scholarly journals Synchronous spiking associated with high gamma oscillations in prefrontal cortex exerts top-down control over a 5Hz-rhythmic modulation of spiking in locus coeruleus

Author(s):  
Nelson K. Totah ◽  
Nikos K. Logothetis ◽  
Oxana Eschenko

AbstractThe brainstem noradrenergic locus coeruleus (LC) is reciprocally connected with the prefrontal cortex (PFC). Strong coupling between LC spiking and depolarizing phase of slow (1 – 2 Hz) waves in the PFC field potentials during sleep and anesthesia suggests that the LC drives cortical state transition. Reciprocal LC-PFC connectivity should also allow interactions in the opposing (top-down) direction, but prior work has only studied prefrontal control over LC activity using direct electrical (or optogenetic) stimulation paradigms. Here, we describe the physiological characteristics of naturally occurring top-down prefrontal-coerulear interactions. Specifically, we recorded LC multi-unit activity (MUA) simultaneously with PFC single unit and local field potential (LFP) activity in urethane-anesthetized rats. We observed cross-regional coupling between the phase of ~5 Hz oscillations in LC population spike rate and the power of PFC LFP oscillations within the high Gamma (hGamma) range (60 – 200 Hz). Specifically, transient increases in PFC hGamma power preceded peaks in the ~5 Hz LC-MUA oscillation. Analysis of cross-regional transfer entropy demonstrated that the PFC hGamma transients were predictive of a transient increase in LC-MUA. A ~29 msec delay between these signals was consistent with the conduction velocity from the PFC to the LC. Finally, we showed that PFC hGamma transients are associated with synchronized spiking of a subset (27%) of PFC single units. Our data suggest that, PFC hGamma transients may indicate the timing of the top-down excitatory input to LC, at least under conditions when LC neuronal population activity fluctuates rhythmically at ~5 Hz. Synchronized PFC neuronal spiking that occurs during hGamma transients may provide a previously unknown mode of top-down control over the LC.

2018 ◽  
Vol 119 (3) ◽  
pp. 904-920 ◽  
Author(s):  
Ricardo M. Neves ◽  
Silvia van Keulen ◽  
Mingyu Yang ◽  
Nikos K. Logothetis ◽  
Oxana Eschenko

The locus coeruleus (LC) noradrenergic (NE) neuromodulatory system is critically involved in regulation of neural excitability via its diffuse ascending projections. Tonic NE release in the forebrain is essential for maintenance of vigilant states and increases the signal-to-noise ratio of cortical sensory responses. The impact of phasic NE release on cortical activity and sensory processing is less explored. We previously reported that LC microstimulation caused a transient desynchronization of population activity in the medial prefrontal cortex (mPFC), similar to noxious somatosensory stimuli. The LC receives nociceptive information from the medulla and therefore may mediate sensory signaling to its forebrain targets. Here we performed extracellular recordings in LC and mPFC while presenting noxious stimuli in urethane-anesthetized rats. A brief train of foot shocks produced a robust phasic response in the LC and a transient change in the mPFC power spectrum, with the strongest modulation in the gamma (30–90 Hz) range. The LC phasic response preceded prefrontal gamma power increase, and cortical modulation was proportional to the LC excitation. We also quantitatively characterized distinct cortical states and showed that sensory responses in both LC and mPFC depend on the ongoing cortical state. Finally, cessation of the LC firing by bilateral local iontophoretic injection of clonidine, an α2-adrenoreceptor agonist, completely eliminated sensory responses in the mPFC without shifting cortex to a less excitable state. Together, our results suggest that the LC phasic response induces gamma power increase in the PFC and is essential for mediating sensory information along an ascending noxious pathway. NEW & NOTEWORTHY Our study shows linear relationships between locus coeruleus phasic excitation and the amplitude of gamma oscillations in the prefrontal cortex. Results suggest that the locus coeruleus phasic response is essential for mediating sensory information along an ascending noxious pathway.


2012 ◽  
Vol 24 (2) ◽  
pp. 304-314 ◽  
Author(s):  
Rafael Polanía ◽  
Walter Paulus ◽  
Michael A. Nitsche

The temporal maintenance and subsequent retrieval of information that no longer exists in the environment is called working memory. It is believed that this type of memory is controlled by the persistent activity of neuronal populations, including the prefrontal, temporal, and parietal cortex. For a long time, it has been controversially discussed whether, in working memory, the PFC stores past sensory events or, instead, its activation is an extramnemonic source of top–down control over posterior regions. Recent animal studies suggest that specific information about the contents of working memory can be decoded from population activity in prefrontal areas. However, it has not been shown whether the contents of working memory during the delay periods can be decoded from EEG recordings in the human brain. We show that by analyzing the nonlinear dynamics of EEG oscillatory patterns it is possible to noninvasively decode with high accuracy, during encoding and maintenance periods, the contents of visual working memory information within high-gamma oscillations in the human PFC. These results are thus in favor of an active storage function of the human PFC in working memory; this, without ruling out the role of PFC in top–down processes. The ability to noninvasively decode the contents of working memory is promising in applications such as brain computer interfaces, together with computation of value function during planning and decision making processes.


