Sharp waves and ripples

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Example of a sharp wave ripple recorded in CA3, unfiltered (top) and high-pass filtered trace (middle). Time-frequency plot (bottom) shows high frequencies (150-200 Hz) in the ascending phase of the SWR. Sharp wave ripple.tif
Example of a sharp wave ripple recorded in CA3, unfiltered (top) and high-pass filtered trace (middle). Time-frequency plot (bottom) shows high frequencies (150-200 Hz) in the ascending phase of the SWR.

Sharp waves and ripples (SPW-R), also called sharp wave ripples (SWR), are oscillatory patterns produced by extremely synchronized activity of neurons in the mammalian hippocampus and neighboring regions which occur spontaneously in idle waking states or during NREM sleep. [2] They can be observed with a variety of electrophysiological methods such as field recordings or EEG. They are composed of large amplitude sharp waves in local field potential and produced by thousands of neurons firing together within a 30–100 ms window. [2] Within this broad time window, pyramidal cells fire only at specific times set by fast spiking GABAergic interneurons. The fast rhythm of inhibition (150-200 Hz) synchronizes the firing of active pyramidal cells, each of which only fires one or two action potentials exactly between the inhibitory peaks, collectively generating the ripple pattern. SWRs have been extensively characterized by György Buzsáki and have been shown to be involved in memory consolidation in NREM sleep. Neuronal firing sequences acquired during wakefulness are replayed during SWRs.

Contents

History and background

Neuronal oscillations are important components of neuroscience research. During the last two decades, hippocampal oscillations have been a major focus in the research of neuronal oscillations. [3] Among different oscillations present in the brain, SWRs are the first population activity that start in the developing hippocampus. [4] Originally, these large waves were observed by Cornelius Vanderwolf in 1969. John O'Keefe investigated SWRs in 1978 while studying the spatial memory of rats. [3] György Buzsáki and his collaborators studied and characterized SWRs in further detail and described their physiological functions and role in different states of the animal. [3] [5]

These patterns are large amplitude, aperiodic recurrent oscillations occurring in the apical dendritic layer of the CA1 regions of the hippocampus. Sharp waves are followed by synchronous fast field oscillations (140–200 Hz frequency), named ripples. [6] Features of these oscillations provided evidences for their role in inducing synaptic plasticity and memory consolidation. Among these features are their widespread effect on the population of neurons in the hippocampus, and the experience-related activity of participating neurons. Studies have shown that elimination of SWRs by electrical stimulation interfered with the ability of rats to recall spatial memories. [7] [8] These features support functional role of sharp waves and ripples in memory consolidation.

Hippocampal formation

Structures

Circuit

Hippocampal circuit in rodent hippocampus. Connections between CA3 and CA1 regions with parahippocampal structures is shown. CajalHippocampus (modified).png
Hippocampal circuit in rodent hippocampus. Connections between CA3 and CA1 regions with parahippocampal structures is shown.

The trisynaptic loop, as the main circuit of the hippocampus responsible for information transfer between the hippocampus and the cortex, is also the circuit producing SWRs. This circuit provides the pathway by which SWRs affect the cortical areas, and also receive inputs from them. Consequently, this loop is shown to be the pathway responsible for conversion of short-term memory to long-term memory. The trisynaptic loop of the hippocampus is one of the most thoroughly studied circuits for long-term potentiation.

Participant neuronal populations

Emergence of these self-organized hippocampal events are dependent on interactions between pyramidal cells and different types of the interneurons in this circuit. Pyramidal cells of CA3 and CA1 are important in generating these waves, and they affect the subiculum, parasubiculum, entorhinal cortex, and ultimately neurons of the neocortex. [4] During SWRs, which last approximately 100 milliseconds, 50,000–100,000 neurons discharge in synchrony, making SWRs the most synchronous event in the brain. [4] An important concept about the neuronal populations participating in these events is the fact that they are experience-dependent. Sequences that have been active during the animal's activity are the ones participating in SWRs. Activity naturally spreads along the pathways that have stronger synapses. This is one of the features of SWRs providing evidence for their role in memory consolidation.

