Theta phase mediates deliberate action switching in human Supplementary Motor Areas

The ability to deliberately overwrite ongoing automatic actions is a necessary feature of adaptive behavior. It has been proposed that the supplementary motor areas (SMAs) operate as a controller that orchestrates the switching between automatic and deliberate processes by inhibiting ongoing behaviors and so facilitating the execution of alternative ones. In addition, previous studies support the involvement of SMAs theta waves (4-9 Hz) in cognitive control. However, the exact role of such oscillatory dynamics and their contribution to the control of action are not fully understood. To investigate the mechanisms by which the SMAs support direct control of deliberate behavior, we recorded intracranial electroencephalography (iEEG) activity in humans performing a motor sequence task. Subjects had to perform a "change of plans" motor task requiring habitual movements to be overwritten at unpredictable moments. We found that SMAs were exclusively active during trials that demand action reprogramming in response to the unexpected cue but were silent during automatic action execution. Importantly, SMAs activity was characterized by a distinct temporal pattern, expressed in a stereotypical phase alignment of theta oscillations. More specifically, single trial motor performance was correlated with the trial contribution to the global inter-trial phase coherence, with higher coherence associated with faster trials. In addition, theta phase modulated the amplitude of gamma oscillations, with higher cross-frequency coupling in faster trials. Our results suggest that within frontal cortical networks, theta oscillations could encode a control signal that promotes the execution of deliberate actions.

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Thalamic theta phase alignment predicts human memory formation and anterior thalamic cross-frequency coupling

eLife ◽

10.7554/elife.07578 ◽

2015 ◽

Vol 4 ◽

Cited By ~ 17

Author(s):

Catherine M Sweeney-Reed ◽

Tino Zaehle ◽

Jürgen Voges ◽

Friedhelm C Schmitt ◽

Lars Buentjen ◽

...

Keyword(s):

Human Memory ◽

Gamma Oscillations ◽

Memory Formation ◽

Anterior Thalamic Nucleus ◽

Memory Processing ◽

Phase Alignment ◽

Theta Frequency ◽

Frequency Coupling ◽

Theta Phase ◽

Cross Frequency Coupling

Previously we reported electrophysiological evidence for a role for the anterior thalamic nucleus (ATN) in human memory formation (<xref ref-type="bibr" rid="bib29">Sweeney-Reed et al., 2014</xref>). Theta-gamma cross-frequency coupling (CFC) predicted successful memory formation, with the involvement of gamma oscillations suggesting memory-relevant local processing in the ATN. The importance of the theta frequency range in memory processing is well-established, and phase alignment of oscillations is considered to be necessary for synaptic plasticity. We hypothesized that theta phase alignment in the ATN would be necessary for memory encoding. Further analysis of the electrophysiological data reveal that phase alignment in the theta rhythm was greater during successful compared with unsuccessful encoding, and that this alignment was correlated with the CFC. These findings support an active processing role for the ATN during memory formation.

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Cholinergic modulation of cortical oscillatory dynamics

Journal of Neurophysiology ◽

10.1152/jn.1995.74.1.288 ◽

1995 ◽

Vol 74 (1) ◽

pp. 288-297 ◽

Cited By ~ 82

Author(s):

H. Liljenstrom ◽

M. E. Hasselmo

Keyword(s):

