Frequency Band-Specific Electrical Brain Stimulation Modulates Cognitive Control Processes

A large body of findings has tied midfrontal theta-band (4–8 Hz) oscillatory activity to adaptive control mechanisms during response conflict. Thus far, this evidence has been correlational. To evaluate whether theta oscillations are causally involved in conflict processing, we applied transcranial alternating current stimulation (tACS) in the theta band to a midfrontal scalp region, while human subjects performed a spatial response conflict task. Conflict was introduced by incongruency between the location of the target stimulus and the required response hand. As a control condition, we used alpha-band (8–12 Hz) tACS over the same location. The exact stimulation frequencies were determined empirically for each subject based on a pre-stimulation EEG session. Behavioral results showed general conflict effects of slower response times (RT) and lower accuracy for high conflict trials compared to low conflict trials. Importantly, this conflict effect was reduced specifically during theta tACS, which was driven by slower response times on low conflict trials. These results show how theta tACS can modulate adaptive cognitive control processes, which is in accordance with the view of midfrontal theta oscillations as an active mechanism for cognitive control.     

Changes in spectral coherent characteristics of EEG in the early postpartum period in mothers with anxious and depressed mood

Postpartum EEG spectral and coherence characteristics were estimated in mothers with or without postpartum depressions. In mothers without affective disorders the power of oscillations in the delta, theta, and alpha 1 frequency bands was increased as compared to controls. Intrahemispheric EEG coherence between the left frontal and adjacent derivations in the delta and theta bands and interhemispheric coherence in the central areas was increased and decreased over the remaining cortical surface. These changes led to a significant decrease in EEG asymmetry. It is suggested that during normal postpartum the influence of the limbicodiencephalic and lower brainstem structures on the cortex is augmented and a certain kind of dominanta is formed. In mothers with postpartum depressions the EEG alpha-band power was lower than in the control and normal groups, coherence changes in the delta and theta bands diminished the EEG asymmetry. The insufficiency of limbicodiencephalic influence and impairment of adaptive brainstem reactions are suggested to be responsible for problems in the formation of maternal dominanta, which results in the development of postpartum depressions.     

Phase locking of single neuron activity to theta oscillations during working memory in monkey extrastriate visual cortex

Working memory has been linked to elevated single neuron discharge in monkeys and to oscillatory changes in the human EEG, but the relation between these effects has remained largely unexplored. We addressed this question by measuring local field potentials and single unit activity simultaneously from multiple electrodes placed in extrastriate visual cortex while monkeys were performing a working memory task. We describe a significant enhancement in theta band energy during the delay period. Theta oscillations had a systematic effect on single neuron activity, with neurons emitting more action potentials near their preferred angle of each theta cycle. Sample-selective delay activity was enhanced if only action potentials emitted near the preferred theta angle were considered. Our results suggest that extrastriate visual cortex is involved in short-term maintenance of information and that theta oscillations provide a mechanism for structuring the recurrent interaction between neurons in different brain regions that underlie working memory.     

Top-Down Control in Contour Grouping

Human observers tend to group oriented line segments into full contours if they follow the Gestalt rule of ''good continuation''. It is commonly assumed that contour grouping emerges automatically in early visual cortex. In contrast, recent work in animal models suggests that contour grouping requires learning and thus involves top-down control from higher brain structures. Here we explore mechanisms of top-down control in perceptual grouping by investigating synchronicity within EEG oscillations. Human participants saw two micro-Gabor arrays in a random order, with the task to indicate whether the first (S1) or the second stimulus (S2) contained a contour of collinearly aligned elements. Contour compared to non-contour S1 produced a larger posterior post-stimulus beta power (15–21 Hz). Contour S2 was associated with a pre-stimulus decrease in posterior alpha power (11–12 Hz) and in fronto-posterior theta (4–5 Hz) phase couplings, but not with a post-stimulus increase in beta power. The results indicate that subjects used prior knowledge from S1 processing for S2 contour grouping. Expanding previous work on theta oscillations, we propose that long-range theta synchrony shapes neural responses to perceptual groupings regulating lateral inhibition in early visual cortex.     

Synchronized oscillations at alpha and theta frequencies in the lateral geniculate nucleus

In relaxed wakefulness, the EEG exhibits robust rhythms in the alpha band (8-13 Hz), which decelerate to theta (approximately 2-7 Hz) frequencies during early sleep. In animal models, these rhythms occur coherently with synchronized activity in the thalamus. However, the mechanisms of this thalamic activity are unknown. Here we show that, in slices of the lateral geniculate nucleus maintained in vitro, activation of the metabotropic glutamate receptor (mGluR) mGluR1a induces synchronized oscillations at alpha and theta frequencies that share similarities with thalamic alpha and theta rhythms recorded in vivo. These in vitro oscillations are driven by an unusual form of burst firing that is present in a subset of thalamocortical neurons and are synchronized by gap junctions. We propose that mGluR1a-induced oscillations are a potential mechanism whereby the thalamus promotes EEG alpha and theta rhythms in the intact brain.     

