monkey visual cortex
N. V. Manyakov and R. Vogels and M. M. Van Hulle
IEEE Trans Neural Netw 21 1892-902 (2010)
Single-trial decoding of brain recordings is a real challenge, since it pushes the signal-to-noise ratio issue to the limit. In this paper, we concentrate on the single-trial decoding of stimulus-reward pairing from local field potentials (LFPs) recorded chronically in the visual cortical area V4 of monkeys during a perceptual conditioning task. We developed a set of physiologically meaningful features that can classify and monitor the monkey's training performance. One of these features is based on the recently discovered propagation of waves of LFPs in the visual cortex. Time-frequency features together with spatial features (phase synchrony and wave propagation) yield, after applying a feature selection procedure, an exceptionally good single-trial classification performance, even when using a linear classifier.
Comparisons of the dynamics of local field potential and multiunit activity signals in macaque visual cortex
S. P. Burns and D. Xing and R. M. Shapley
J Neurosci 30 13739-49 (2010)
The local field potential (LFP) and multiunit activity (MUA) are extracellularly recorded signals that describe local neuronal network dynamics. In our experiments, the LFP and MUA, recorded from the same electrode in macaque primary visual cortex V1 in response to drifting grating visual stimuli, were evaluated on coarse timescales (∼1-5 s) and fine timescales (<0.1 s). On coarse timescales, MUA and the LFP both produced sustained visual responses to optimal and non-optimal oriented visual stimuli. The sustainedness of the two signals across the population of recording sites was correlated (correlation coefficient, ∼0.4). At most recording sites, the MUA was at least as sustained as the LFP and significantly more sustained for optimal orientations. In previous literature, the blood oxygen level-dependent (BOLD) signal of functional magnetic resonance imaging studies was found to be more strongly correlated with the LFP than with the MUA as a result of the lack of sustained response in the MUA signal. Because we found that MUA was as sustained as the LFP, MUA may also be correlated with BOLD. On fine timescales, we computed the coherence between the LFP and MUA over the frequency range 10-150 Hz. The LFP and MUA were weakly but significantly coherent (∼0.14) in the gamma band (20-90 Hz). The amount of gamma-band coherence was correlated with the power in the gamma band of the LFP. The data were consistent with the proposal that the LFP and MUA are generated in a noisy, resonant cortical network.
Removal of spurious correlations between spikes and local field potentials
T. P. Zanos and P. J. Mineault and C. C. Pack
J Neurophysiol 105 474-86 (2011)
Single neurons carry out important sensory and motor functions related to the larger networks in which they are embedded. Understanding the relationships between single-neuron spiking and network activity is therefore of great importance and the latter can be readily estimated from low-frequency brain signals known as local field potentials (LFPs). In this work we examine a number of issues related to the estimation of spike and LFP signals. We show that spike trains and individual spikes contain power at the frequencies that are typically thought to be exclusively related to LFPs, such that simple frequency-domain filtering cannot be effectively used to separate the two signals. Ground-truth simulations indicate that the commonly used method of estimating the LFP signal by low-pass filtering the raw voltage signal leads to artifactual correlations between spikes and LFPs and that these correlations exert a powerful influence on popular metrics of spike-LFP synchronization. Similar artifactual results were seen in data obtained from electrophysiological recordings in macaque visual cortex, when low-pass filtering was used to estimate LFP signals. In contrast LFP tuning curves in response to sensory stimuli do not appear to be affected by spike contamination, either in simulations or in real data. To address the issue of spike contamination, we devised a novel Bayesian spike removal algorithm and confirmed its effectiveness in simulations and by applying it to the electrophysiological data. The algorithm, based on a rigorous mathematical framework, outperforms other methods of spike removal on most metrics of spike-LFP correlations. Following application of this spike removal algorithm, many of our electrophysiological recordings continued to exhibit spike-LFP correlations, confirming previous reports that such relationships are a genuine aspect of neuronal activity. Overall, these results show that careful preprocessing is necessary to remove spikes from LFP signals, but that when effective spike removal is used, spike-LFP correlations can potentially yield novel insights about brain function.
High accuracy decoding of movement target direction in non-human primates based on common spatial patterns of local field potentials
N. F. Ince and R. Gupta and S. Arica and A. H. Tewfik and J. Ashe and G. Pellizzer
PLoS One 5 e14384 (2010)
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.
Effects of visual stimulation on LFPs, spikes, and LFP-spike relations in PRR
E. J. Hwang and R. A. Andersen
J Neurophysiol 105 1850-60 (2011)
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.