2021 ◽  
Vol 11 (1) ◽  
Author(s):  
Bin Wang ◽  
Chuanliang Han ◽  
Tian Wang ◽  
Weifeng Dai ◽  
Yang Li ◽  
...  

AbstractStimulus-dependence of gamma oscillations (GAMMA, 30–90 Hz) has not been fully understood, but it is important for revealing neural mechanisms and functions of GAMMA. Here, we recorded spiking activity (MUA) and the local field potential (LFP), driven by a variety of plaids (generated by two superimposed gratings orthogonal to each other and with different contrast combinations), in the primary visual cortex of anesthetized cats. We found two distinct narrow-band GAMMAs in the LFPs and a variety of response patterns to plaids. Similar to MUA, most response patterns showed that the second grating suppressed GAMMAs driven by the first one. However, there is only a weak site-by-site correlation between cross-orientation interactions in GAMMAs and those in MUAs. We developed a normalization model that could unify the response patterns of both GAMMAs and MUAs. Interestingly, compared with MUAs, the GAMMAs demonstrated a wider range of model parameters and more diverse response patterns to plaids. Further analysis revealed that normalization parameters for high GAMMA, but not those for low GAMMA, were significantly correlated with the discrepancy of spatial frequency between stimulus and sites’ preferences. Consistent with these findings, normalization parameters and diversity of high GAMMA exhibited a clear transition trend and region difference between area 17 to 18. Our results show that GAMMAs are also regulated in the form of normalization, but that the neural mechanisms for these normalizations might differ from those of spiking activity. Normalizations in different brain signals could be due to interactions of excitation and inhibitions at multiple stages in the visual system.


2019 ◽  
Author(s):  
Agrita Dubey ◽  
Supratim Ray

AbstractElectrocorticogram (ECoG), obtained from macroelectrodes placed on the cortex, is typically used in drug-resistant epilepsy patients, and is increasingly being used to study cognition in humans. These studies often use power in gamma (30-70 Hz) or high-gamma (>80 Hz) ranges to make inferences about neural processing. However, while the stimulus tuning properties of gamma/high-gamma power have been well characterized in local field potential (LFP; obtained from microelectrodes), analogous characterization has not been done for ECoG. Using a hybrid array containing both micro and ECoG electrodes implanted in the primary visual cortex of two female macaques, we compared the stimulus tuning preferences of gamma/high-gamma power in LFP versus ECoG and found them to be surprisingly similar. High-gamma power, thought to index the average firing rate around the electrode, was highest for the smallest stimulus (0.3° radius), and decreased with increasing size in both LFP and ECoG, suggesting local origins of both signals. Further, gamma oscillations were similarly tuned in LFP and ECoG to stimulus orientation, contrast and spatial frequency. This tuning was significantly weaker in electroencephalogram (EEG), suggesting that ECoG is more like LFP than EEG. Overall, our results validate the use of ECoG in clinical and basic cognitive research.


2011 ◽  
Vol 106 (6) ◽  
pp. 2910-2921 ◽  
Author(s):  
Marcel Ruiz-Mejias ◽  
Laura Ciria-Suarez ◽  
Maurizio Mattia ◽  
Maria V. Sanchez-Vives

A characterization of the oscillatory activity in the cerebral cortex of the mouse was realized under ketamine anesthesia. Bilateral recordings were obtained from deep layers of primary visual, somatosensory, motor, and medial prefrontal cortex. A slow oscillatory activity consisting of up and down states was detected, the average frequency being 0.97 Hz in all areas. Different parameters of the oscillation were estimated across cortical areas, including duration of up and down states and their variability, speed of state transitions, and population firing rate. Similar values were obtained for all areas except for prefrontal cortex, which showed significant faster down-to-up state transitions, higher firing rate during up states, and more regular cycles. The wave propagation patterns in the anteroposterior axis in motor cortex and the mediolateral axis in visual cortex were studied with multielectrode recordings, yielding speed values between 8 and 93 mm/s. The firing of single units was analyzed with respect to the population activity. The most common pattern was that of neurons firing in >90% of the up states with 1–6 spikes. Finally, fast rhythms (beta, low gamma, and high gamma) were analyzed, all of them showing significantly larger power during up states than in down states. Prefrontal cortex exhibited significantly larger power in both beta and gamma bands (up to 1 order of magnitude larger in the case of high gamma) than the rest of the cortical areas. This study allows us to carry out interareal comparisons and provides a baseline to compare against cortical emerging activity from genetically altered animals.


2016 ◽  
Vol 113 (19) ◽  
pp. E2721-E2729 ◽  
Author(s):  
Matthew Ainsworth ◽  
Shane Lee ◽  
Marcus Kaiser ◽  
Jennifer Simonotto ◽  
Nancy J. Kopell ◽  
...  