Induced cortical electrical activity during different time-spans between warning and target stimuli

A certain alpha-band EEG dynamics was revealed in healthy adults (n = 16) at the interval between a warning and a target stimulus in a simple visuospatial task (subjects were instructed to locate a specific letter in the table of letters). Two series of experiment--either with a 2-sec or a 9-sec inter-stimulus interval were conducted, each consisting of 60 trials. In both series, we observed an induced desynchronization of low alpha (8-10 Hz) at the first second after the warning stimulus and its desynchronization just before the target stimulus. In series with a 9-sec inter-stimulus interval at the 4-6 s of it we observed an alpha-band synchronization, especially distinct in high alpha (10.5-13 Hz). This synchronization gradually reduced towards the end of the inter-stimulus interval. We consider the above changes in alpha-band spectral power during the inter-stimulus interval to be induced by "inner impulsations" caused by an internal representation (set) of the stimuli time-sequence. Changes in the level of cognitive control during the inter-stimulus interval cause increases and decreases in fronto-thalamic system activity, which are manifested in changes of alpha-band spectral power. Analysis of theta-band dynamics suggests that cortico-hippocampal system doesn't participate in this process.     

Human cortical traveling waves: dynamical properties and correlations with responses

The spatiotemporal behavior of human EEG oscillations is investigated. Traveling waves in the alpha and theta ranges are found to be common in both prestimulus and poststimulus EEG activity. The dynamical properties of these waves, including their speeds, directions, and durations, are systematically characterized for the first time, and the results show that there are significant changes of prestimulus spontaneous waves in the presence of an external stimulus. Furthermore, the functional relevance of these waves is examined by studying how they are correlated with reaction times on a single trial basis; prestimulus alpha waves traveling in the frontal-to-occipital direction are found to be most correlated to reaction speeds. These findings suggest that propagating waves of brain oscillations might be involved in mediating long-range interactions between widely distributed parts of human cortex.     

Hippocampal State-Dependent Behavioral Reflex to an Identical Sensory Input in Rats

We examined the local field potential of the hippocampus to monitor brain states during a conditional discrimination task, in order to elucidate the relationship between ongoing brain states and a conditioned motor reflex. Five 10-week-old Wistar/ST male rats underwent a serial feature positive conditional discrimination task in eyeblink conditioning using a preceding light stimulus as a conditional cue for reinforced trials. In this task, a 2-s light stimulus signaled that the following 350-ms tone (conditioned stimulus) was reinforced with a co-terminating 100-ms periorbital electrical shock. The interval between the end of conditional cue and the onset of the conditioned stimulus was 4±1 s. The conditioned stimulus was not reinforced when the light was not presented. Animals successfully utilized the light stimulus as a conditional cue to drive differential responses to the identical conditioned stimulus. We found that presentation of the conditional cue elicited hippocampal theta oscillations, which persisted during the interval of conditional cue and the conditioned stimulus. Moreover, expression of the conditioned response to the tone (conditioned stimulus) was correlated with the appearance of theta oscillations immediately before the conditioned stimulus. These data support hippocampal involvement in the network underlying a conditional discrimination task in eyeblink conditioning. They also suggest that the preceding hippocampal activity can determine information processing of the tone stimulus in the cerebellum and its associated circuits.     

Selective coupling between theta phase and neocortical fast gamma oscillations during REM-sleep in mice

Background

The mammalian brain expresses a wide range of state-dependent network oscillations which vary in frequency and spatial extension. Such rhythms can entrain multiple neurons into coherent patterns of activity, consistent with a role in behaviour, cognition and memory formation. Recent evidence suggests that locally generated fast network oscillations can be systematically aligned to long-range slow oscillations. It is likely that such cross-frequency coupling supports specific tasks including behavioural choice and working memory.

Principal Findings

We analyzed temporal coupling between high-frequency oscillations and EEG theta activity (4–12 Hz) in recordings from mouse parietal neocortex. Theta was exclusively present during active wakefulness and REM-sleep. Fast oscillations occurred in two separate frequency bands: gamma (40–100 Hz) and fast gamma (120–160 Hz). Theta, gamma and fast gamma were more prominent during active wakefulness as compared to REM-sleep. Coupling between theta and the two types of fast oscillations, however, was more pronounced during REM-sleep. This state-dependent cross-frequency coupling was particularly strong for theta-fast gamma interaction which increased 9-fold during REM as compared to active wakefulness. Theta-gamma coupling increased only by 1.5-fold.