Network mechanisms of generation

Self-emergent network activity

Population bursts of pyramidal cells in the CA3 region of the hippocampus via CA3 collaterals cause depolarization of pyramidal cells in the dendritic layer of the CA1 which give rise to extracellular negative waves – the sharp waves – followed by fast ripples. [9] Discharge of pyramidal cells of CA3 region also activates the GABAergic interneurons. [4] Sparse firing of CA1 pyramidal cells and in-phase inhibition from the activated interneurons, give rise to high frequency (200 Hz) network oscillations, which are the ripples. [10] The rhythmic activity is exported to CA1 and eventually reaches the target population of parahippocampal structures. [11]

Effects of neocortical inputs

sleep spindle and K-complex in EEG Stage2sleep.svg
sleep spindle and K-complex in EEG

In spite of the self-emergent nature of the SWRs, their activity could be altered by inputs from the neocortex via the trisynaptic loop to the hippocampus. Activity of the neocortex during slow wave sleep determines inputs to the hippocampus; thalamocortical sleep spindles and delta waves are the sleep patterns of the neocortex. [12] These inputs contribute to the selection of different neuronal assemblies for initiation of SWRs, and affect the timing of the SWRs. [4] Different thalamocortical neuronal assemblies give rise to sleep spindles, and these cell assemblies affect the burst initiator for the sharp waves. In this manner, thalamocortical inputs affect the content of the SWRs going to neocortex.

Memory consolidation

Sharp waves and associated ripples are present in the mammalian brains of the species that have been investigated for this purpose, including mice, rats, rabbits, monkeys and humans. [6] In all of these species, they have been shown primarily to be involved in consolidation of recently acquired memories during the immobility and slow-wave sleep. Characteristics of these oscillations, such as having experience dependent neuronal content, being affected by the cortical input, and reactivating neocortical pathways formed through recent experiences, provides evidences for their role in memory consolidation. Besides, some direct evidences for their role come from studies, investigating effects of their removal. Animal studies indicated that depletion of ripple activity by electrical stimulation, would impair formation of new memories in rats. [8] [7] Furthermore, in spatially non-demanding tasks, such as passive exploration, optogenetic disruption of SWR events interferes with the stabilisation of the newly formed hippocampal place cell code (ref, [13] but see ref [14] ). As for humans, what is currently suspected is that the hippocampus as a whole is important for some forms of memory consolidation such as declarative and spatial memories. [3] However, clear evidence for the role of SWR events in memory consolidation in the hippocampus of humans is still missing.

Two-stage model of memory

Based on the research findings about SWRs, in 1989 an influential two-stage model of memory proposed by Buzsáki, that subsequent evidences supported it. Based on this model initial memories of the events are formed during the acquisition and reinforced during replay. Acquisition occurs by theta and gamma waves activating a neuronal pathway for initial formation of the memory. Later this pathway would get replayed following the SPW-Rs propagation to neocortex. Neuronal sequences during replay happen in a faster rate and are in both forward and reverse direction of the initial formation. [5]

Ripples and fast gamma

In spite of the fact that hippocampal ripples (140–220 Hz) and fast gamma (90–150 Hz) oscillations have similar mechanisms of generation, they are two distinct patterns in the hippocampus. They are both produced as the response of the CA1 region to inputs from the CA3 region. Ripples are only present when theta waves are relatively absent during sharp waves, whereas fast gamma waves occur during theta waves and sharp waves. [11] The magnitude and frequency of both ripples and fast gamma patterns are dependent on the magnitude of hippocampal sharp waves. Stronger excitation from sharp waves results in ripple oscillations, whereas weaker stimulations generate fast gamma patterns. [15] Besides they are shown to be region dependent, ripples that are the fastest oscillations are present in the CA1 region pyramidal cells while gamma oscillations dominate in CA3 region and parahippocampal structures. [11]

Disease state

Epilepsy

In addition to ongoing research on the role of SWR complexes in memory consolidation and neuronal plasticity, another major area of the attention is their role in development of epilepsy. One of the deviations from normal activity is fast ripples. Fast ripples are a pathologic pattern that emerges from the physiologic ripples. These fast ripples are field potentials of hypersynchronous bursting of excitatory neurons pyramidal cells at frequencies between 250 and 600 Hz. [16] Fast ripples in the hippocampus are considered as pathologic patterns directly associated with epilepsy, but they appear during both physiological and pathological states in neocortex. [17] Although the underlying physiology and identifying contributions of fast ripples in generation of seizures are still under investigation, some studies suggest that fast ripples could be used as a biomarker of epileptogenic tissues. [18]

See also

Other brain waves

Related Research Articles

<span class="mw-page-title-main">Entorhinal cortex</span> Area of the temporal lobe of the brain

The entorhinal cortex (EC) is an area of the brain's allocortex, located in the medial temporal lobe, whose functions include being a widespread network hub for memory, navigation, and the perception of time. The EC is the main interface between the hippocampus and neocortex. The EC-hippocampus system plays an important role in declarative (autobiographical/episodic/semantic) memories and in particular spatial memories including memory formation, memory consolidation, and memory optimization in sleep. The EC is also responsible for the pre-processing (familiarity) of the input signals in the reflex nictitating membrane response of classical trace conditioning; the association of impulses from the eye and the ear occurs in the entorhinal cortex.