Synaptic Transmission ◽

Time Constant ◽

Field Potential ◽

Pyramidal Cells ◽

Gamma Oscillations ◽

Theta Oscillations ◽

Cortical Region ◽

Cholinergic Modulation ◽

Neuronal Adaptation ◽

Oscillatory Dynamics

1. The effect of cholinergic modulation on cortical oscillatory dynamics was studied in a computational model of the piriform (olfactory) cortex. The model included the cholinergic suppression of neuronal adaptation, the cholinergic suppression of intrinsic fiber synaptic transmission, the cholinergic enhancement of interneuron activity, and the cholinergic suppression of inhibitory synaptic transmission. 2. Electroencephalographic (EEG) recordings and field potential recordings from the piriform cortex were modeled with a simplified network in which cortical pyramidal cells were represented by excitatory input/output functions with gain parameters dependent on previous activity. The model incorporated distributed excitatory afferent input and excitatory connections between units. In addition, the model contained two sets of inhibitory units mediating inhibition with different time constants and different reversal potentials. This model can match effectively the patterns of cortical EEG and field potentials, showing oscillatory dynamics in both the gamma (30-80 Hz) and theta (3-10 Hz) frequency range. 3. Cholinergic suppression of neuronal adaptation was modeled by reducing the change in gain associated with previous activity. This caused an increased number of oscillations within the network in response to shock stimulation of the lateral olfactory tract, effectively replicating the effect of carbachol on the field potential response in physiological experiments. 4. Cholinergic suppression of intrinsic excitatory synaptic transmission decreased the prominence of gamma oscillations within the network, allowing theta oscillations to predominate. Coupled with the cholinergic suppression of neuronal adaptation, this caused the network to shift from a nonoscillatory state into an oscillatory state of predominant theta oscillations. This replicates the longer term effect of carbachol in experimental preparations on the EEG potential recorded from the cortex in vivo and from brain-slice preparations of the hippocampus in vitro. Analysis of the model suggests that these oscillations depend upon the time constant of neuronal adaptation rather than the time constant of inhibition or the activity of bursting neurons. 5. Cholinergic modulation may be involved in switching the dynamics of this cortical region between those appropriate for learning and those appropriate for recall. During recall, the spread of activity along intrinsic excitatory connections allows associative memory function, whereas neuronal adaptation prevents the spread of activity between different patterns. During learning, the recall of previously stored patterns is prevented by suppression of intrinsic excitatory connections, whereas the response to the new patterns is enhanced by suppression of neuronal adaptation.

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Learning to synchronize: Midfrontal theta dynamics during rule switching

10.1101/2020.06.01.127175 ◽

2020 ◽

Author(s):

Pieter Verbeke ◽

Kate Ergo ◽

Esther De Loof ◽

Tom Verguts

Keyword(s):

Negative Feedback ◽

Human Subjects ◽

Learning Task ◽

Theta Oscillations ◽

Prediction Errors ◽

Hierarchical Learning ◽

Theta Power ◽

Negative Prediction ◽

Theta Phase ◽

The Brain

AbstractIn recent years, several hierarchical extensions of well-known learning algorithms have been proposed. For example, when stimulus-action mappings vary across time or context, the brain may learn two or more stimulus-action mappings in separate modules, and additionally (at a hierarchically higher level) learn to appropriately switch between those modules. However, how the brain mechanistically coordinates neural communication to implement such hierarchical learning, remains unknown. Therefore, the current study tests a recent computational model that proposed how midfrontal theta oscillations implement such hierarchical learning via the principle of binding by synchrony (Sync model). More specifically, the Sync model employs bursts at theta frequency to flexibly bind appropriate task modules by synchrony. 64-channel EEG signal was recorded while 27 human subjects (Female: 21, Male: 6) performed a probabilistic reversal learning task. In line with the Sync model, post-feedback theta power showed a linear relationship with negative prediction errors, but not with positive prediction errors. This relationship was especially pronounced for subjects with better behavioral fit (measured via AIC) of the Sync model. Also consistent with Sync model simulations, theta phase-coupling between midfrontal electrodes and temporo-parietal electrodes was stronger after negative feedback. Our data suggest that the brain uses theta power and synchronization for flexibly switching between task rule modules, as is useful for example when multiple stimulus-action mappings must be retained and used.Significance StatementEveryday life requires flexibility in switching between several rules. A key question in understanding this ability is how the brain mechanistically coordinates such switches. The current study tests a recent computational framework (Sync model) that proposed how midfrontal theta oscillations coordinate activity in hierarchically lower task-related areas. In line with predictions of this Sync model, midfrontal theta power was stronger when rule switches were most likely (strong negative prediction error), especially in subjects who obtained a better model fit. Additionally, also theta phase connectivity between midfrontal and task-related areas was increased after negative feedback. Thus, the data provided support for the hypothesis that the brain uses theta power and synchronization for flexibly switching between rules.

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Hippocampal-prefrontal theta coupling develops as mice become proficient in associative odorant discrimination learning

10.1101/2021.09.28.462143 ◽

2021 ◽

Author(s):

Daniel Ramirez-Gordillo ◽

Andrew A. Parra ◽

K. Ulrich Bayer ◽

Diego Restrepo

Keyword(s):