Significance

State-dependent cross-frequency-coupling provides a new functional characteristic of REM-sleep and establishes a unique property of neocortical fast gamma oscillations. Interactions between defined patterns of slow and fast network oscillations may serve selective functions in sleep-dependent information processing.     

Long lasting modulation of cortical oscillations after continuous theta burst transcranial magnetic stimulation

Transcranial magnetic theta burst stimulation (TBS) differs from other high-frequency rTMS protocols because it induces plastic changes up to an hour despite lower stimulus intensity and shorter duration of stimulation. However, the effects of TBS on neuronal oscillations remain unclear. In this study, we used electroencephalography (EEG) to investigate changes of neuronal oscillations after continuous TBS (cTBS), the protocol that emulates long-term depression (LTD) form of synaptic plasticity. We randomly divided 26 healthy humans into two groups receiving either Active or Sham cTBS as control over the left primary motor cortex (M1). Post-cTBS aftereffects were assessed with behavioural measurements at rest using motor evoked potentials (MEPs) and at active state during the execution of a choice reaction time (RT) task in combination with continuous electrophysiological recordings. The cTBS-induced EEG oscillations were assessed using event-related power (ERPow), which reflected regional oscillatory activity of neural assemblies of θ (4-7.5 Hz), low α (8-9.5 Hz), μ (10-12.5 Hz), low β (13-19.5 Hz), and high β (20-30 Hz) brain rhythms. Results revealed 20-min suppression of MEPs and at least 30-min increase of ERPow modulation, suggesting that besides MEPs, EEG has the potential to provide an accurate cortical readout to assess cortical excitability and to investigate the interference of cortical oscillations in the human brain post-cTBS. We also observed a predominant modulation of β frequency band, supporting the hypothesis that cTBS acts more on cortical level. Theta oscillations were also modulated during rest implying the involvement of independent cortical theta generators over the motor network post cTBS. This work provided more insights into the underlying mechanisms of cTBS, providing a possible link between synchronised neural oscillations and LTD in humans.     

Directional Theta Coherence in Prefrontal Cortical to Amygdalo-Hippocampal Pathways Signals Fear Extinction

Theta oscillations are considered crucial mechanisms in neuronal communication across brain areas, required for consolidation and retrieval of fear memories. One form of inhibitory learning allowing adaptive control of fear memory is extinction, a deficit of which leads to maladaptive fear expression potentially leading to anxiety disorders. Behavioral responses after extinction training are thought to reflect a balance of recall from extinction memory and initial fear memory traces. Therefore, we hypothesized that the initial fear memory circuits impact behavioral fear after extinction, and more specifically, that the dynamics of theta synchrony in these pathways signal the individual fear response. Simultaneous multi-channel local field and unit recordings were obtained from the infralimbic prefrontal cortex, the hippocampal CA1 and the lateral amygdala in mice. Data revealed that the pattern of theta coherence and directionality within and across regions correlated with individual behavioral responses. Upon conditioned freezing, units were phase-locked to synchronized theta oscillations in these pathways, characterizing states of fear memory retrieval. When the conditioned stimulus evoked no fear during extinction recall, theta interactions were directional with prefrontal cortical spike firing leading hippocampal and amygdalar theta oscillations. These results indicate that the directional dynamics of theta-entrained activity across these areas guide changes in appraisal of threatening stimuli during fear memory and extinction retrieval. Given that exposure therapy involves procedures and pathways similar to those during extinction of conditioned fear, one therapeutical extension might be useful that imposes artificial theta activity to prefrontal cortical-amygdalo-hippocampal pathways that mimics the directionality signaling successful extinction recall.     