<span class="mw-page-title-main">Hippocampus</span> Vertebrate brain region involved in memory consolidation

The hippocampus, also hippocampus proper, is a major component of the brain of humans and many other vertebrates. In the human brain the hippocampus, the dentate gyrus, and the subiculum are the components of the hippocampal formation located in the limbic system. The hippocampus plays important roles in the consolidation of information from short-term memory to long-term memory, and in spatial memory that enables navigation. In humans, and other primates the hippocampus is located in the archicortex, one of the three regions of allocortex, in each hemisphere with neural projections to the neocortex. The hippocampus, as the medial pallium, is a structure found in all vertebrates.

A gamma wave or gamma rhythm is a pattern of neural oscillation in humans with a frequency between 30 and 100 Hz, the 40 Hz point being of particular interest. Gamma rhythms are correlated with large-scale brain network activity and cognitive phenomena such as working memory, attention, and perceptual grouping, and can be increased in amplitude via meditation or neurostimulation. Altered gamma activity has been observed in many mood and cognitive disorders such as Alzheimer's disease, epilepsy, and schizophrenia.

Schaffer collaterals are axon collaterals given off by CA3 pyramidal cells in the hippocampus. These collaterals project to area CA1 of the hippocampus and are an integral part of memory formation and the emotional network of the Papez circuit, and of the hippocampal trisynaptic loop. It is one of the most studied synapses in the world and named after the Hungarian anatomist-neurologist Károly Schaffer.

An apical dendrite is a dendrite that emerges from the apex of a pyramidal cell. Apical dendrites are one of two primary categories of dendrites, and they distinguish the pyramidal cells from spiny stellate cells in the cortices. Pyramidal cells are found in the prefrontal cortex, the hippocampus, the entorhinal cortex, the olfactory cortex, and other areas. Dendrite arbors formed by apical dendrites are the means by which synaptic inputs into a cell are integrated. The apical dendrites in these regions contribute significantly to memory, learning, and sensory associations by modulating the excitatory and inhibitory signals received by the pyramidal cells.

Theta waves generate the theta rhythm, a neural oscillation in the brain that underlies various aspects of cognition and behavior, including learning, memory, and spatial navigation in many animals. It can be recorded using various electrophysiological methods, such as electroencephalogram (EEG), recorded either from inside the brain or from electrodes attached to the scalp.

In the rodent, the parasubiculum is a retrohippocampal isocortical structure, and a major component of the subicular complex. It receives numerous subcortical and cortical inputs, and sends major projections to the superficial layers of the entorhinal cortex.

<span class="mw-page-title-main">Perforant path</span>

In the brain, the perforant path or perforant pathway provides a connectional route from the entorhinal cortex to all fields of the hippocampal formation, including the dentate gyrus, all CA fields, and the subiculum.

<span class="mw-page-title-main">Median raphe nucleus</span> Brain region having polygonal, fusiform, piriform neurons

The median raphe nucleus(MRN), also known as the superior central nucleus, is a nucleus in the brainstem composed of polygonal, fusiform, and piriform neurons, which exists rostral to the pontine raphe nucleus. The median raphe nucleus is one of several raphe nuclei that lies on the brainstem midline. It is one of two nuclei that are situated more superior to the others. The second of these nuclei is the dorsal raphe nucleus (DRN). The MRN extends from the lower part of the dorsal raphe nucleus to an approximate position at the decussation of the superior cerebellar peduncle.

<span class="mw-page-title-main">Mossy fiber (hippocampus)</span> Pathway in the hippocampus

In the hippocampus, the mossy fiber pathway consists of unmyelinated axons projecting from granule cells in the dentate gyrus that terminate on modulatory hilar mossy cells and in Cornu Ammonis area 3 (CA3), a region involved in encoding short-term memory. These axons were first described as mossy fibers by Santiago Ramón y Cajal as they displayed varicosities along their lengths that gave them a mossy appearance.

Recurrent thalamo-cortical resonance or Thalamocortical oscillation is an observed phenomenon of oscillatory neural activity between the thalamus and various cortical regions of the brain. It is proposed by Rodolfo Llinas and others as a theory for the integration of sensory information into the whole of perception in the brain. Thalamocortical oscillation is proposed to be a mechanism of synchronization between different cortical regions of the brain, a process known as temporal binding. This is possible through the existence of thalamocortical networks, groupings of thalamic and cortical cells that exhibit oscillatory properties.