Learning And Memory ◽

Discrimination Learning ◽

Gamma Oscillations ◽

Oscillatory Activity ◽

Dependent Protein Kinase ◽

Dependent Protein ◽

Theta Phase ◽

Phase Amplitude ◽

The Brain

Learning and memory requires coordinated activity between different regions of the brain. Here we studied the interaction between medial prefrontal cortex (mPFC) and hippocampal dorsal CA1 during associative odorant discrimination learning in the mouse. We found that as the animal learns to discriminate odorants in a go-no go task the coupling of high frequency neural oscillations to the phase of theta oscillations (phase-amplitude coupling or PAC) changes in a manner that results in divergence between rewarded and unrewarded odorant-elicited changes in the theta-phase referenced power (tPRP) for beta and gamma oscillations. In addition, in the proficient animal there was a decrease in the coordinated oscillatory activity between CA1 and mPFC in the presence of the unrewarded odorant. Furthermore, the changes in PAC resulted in a marked increase in the accuracy for decoding odorant identity from tPRP when the animal became proficient. Finally, we studied the role of Ca2+/calmodulin-dependent protein kinase II α (CaMKIIα), a protein involved in learning and memory, in oscillatory neural processing in this task. We find that the accuracy for decoding the odorant identity from tPRP decreases in CaMKIIα knockout mice and that this accuracy correlates with behavioral performance. These results implicate a role for PAC and CaMKIIα in olfactory go-no go associative learning in the hippocampal-prefrontal circuit.

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Optogenetically induced spatiotemporal gamma oscillations and neuronal spiking activity in primate motor cortex

Journal of Neurophysiology ◽

10.1152/jn.00792.2014 ◽

2015 ◽

Vol 113 (10) ◽

pp. 3574-3587 ◽

Cited By ~ 38

Author(s):

Yao Lu ◽

Wilson Truccolo ◽

Fabien B. Wagner ◽

Carlos E. Vargas-Irwin ◽

Ilker Ozden ◽

...

Keyword(s):

Motor Cortex ◽

Microelectrode Array ◽

Motor Task ◽

Optical Power ◽

Gamma Oscillations ◽

Constant Stimulus ◽

Spatiotemporal Patterns ◽

Gamma Activity ◽

Cortical Function ◽

Optogenetic Stimulation

Transient gamma-band (40–80 Hz) spatiotemporal patterns are hypothesized to play important roles in cortical function. Here we report the direct observation of gamma oscillations as spatiotemporal waves induced by targeted optogenetic stimulation, recorded by intracortical multichannel extracellular techniques in macaque monkeys during their awake resting states. Microelectrode arrays integrating an optical fiber at their center were chronically implanted in primary motor (M1) and ventral premotor (PMv) cortices of two subjects. Targeted brain tissue was transduced with the red-shifted opsin C1V1(T/T). Constant (1-s square pulses) and ramp stimulation induced narrowband gamma oscillations during awake resting states. Recordings across 95 microelectrodes (4 × 4-mm array) enabled us to track the transient gamma spatiotemporal patterns manifested, e.g., as concentric expanding and spiral waves. Gamma oscillations were induced well beyond the light stimulation volume, via network interactions at distal electrode sites, depending on optical power. Despite stimulation-related modulation in spiking rates, neuronal spiking remained highly asynchronous during induced gamma oscillations. In one subject we examined stimulation effects during preparation and execution of a motor task and observed that movement execution largely attenuated optically induced gamma oscillations. Our findings demonstrate that, beyond previously reported induced gamma activity under periodic drive, a prolonged constant stimulus above a certain threshold may carry primate motor cortex network dynamics into gamma oscillations, likely via a Hopf bifurcation. More broadly, the experimental capability in combining microelectrode array recordings and optogenetic stimulation provides an important approach for probing spatiotemporal dynamics in primate cortical networks during various physiological and behavioral conditions.

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Alternating sequences of future and past behavior encoded within hippocampal theta oscillations

Science ◽

10.1126/science.abb4151 ◽

2020 ◽

Vol 370 (6513) ◽

pp. 247-250 ◽

Cited By ~ 3

Author(s):

Mengni Wang ◽

David J. Foster ◽

Brad E. Pfeiffer

Keyword(s):

Activity Patterns ◽

Place Cells ◽

Theta Oscillations ◽

Retrospective Evaluation ◽

Past Behavior ◽

Hippocampal Ca1 ◽

Ongoing Behavior ◽

Theta Phase ◽

Hippocampal Theta ◽

And Storage

Neural networks display the ability to transform forward-ordered activity patterns into reverse-ordered, retrospective sequences. The mechanisms underlying this transformation remain unknown. We discovered that, during active navigation, rat hippocampal CA1 place cell ensembles are inherently organized to produce independent forward- and reverse-ordered sequences within individual theta oscillations. This finding may provide a circuit-level basis for retrospective evaluation and storage during ongoing behavior. Theta phase procession arose in a minority of place cells, many of which displayed two preferred firing phases in theta oscillations and preferentially participated in reverse replay during subsequent rest. These findings reveal an unexpected aspect of theta-based hippocampal encoding and provide a biological mechanism to support the expression of reverse-ordered sequences.