Synchronization between the end stages of the dorsal and the ventral visual stream
B.-E. Verhoef and R. Vogels and P. Janssen
J Neurophysiol 105 2030-42 (2011)
The end stage areas of the ventral (IT) and the dorsal (AIP) visual streams encode the shape of disparity-defined three-dimensional (3D) surfaces. Recent anatomical tracer studies have found direct reciprocal connections between the 3D-shape selective areas in IT and AIP. Whether these anatomical connections are used to facilitate 3D-shape perception is still unknown. We simultaneously recorded multi-unit activity (MUA) and local field potentials in IT and AIP while monkeys discriminated between concave and convex 3D shapes and measured the degree to which the activity in IT and AIP synchronized during the task. We observed strong beta-band synchronization between IT and AIP preceding stimulus onset that decreased shortly after stimulus onset and became modulated by stereo-signal strength and stimulus contrast during the later portion of the stimulus period. The beta-coherence modulation was unrelated to task-difficulty, regionally specific, and dependent on the MUA selectivity of the pairs of sites under study. The beta-spike-field coherence in AIP predicted the upcoming choice of the monkey. Several convergent lines of evidence suggested AIP as the primary source of the AIP-IT synchronized activity. The synchronized beta activity seemed to occur during perceptual anticipation and when the system has stabilized to a particular perceptual state but not during active visual processing. Our findings demonstrate for the first time that synchronized activity exists between the end stages of the dorsal and ventral stream during 3D-shape discrimination.
Local Computation of Decision-Relevant Net Sensory Evidence in Parietal Cortex
A. Bollimunta and J. Ditterich
Cereb Cortex (2011)
To investigate the contribution of parietal cortex to perceptual decisions, we trained monkeys on a perceptual decision task that allowed simultaneous experimental control over how much sensory evidence was provided for each of 3 possible alternative choices and recorded single unit activity and local field potentials (LFPs) from the lateral intraparietal area (LIP). While both the behavior and the spiking activity were largely determined by the difference between how much supporting sensory evidence was provided for a particular choice (pro evidence) and how much sensory evidence was provided for the other alternatives (anti evidence), the LFP reflected roughly the sum of these 2 components. Furthermore, the firing rates showed an earlier influence of the anti evidence than the pro evidence. These observations indicate that LIP does not simply receive already precomputed decision signals but that it plays an active role in computing the decision-relevant net sensory evidence and that this local computation is reflected in the LFP. The results further demonstrate that the competition between the different alternatives cannot solely be mediated by lateral or feedback inhibition, as proposed by a major class of decision models but that feedforward inhibition makes an important contribution.
Dissociable effects of natural image structure and color on LFP and spiking activity in the lateral prefrontal cortex and extrastriate visual area V4
S. Liebe and N. K. Logothetis and G. Rainer
J Neurosci 31 10215-27 (2011)
Visual perception is mediated by unique contributions of the numerous brain regions that constitute the visual system. We performed simultaneous recordings of local field potentials (LFPs) and single unit activity (SUA) in areas V4 and lateral prefrontal cortex to characterize their contribution to visual processing. Here, we trained monkeys to identify natural images at different degradation levels in a visual recognition task. We parametrically varied color and structural information of natural images while the animals were performing the task. We show that the visual-evoked potential (VEP) of the LFP in V4 is highly sensitive to color, whereas the VEP in prefrontal cortex predominantly depends on image structure. When examining the relationship between VEP and SUA, we found that stimulus sensitivity for SUA was well predicted by the VEP in PF cortex but not in V4. Our results first reveal a functional specialization in both areas at the level of the LFP and further suggest that the degree to which mesoscopic signals, such as the VEP, are representative of the underlying SUA neural processing may be brain region specific within the context of visual recognition.
A modeling based study on the origin and nature of evoked post-synaptic local field potentials in granular layer
H. Parasuram and B. Nair and G. Naldi and E. D'Angelo and S. Diwakar
J Physiol Paris (2011)
Understanding population activities of underlying neurons reveal emergent behavior as patterns of information flow in neural circuits. Evoked local field potentials (LFPs) arise from complex interactions of spatial distribution of current sources, time dynamics, and spatial distribution of dipoles apart underlying conductive properties of the extracellular medium. We reconstructed LFP to test and parameterize the molecular mechanisms of cellular function with network properties. The sensitivity of LFP to local excitatory and inhibitory connections was tested using two novel techniques. In the first, we used a single granule neuron as a model kernel for reconstructing population activity. The second technique consisted using a detailed network model. LTP and LTD regulating the spatiotemporal pattern of granular layer responses to mossy fiber inputs was studied. The effect of changes in synaptic release probability and modulation in intrinsic excitability of granule cell on LFP was studied. The study revealed cellular function and plasticity were represented in LFP wave revealing the activity of underlying neurons. Changes to single cell properties during LTP and LTD were reflected in the LFP wave suggesting the sparse recoding function of granule neurons as spatial pattern generators. Both modeling approaches generated LFP in vitro (Mapelli and D'Angelo, 2007) and in vivo (Roggeri et al., 2008) waveforms as reported in experiments and predict that the expression mechanisms revealed in vitro can explain the LFP changes associated with LTP and LTD in vivo.