Human gamma oscillations during slow wave sleep

Neocortical local field potentials have shown that gamma oscillations occur spontaneously during slow-wave sleep (SWS). At the macroscopic EEG level in the human brain, no evidences were reported so far. In this study, by using simultaneous scalp and intracranial EEG recordings in 20 epileptic subjects, we examined gamma oscillations in cerebral cortex during SWS. We report that gamma oscillations in low (30-50 Hz) and high (60-120 Hz) frequency bands recurrently emerged in all investigated regions and their amplitudes coincided with specific phases of the cortical slow wave. In most of the cases, multiple oscillatory bursts in different frequency bands from 30 to 120 Hz were correlated with positive peaks of scalp slow waves ("IN-phase" pattern), confirming previous animal findings. In addition, we report another gamma pattern that appears preferentially during the negative phase of the slow wave ("ANTI-phase" pattern). This new pattern presented dominant peaks in the high gamma range and was preferentially expressed in the temporal cortex. Finally, we found that the spatial coherence between cortical sites exhibiting gamma activities was local and fell off quickly when computed between distant sites. Overall, these results provide the first human evidences that gamma oscillations can be observed in macroscopic EEG recordings during sleep. They support the concept that these high-frequency activities might be associated with phasic increases of neural activity during slow oscillations. Such patterned activity in the sleeping brain could play a role in off-line processing of cortical networks.     

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

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

Smell-induced gamma oscillations in human olfactory cortex are required for accurate perception of odor identity

Studies of neuronal oscillations have contributed substantial insight into the mechanisms of visual, auditory, and somatosensory perception. However, progress in such research in the human olfactory system has lagged behind. As a result, the electrophysiological properties of the human olfactory system are poorly understood, and, in particular, whether stimulus-driven high-frequency oscillations play a role in odor processing is unknown. Here, we used direct intracranial recordings from human piriform cortex during an odor identification task to show that 3 key oscillatory rhythms are an integral part of the human olfactory cortical response to smell: Odor induces theta, beta, and gamma rhythms in human piriform cortex. We further show that these rhythms have distinct relationships with perceptual behavior. Odor-elicited gamma oscillations occur only during trials in which the odor is accurately perceived, and features of gamma oscillations predict odor identification accuracy, suggesting that they are critical for odor identity perception in humans. We also found that the amplitude of high-frequency oscillations is organized by the phase of low-frequency signals shortly following sniff onset, only when odor is present. Our findings reinforce previous work on theta oscillations, suggest that gamma oscillations in human piriform cortex are important for perception of odor identity, and constitute a robust identification of the characteristic electrophysiological response to smell in the human brain. Future work will determine whether the distinct oscillations we identified reflect distinct perceptual features of odor stimuli.

Intracranial recordings from human olfactory cortex reveal a characteristic spectrotemporal response to odors, including theta, beta and gamma oscillations, and show that high-frequency responses are critical for accurate perception of odors.     

Association between individual EEG characteristics and the level of intelligence

The aim of this study was to investigate the relationship between individual electroencephalogram (EEG) characteristics in the resting state and the level of nonverbal intelligence. The study involved 77 students of Demidov Yaroslavl State University. Analysis of the relationship between IQ and spectral parameters of EEG theta, alpha, and two subbands of beta oscillations revealed that the amplitude and power of alphaband EEG oscillations and low frequency beta-band EEG oscillations were positively correlated with the performance in the nonverbal intelligence test. The variety of brain periodic regimes was assessed using the correlation dimension (CD) of EEG. The correlation dimension can be used to quantify the degree of complexity of the nonlinear dynamical system. It was found that the value of the EEG correlation dimension was positively associated with the level of intelligence. The periodicity of the EEG signal was studied using autocorrelation analysis. It was shown that the autocorrelogram duration was negatively associated with IQ and the autocorrelogram amplitude was positively associated with IQ. A regression equation for predicting the level of nonverbal intelligence based on the power of theta- and beta-band oscillations, alpha-band oscillation indexes, and the amplitude and autocorrelation characteristics of the EEG signal was obtained.     

Theta returns

Recent physiological studies have implicated theta - a high-amplitude 4-8 Hz oscillation that is prominent in rat hippocampus during locomotion, orienting and other voluntary behaviors - in synaptic plasticity, information coding and the function of working memory. Intracranial recordings from human cortex have revealed evidence of high-amplitude theta oscillations throughout the brain, including the neocortex. Although its specific role is largely unknown, the observation of human theta has begun to reveal an intriguing connection between brain oscillations and cognitive processes.     