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Midline Frontal ERPS and Theta Phase Alignment

Psychophysiology ◽

10.1111/psyp.12490 ◽

2015 ◽

Vol 52 ◽

pp. S18-S18

Keyword(s):

Phase Alignment ◽

Theta Phase

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Altered GABAA,slow Inhibition and Network Oscillations in Mice Lacking the GABAA Receptor β3 Subunit

Journal of Neurophysiology ◽

10.1152/jn.00651.2009 ◽

2009 ◽

Vol 102 (6) ◽

pp. 3643-3655 ◽

Cited By ~ 23

Author(s):

Harald Hentschke ◽

Claudia Benkwitz ◽

Matthew I. Banks ◽

Mark G. Perkins ◽

Gregg E. Homanics ◽

...

Keyword(s):

Pyramidal Neurons ◽

Epileptiform Activity ◽

Gamma Oscillations ◽

Theta Oscillations ◽

Network Activity ◽

Inhibitory Synapses ◽

Gabaergic Inhibition ◽

Wild Type ◽

Hippocampal Network

Phasic GABAergic inhibition in hippocampus and neocortex falls into two kinetically distinct categories, GABAA,fast and GABAA,slow. In hippocampal area CA1, GABAA,fast is generally believed to underlie gamma oscillations, whereas the contribution of GABAA,slow to hippocampal rhythms has been speculative. Hypothesizing that GABAA receptors containing the β3 subunit contribute to GABAA,slow inhibition and that slow inhibitory synapses control excitability as well as contribute to network rhythms, we investigated the consequences of this subunit's absence on synaptic inhibition and network function. In pyramidal neurons of GABAA receptor β3 subunit-deficient (β3−/−) mice, spontaneous GABAA,slow inhibitory postsynaptic currents (IPSCs) were much less frequent, and evoked GABAA,slow currents were much smaller than in wild-type mice. Fittingly, long-lasting recurrent inhibition of population spikes was less powerful in the mutant, indicating that receptors containing β3 subunits contribute substantially to GABAA,slow currents in pyramidal neurons. By contrast, slow inhibitory control of GABAA,fast-producing interneurons was unaffected in β3−/− mice. In vivo hippocampal network activity was markedly different in the two genotypes. In β3−/− mice, epileptiform activity was observed, and theta oscillations were weaker, slower, less regular and less well coordinated across laminae compared with wild-type mice, whereas gamma oscillations were weaker and faster. The amplitude modulation of gamma oscillations at theta frequency (“nesting”) was preserved but was less well coordinated with theta oscillations. With the caveat that seizure-induced changes in inhibitory circuits might have contributed to the changes observed in the mutant animals, our results point to a strong contribution of β3 subunits to slow GABAergic inhibition onto pyramidal neurons but not onto GABAA,fast -producing interneurons and support different roles for these slow inhibitory synapses in the generation and coordination of hippocampal network rhythms.

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Studio funzionale RM delle aree motorie corticali nel morbo di Parkinson

Rivista di Neuroradiologia ◽

10.1177/19714009970100s206 ◽

1997 ◽

Vol 10 (2_suppl) ◽

pp. 21-24 ◽

Cited By ~ 1

Author(s):

G.P. Pelliccioli ◽

O. Presciutti ◽

N. Tambasco ◽

P. Floridi ◽

R. Tarducci ◽

...

Keyword(s):

Primary Motor Cortex ◽

Motor Task ◽

Activation Pattern ◽

Fixed Sequence ◽

Dopaminergic Drugs ◽

Cortical Motor ◽

Major Increase ◽

And Performance ◽

Mri Study ◽

Motor Areas

Impaired motor programming and performance in Parkinson's Disease (PD) is related to a functional deafferentation from the basal ganglia to the cortical motor areas, which can be partially reversed by dopaminergic drugs. The aim of this functional MRI study was to compare the activation pattern of motor areas in early PD patients on therapy versus age-matched controls and to show how the dopaminergic drug apomorphine modifies this activation pattern. The self-paced motor task was a complex fixed sequence of finger movements in opposition to the thumb. Comparison between whole activation of cortical motor areas in patients and controls revealed no significant differences. In patients a significant reduction of the activation was found in the primary motor cortex contralateral to the more affected hand; on the contrary a major increase in activation in the same motor area was observed after apomorphine. This could be evidence of the reversal of the partial deafferentation due to the direct dopaminergic action of apomorphine which is complementary to levodopa.

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