Infragranular sources of sustained local field potential responses in macaque primary visual cortex
A. Maier and C. J. Aura and D. A. Leopold
J Neurosci 31 1971-80 (2011)
A local field potential (LFP) response can be measured throughout the visual cortex in response to the abrupt appearance of a visual stimulus. Averaging LFP responses to many stimulus presentations isolates transient, phase-locked components of the response that are consistent from trial to trial. However, stimulus responses are also composed of sustained components, which differ in their phase from trial to trial and therefore must be evaluated using other methods, such as computing the power of the response of each trial before averaging. Here, we investigate the basis of phase-locked and non-phase-locked LFP responses in the primary visual cortex of the macaque monkey using a novel variant of current source density (CSD) analysis. We applied a linear array of electrode contacts spanning the thickness of the cortex to measure the LFP and compute band-limited CSD power to identify the laminar sites of persistent current exchange that may be the basis of sustained visual LFP responses. In agreement with previous studies, we found a short-latency phase-locked current sink, thought to correspond to thalamocortical input to layer 4C. In addition, we found a prominent non-phase-locked component of the CSD that persisted as long as the stimulus was physically present. The latter was relatively broadband, lasted throughout the stimulus presentation, and was centered ∼500 μm deeper than the initial current sink. These findings demonstrate a fundamental difference in the neural mechanisms underlying the initial and sustained processing of simple visual stimuli in the V1 microcircuit.
Perception-related modulations of local field potential power and coherence in primary visual cortex of awake monkey during binocular rivalry.
A. Gail and H. J. Brinksmeyer and R. Eckhorn
Cereb Cortex 14 300-13 (2004)
Cortical synchronization at gamma-frequencies (35-90 Hz) has been proposed to define the connectedness among the local parts of a perceived visual object. This hypothesis is still under debate. We tested it under conditions of binocular rivalry (BR), where a monkey perceived alternations among conflicting gratings presented singly to each eye at orthogonal orientations. We made multi-channel microelectrode recordings of multi-unit activity (MUA) and local field potentials (LFP) from striate cortex (V1) during BR while the monkey indicated his perception by pushing a lever. We analyzed spectral power and coherence of MUA and LFP over 4-90 Hz. As in previous work, coherence of gamma-signals in most pairs of recording locations strongly depended on grating orientation when stimuli were presented congruently in both eyes. With incongruent (rivalrous) stimulation LFP power was often consistently modulated in consonance with the perceptual state. This was not visible in MUA. These perception-related modulations of LFP occurred at low and medium frequencies (< 30 Hz), but not at gamma-frequencies. Perception-related modulations of LFP coherence were also restricted to the low-medium range. In conclusion, our results do not support the expectation that gamma-synchronization in V1 is related to the perceptual state during BR, but instead suggest a perception-related role of synchrony at low and medium frequencies.
Local field potential reflects perceptual suppression in monkey visual cortex
M. Wilke and N. K. Logothetis and D. A. Leopold
Proc Natl Acad Sci U S A 103 17507-12 (2006)
Neurophysiological and functional imaging experiments remain in apparent disagreement on the role played by the earliest stages of the visual cortex in supporting a visual percept. Here, we report electrophysiological findings that shed light on this issue. We monitored neural activity in the visual cortex of monkeys as they reported their perception of a high-contrast visual stimulus that was induced to vanish completely from perception on a subset of trials. We found that the spiking of neurons in cortical areas V1 and V2 was uncorrelated with the perceptual visibility of the target, whereas that in area V4 showed significant perception-related changes. In contrast, power changes in the lower frequency bands (particularly 9-30 Hz) of the local field potential (LFP), collected on the same trials, showed consistent and sustained perceptual modulation in all three areas. In addition, for the gamma frequency range (30-50 Hz), the responses during perceptual suppression of the target were correlated significantly with the responses to its physical removal in all areas, although the modulation magnitude was considerably higher in area V4 than in V1 and V2. These results, taken together, suggest that low-frequency LFP power in early cortical processing is more closely related to the representation of stimulus visibility than is spiking or higher frequency LFP activity.
Object selectivity of local field potentials and spikes in the macaque inferior temporal cortex.