Interhemispheric EEG asymmetries during unilateral bright-light exposure and subsequent sleep in humans

We tested whether evening exposure to unilateral photic stimulation has repercussions on interhemispheric EEG asymmetries during wakefulness and later sleep. Because light exerts an alerting response in humans, which correlates with a decrease in waking EEG theta/alpha-activity and a reduction in sleep EEG delta activity, we hypothesized that EEG activity in these frequency bands show interhemispheric asymmetries after unilateral bright light (1,500 lux) exposure. A 2-h hemi-field light exposure acutely suppressed occipital EEG alpha activity in the ipsilateral hemisphere activated by light. Subjects felt more alert during bright light than dim light, an effect that was significantly more pronounced during activation of the right than the left visual cortex. During subsequent sleep, occipital EEG activity in the delta and theta range was significantly reduced after activation of the right visual cortex but not after stimulation of the left visual cortex. Furthermore, hemivisual field light exposure was able to shift the left predominance in occipital spindle EEG activity toward the stimulated hemisphere. Time course analysis revealed that this spindle shift remained significant during the first two sleep cycles. Our results reflect rather a hemispheric asymmetry in the alerting action of light than a use-dependent recovery function of sleep in response to the visual stimulation during prior waking. However, the observed shift in the spindle hemispheric dominance in the occipital cortex may still represent subtle local use-dependent recovery functions during sleep in a frequency range different from the delta range.     

Spectral analysis of EEG in normal rats and in rats genetically predisposed to seizures

Spectral and visual analyses were performed on the EEG of the motor and visual cortex, hippocampus, caudate nucleus, and intralaminary thalamic nuclei in two strains of rats; animals were maintained in a state of "awake immobility." It was found that KM rats, genetically predisposed to audiogenic fits, differed from the Wistar strain not subject to this genetic predisposition in that mean relative intensity of theta rhythm diminished and high amplitude slow irregular hippocampal activity intensified in the neocortex, as did generalized spindling. Susceptibility to seizure was reduced in KM rats as a result of protracted and graded increasing camphor administration to match the level of mean EEG spectral density changes characteristic of the Wistar strain. The part which brainstem reticular formation mechanisms may play in raising susceptibility to seizures is discussed, together with the EEG pattern characteristic of this condition.Institute of Higher Nervous Activity and Neurophysiology, Academy of Sciences of the USSR, Moscow. Translated from Neirofiziologiya, Vol. 19, No. 2, pp. 171–179, March–April, 1987.     

Learning to learn: theta oscillations predict new learning, which enhances related learning and neurogenesis

Animals in the natural world continuously encounter learning experiences of varying degrees of novelty. New neurons in the hippocampus are especially responsive to learning associations between novel events and more cells survive if a novel and challenging task is learned. One might wonder whether new neurons would be rescued from death upon each new learning experience or whether there is an internal control system that limits the number of cells that are retained as a function of learning. In this experiment, it was hypothesized that learning a task that was similar in content to one already learned previously would not increase cell survival. We further hypothesized that in situations in which the cells are rescued hippocampal theta oscillations (3-12 Hz) would be involved and perhaps necessary for increasing cell survival. Both hypotheses were disproved. Adult male Sprague-Dawley rats were trained on two similar hippocampus-dependent tasks, trace and very-long delay eyeblink conditioning, while recording hippocampal local-field potentials. Cells that were generated after training on the first task were labeled with bromodeoxyuridine and quantified after training on both tasks had ceased. Spontaneous theta activity predicted performance on the first task and the conditioned stimulus induced a theta-band response early in learning the first task. As expected, performance on the first task correlated with performance on the second task. However, theta activity did not increase during training on the second task, even though more cells were present in animals that had learned. Therefore, as long as learning occurs, relatively small changes in the environment are sufficient to increase the number of surviving neurons in the adult hippocampus and they can do so in the absence of an increase in theta activity. In conclusion, these data argue against an upper limit on the number of neurons that can be rescued from death by learning.     

Effect of bacterial lypopolysaccharide on penicillin-induced seizure activity in rats

In experiments on Wistar rats, we found that, within an early period (2 to 4 h) after injection of bacterial lypopolysaccharide, LPS (0.1 mg/kg, i.p.), the latency of generalized seizures induced by injection of benzylpenicillin (sodium salt; 3.0 million IU/kg, i.p.) became significantly shorter, while the severity of seizure manifestations was higher than in the control group. Within this period, the power of oscillations of the delta and alpha-frequency ranges increased in the frontal cortex and hippocampal structures; fast ECoG components (beta and gamma rhythms) were suppressed, and the power of the theta activity decreased. In the hippocampal structures, these changes were more clearly pronounced, as compared with the neocortex. Within a later period of the action of LPS (12 to 18 h from the moment of injection), the latency of penicillin-induced seizures significantly exceeded the control value, and the severity of such seizures was lower. Under such conditions, we observed a smaller power of the synchronized activity of delta and alpha frequencies combined with intensification of the theta activity (most clearly pronounced in the hippocampal structures), and also an increase in the power of “desynchronized” rhythms (beta and gamma oscillations) in the cortex and hippocampus. Neirofiziologiya/Neurophysiology, Vol. 40, No. 3, pp. 236–241, May–June, 2008.