Repeated presentations of sensory stimuli generate transient gamma-frequency (30–80 Hz) responses in neocortex that show plasticity in a task-dependent manner. Complex relationships between individual neuronal outputs and the mean, local field potential (population activity) accompany these changes, but little is known about the underlying mechanisms responsible. Here we show that transient stimulation of input layer 4 sufficient to generate gamma oscillations induced two different, lamina-specific plastic processes that correlated with lamina-specific changes in responses to further, repeated stimulation: Unit rates and recruitment showed overall enhancement in supragranular layers and suppression in infragranular layers associated with excitatory or inhibitory synaptic potentiation onto principal cells, respectively. Both synaptic processes were critically dependent on activation of GABAB receptors and, together, appeared to temporally segregate the cortical representation. These data suggest that adaptation to repetitive sensory input dramatically alters the spatiotemporal properties of the neocortical response in a manner that may both refine and minimize cortical output simultaneously.


2016 ◽  
Vol 116 (1) ◽  
pp. 5-17 ◽  
Author(s):  
Julien Catanese ◽  
J. Eric Carmichael ◽  
Matthijs A. A. van der Meer

The loop structure of cortico-striatal anatomy in principle enables both descending (cortico-striatal) and ascending (striato-cortical) influences, but the factors that regulate the flow of information in these loops are not known. We report that low- and high-gamma oscillations (∼50 and ∼80 Hz, respectively) in the local field potential of freely moving rats are highly synchronous between the infralimbic region of the medial prefrontal cortex (mPFC) and the ventral striatum (vStr). Strikingly, high-gamma oscillations in mPFC preceded those in vStr, whereas low-gamma oscillations in mPFC lagged those in vStr, with short (∼1 ms) time lags. These systematic deviations from zero-phase synchrony were consistent across measures based on amplitude cross-correlation and phase slopes and were robustly maintained between behavioral states and different individual subjects. Furthermore, low- and high-gamma oscillations were associated with distinct ensemble spiking patterns in vStr, even when controlling for overt behavioral differences and slow changes in neural activity. These results imply that neural activity in vStr and mPFC is tightly coupled at the gamma timescale and raise the intriguing possibility that frequency-specific deviations from this coupling may signal transient leader-follower switches.


2010 ◽  
Vol 2010 ◽  
pp. 1-12 ◽  
Author(s):  
Stephen V. David ◽  
Nicolas Malaval ◽  
Shihab A. Shamma

Neurophysiologists have recently become interested in studying neuronal population activity through local field potential (LFP) recordings during experiments that also record the activity of single neurons. This experimental approach differs from early LFP studies because it uses high impendence electrodes that can also isolate single neuron activity. A possible complication for such studies is that the synaptic potentials and action potentials of the small subset of isolated neurons may contribute disproportionately to the LFP signal, biasing activity in the larger nearby neuronal population to appear synchronous and cotuned with these neurons. To address this problem, we used linear filtering techniques to remove features correlated with spike events from LFP recordings. This filtering procedure can be applied for well-isolated single units or multiunit activity. We illustrate the effects of this correction in simulation and on spike data recorded from primary auditory cortex. We find that local spiking activity can explain a significant portion of LFP power at most recording sites and demonstrate that removing the spike-correlated component can affect measurements of auditory tuning of the LFP.


2014 ◽  
Vol 112 (11) ◽  
pp. 3001-3011 ◽  
Author(s):  
Piotr Suffczynski ◽  
Nathan E. Crone ◽  
Piotr J. Franaszczuk

High-gamma activity, ranging in frequency between ∼60 Hz and 200 Hz, has been observed in local field potential, electrocorticography, EEG and magnetoencephalography signals during cortical activation, in a variety of functional brain systems. The origin of these signals is yet unknown. Using computational modeling, we show that a cortical network model receiving thalamic input generates high-gamma responses comparable to those observed in local field potential recorded in monkey somatosensory cortex during vibrotactile stimulation. These high-gamma oscillations appear to be mediated mostly by an excited population of inhibitory fast-spiking interneurons firing at high-gamma frequencies and pacing excitatory regular-spiking pyramidal cells, which fire at lower rates but in phase with the population rhythm. The physiological correlates of high-gamma activity, in this model of local cortical circuits, appear to be similar to those proposed for hippocampal ripples generated by subsets of interneurons that regulate the discharge of principal cells.


2020 ◽  
Author(s):  
Shahryar Noei ◽  
Ioannis S. Zouridis ◽  
Nikos K. Logothetis ◽  
Stefano Panzeri ◽  
Nelson K. Totah

AbstractThe noradrenergic locus coeruleus (LC) is crucial for controlling brain and behavioral states. While synchronous stimulation of LC neurons evokes a single activated cortical state with increased high-frequency power, little is known about how spontaneous patterns of LC population activity drive cortical states. Since LC neurons selectively project to specific forebrain regions, we hypothesized that individual LC ensembles produce different cortical states. We recorded up to 34 single units simultaneously in the rat LC and used non-negative matrix factorization to identify spontaneously activated ensembles of co-active LC neurons. The ensembles were active mostly at different times and were simultaneously active only rarely. We assessed cortical state in area 24a by examining local field potential power spectrograms triggered on activations of individual LC ensembles. We observed four spectrotemporally-distinct cortical states associated with activation of specific LC ensembles. Thus, distinct spontaneously active LC ensembles contribute to unexpectedly diverse cortical states.


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