G. Kreiman and C. P. Hung and A. Kraskov and R. Q. Quiroga and T. Poggio and J. J. DiCarlo
Neuron 49 433--445 (2006)
Local field potentials (LFPs) arise largely from dendritic activity over large brain regions and thus provide a measure of the input to and local processing within an area. We characterized LFPs and their relationship to spikes (multi and single unit) in monkey inferior temporal cortex (IT). LFP responses in IT to complex objects showed strong selectivity at 44% of the sites and tolerance to retinal position and size. The LFP preferences were poorly predicted by the spike preferences at the same site but were better explained by averaging spikes within approximately 3 mm. A comparison of separate sites suggests that selectivity is similar on a scale of approximately 800 microm for spikes and approximately 5 mm for LFPs. These observations imply that inputs to IT neurons convey selectivity for complex shapes and that such input may have an underlying organization spanning several millimeters.
Inferring spike trains from local field potentials.
M. J. Rasch and A. Gretton and Y. Murayama and W. Maass and N. K. Logothetis
J Neurophysiol 99 1461--1476 (2008)
We investigated whether it is possible to infer spike trains solely on the basis of the underlying local field potentials (LFPs). Using support vector machines and linear regression models, we found that in the primary visual cortex (V1) of monkeys, spikes can indeed be inferred from LFPs, at least with moderate success. Although there is a considerable degree of variation across electrodes, the low-frequency structure in spike trains (in the 100-ms range) can be inferred with reasonable accuracy, whereas exact spike positions are not reliably predicted. Two kinds of features of the LFP are exploited for prediction: the frequency power of bands in the high gamma-range (40-90 Hz) and information contained in low-frequency oscillations (<10 Hz), where both phase and power modulations are informative. Information analysis revealed that both features code (mainly) independent aspects of the spike-to-LFP relationship, with the low-frequency LFP phase coding for temporally clustered spiking activity. Although both features and prediction quality are similar during seminatural movie stimuli and spontaneous activity, prediction performance during spontaneous activity degrades much more slowly with increasing electrode distance. The general trend of data obtained with anesthetized animals is qualitatively mirrored in that of a more limited data set recorded in V1 of non-anesthetized monkeys. In contrast to the cortical field potentials, thalamic LFPs (e.g., LFPs derived from recordings in the dorsal lateral geniculate nucleus) hold no useful information for predicting spiking activity.
Low-frequency local field potentials and spikes in primary visual cortex convey independent visual information.
A. Belitski and A. Gretton and C. Magri and Y. Murayama and M. A. Montemurro and N. K. Logothetis and S. Panzeri
J Neurosci 28 5696--5709 (2008)
Local field potentials (LFPs) reflect subthreshold integrative processes that complement spike train measures. However, little is yet known about the differences between how LFPs and spikes encode rich naturalistic sensory stimuli. We addressed this question by recording LFPs and spikes from the primary visual cortex of anesthetized macaques while presenting a color movie. We then determined how the power of LFPs and spikes at different frequencies represents the visual features in the movie. We found that the most informative LFP frequency ranges were 1-8 and 60-100 Hz. LFPs in the range of 12-40 Hz carried little information about the stimulus, and may primarily reflect neuromodulatory inputs. Spike power was informative only at frequencies <12 Hz. We further quantified "signal correlations" (correlations in the trial-averaged power response to different stimuli) and "noise correlations" (trial-by-trial correlations in the fluctuations around the average) of LFPs and spikes recorded from the same electrode. We found positive signal correlation between high-gamma LFPs (60-100 Hz) and spikes, as well as strong positive signal correlation within high-gamma LFPs, suggesting that high-gamma LFPs and spikes are generated within the same network. LFPs <24 Hz shared strong positive noise correlations, indicating that they are influenced by a common source, such as a diffuse neuromodulatory input. LFPs <40 Hz showed very little signal and noise correlations with LFPs >40 Hz and with spikes, suggesting that low-frequency LFPs reflect neural processes that in natural conditions are fully decoupled from those giving rise to spikes and to high-gamma LFPs.
Divergence of fMRI and neural signals in V1 during perceptual suppression in the awake monkey
A. Maier and M. Wilke and C. Aura and C. Zhu and F. Q. Ye and D. A. Leopold
Nat Neurosci 11 1193-200 (2008)
The role of primary visual cortex (V1) in determining the contents of perception is controversial. Human functional magnetic resonance imaging (fMRI) studies of perceptual suppression have revealed a robust drop in V1 activity when a stimulus is subjectively invisible. In contrast, monkey single-unit recordings have failed to demonstrate such perception-locked changes in V1. To investigate the basis of this discrepancy, we measured both the blood oxygen level-dependent (BOLD) response and several electrophysiological signals in two behaving monkeys. We found that all signals were in good agreement during conventional stimulus presentation, showing strong visual modulation to presentation and removal of a stimulus. During perceptual suppression, however, only the BOLD response and the low-frequency local field potential (LFP) power showed decreases, whereas the spiking and high-frequency LFP power were unaffected. These results demonstrate that the coupling between the BOLD and electrophysiological signals in V1 is context dependent, with a marked dissociation occurring during perceptual suppression.