Synaptic noise refers to the constant bombardment of synaptic activity in neurons. This occurs in the background of a cell when potentials are produced without the nerve stimulation of an action potential, and are due to the inherently random nature of synapses. These random potentials have similar time courses as excitatory postsynaptic potentials (EPSPs) and inhibitory postsynaptic potentials (IPSPs), yet they lead to variable neuronal responses. The variability is due to differences in the discharge times of action potentials.

The trisynaptic circuit or trisynaptic loop is a relay of synaptic transmission in the hippocampus. The trisynaptic circuit is a neural circuit in the hippocampus, which is made up of three major cell groups: granule cells in the dentate gyrus, pyramidal neurons in CA3, and pyramidal neurons in CA1. The hippocampal relay involves 3 main regions within the hippocampus which are classified according to their cell type and projection fibers. The first projection of the hippocampus occurs between the entorhinal cortex (EC) and the dentate gyrus (DG). The entorhinal cortex transmits its signals from the parahippocampal gyrus to the dentate gyrus via granule cell fibers known collectively as the perforant path. The dentate gyrus then synapses on pyramidal cells in CA3 via mossy cell fibers. CA3 then fires to CA1 via Schaffer collaterals which synapse in the subiculum and are carried out through the fornix. Collectively the dentate gyrus, CA1 and CA3 of the hippocampus compose the trisynaptic loop.

<span class="mw-page-title-main">Hippocampus anatomy</span> Component of brain anatomy

Hippocampus anatomy describes the physical aspects and properties of the hippocampus, a neural structure in the medial temporal lobe of the brain. It has a distinctive, curved shape that has been likened to the sea-horse monster of Greek mythology and the ram's horns of Amun in Egyptian mythology. This general layout holds across the full range of mammalian species, from hedgehog to human, although the details vary. For example, in the rat, the two hippocampi look similar to a pair of bananas, joined at the stems. In the human and other primates, the portion of the hippocampus near the base of the temporal lobe is much broader than the part at the top. Due to the three-dimensional curvature of this structure, two-dimensional sections such as shown are commonly seen. Neuroimaging pictures can show a number of different shapes, depending on the angle and location of the cut.

<span class="mw-page-title-main">Large irregular activity</span>

Large (amplitude) irregular activity (LIA), refers to one of two local field states that have been observed in the hippocampus. The other field state is that of the theta rhythm. The theta state is characterised by a steady slow oscillation of around 6–7 Hz. LIA has a predominantly lower oscillation frequency but contains some sharp spikes, called sharp waves of a higher frequency than that of theta. LIA accompanies the small irregular activity state to which the term LIA has been used to describe overall.

Hippocampal replay is a phenomenon observed in rats, mice, cats, rabbits, songbirds and monkeys. During sleep or awake rest, replay refers to the re-occurrence of a sequence of cell activations that also occurred during activity, but the replay has a much faster time scale. It may be in the same order, or in reverse. Cases were also found where a sequence of activations occurs before the actual activity, but it is still the same sequence. This is called preplay.

György Buzsáki is the Biggs Professor of Neuroscience at New York University School of Medicine.

<span class="mw-page-title-main">Hippocampal subfields</span> Part of the brain of mammals

The hippocampal subfields are four subregions that make up the structure of the hippocampus. The subfields CA1, CA2, CA3, and CA4 use the initials of cornu Ammonis, an earlier name of the hippocampus.

<span class="mw-page-title-main">Phase precession</span> Neural mechanism

Phase precession is a neurophysiological process in which the time of firing of action potentials by individual neurons occurs progressively earlier in relation to the phase of the local field potential oscillation with each successive cycle. In place cells, a type of neuron found in the hippocampal region of the brain, phase precession is believed to play a major role in the neural coding of information. John O'Keefe, who later shared the 2014 Nobel Prize in Physiology or Medicine for his discovery that place cells help form a "map" of the body's position in space, co-discovered phase precession with Michael Recce in 1993.

<span class="mw-page-title-main">High-frequency oscillations</span> Brainwaves with frequencies larger than 80 Hz

High-frequency oscillations (HFO) are brain waves of the frequency faster than ~80 Hz, generated by neuronal cell population. High-frequency oscillations can be recorded during an electroencephalagram (EEG), local field potential (LFP) or electrocorticogram (ECoG) electrophysiology recordings. They are present in physiological state during sharp waves and ripples - oscillatory patterns involved in memory consolidation processes. HFOs are associated with pathophysiology of the brain like epileptic seizure and are often recorded during seizure onset. It makes a promising biomarker for the identification of the epileptogenic zone. Other studies points to the HFO role in psychiatric disorders and possible implications to psychotic episodes in schizophrenia.

References

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