Phase precession

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Place Cell Spiking Activity Example.png
Spatial firing patterns of 8 place cells recorded from the hippocampal CA1 layer of a rat's brain. Dots indicate positions (place fields) where action potentials were recorded as the rat moved back and forth along a track, with color indicating which neuron emitted that action potential.
Place field spikes cropped.jpg
Action potentials (one in the box) recorded from a single place cell during a burst of activity
Eeg theta.svg
An EEG theta wave

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. [1] [2]

Contents

Place cells

Pyramidal cells in the hippocampus called place cells play a significant role in self-location during movement over short distances. [3] As a rat moves along a path, individual place cells fire action potentials at an increased rate at particular positions along the path, termed "place fields". Each place cell's maximum firing rate –with action potentials occurring in rapid bursts  –occurs at the position encoded by that cell; and that cell fires only occasionally when the animal is at other locations. [4] Within a relatively small path, the same cells are repeatedly activated as the animal returns to the same position.

Although simple rate coding (the coding of information based on whether neurons fire more rapidly or more slowly) resulting from these changes in firing rates may account for some of the neural coding of position, there is also a prominent role for the timing of the action potentials of a single place cell, relative to the firing of nearby cells in the local population. [5] [6] As the larger population of cells fire occasionally when the rat is outside of the cells' individual place fields, the firing patterns are organized to occur synchronously, forming wavelike voltage oscillations. These oscillations are measurable in local field potentials and electroencephalography (EEG). In the CA1 region of the hippocampus, where the place cells are located, these firing patterns give rise to theta waves. [7] Theta oscillations have classically been described in rats, but evidence is emerging that they also occur in humans. [8]

In 1993, O'Keefe and Recce discovered a relationship between the theta wave and the firing patterns of individual place cells. [1] Although the occasional action potentials of cells when rats were outside of the place fields occurred in phase with (at the peaks of) the theta waves, the bursts of more rapid spikes elicited when the rats reached the place fields were out of synchrony with the oscillation. As a rat approached the place field, the corresponding place cell would fire slightly in advance of the theta wave peak. As the rat moved closer and closer, each successive action potential occurred earlier and earlier within the wave cycle. At the center of the place field, when the cell would fire at its maximal rate, the firing had been advanced sufficiently to be anti-phase to the theta potential (at the bottom, rather than at the peak, of the theta waveform). Then, as the rat continued to move on past the place field and the cell firing slowed, the action potentials continued to occur progressively earlier relative to the theta wave, until they again became synchronous with the wave, aligned now with one wave peak earlier than before. O'Keefe and Recce termed this advancement relative to the wave phase "phase precession". Subsequent studies showed that each time a rat entered a completely different area and the place fields would be remapped, place cells would again become phase-locked to the theta rhythm. [9] It is now widely accepted that the anti-phase cell firing that results from phase precession is an important component of information coding about place. [3] [5] [6] [7] [10]

Other systems

Schematic of phase precession in three place cells. A rat runs left-to-right and the firing of the cells (shown as colored tick marks) is spatially localized, with the three place fields (represented by the three colors) overlapping. The local field potential theta rhythm is shown at the bottom in black. The action potentials of each cell occur earlier and earlier with respect to the theta peak on each successive cycle - this is phase precession. One consequence of this is that within a single theta cycle (blue-shaded rectangle, for example) the cells fire in the same sequence in time as their triggering is organized in space: thus converting a spatial code into a temporal one. Phase precession.jpg
Schematic of phase precession in three place cells. A rat runs left-to-right and the firing of the cells (shown as colored tick marks) is spatially localized, with the three place fields (represented by the three colors) overlapping. The local field potential theta rhythm is shown at the bottom in black. The action potentials of each cell occur earlier and earlier with respect to the theta peak on each successive cycle – this is phase precession. One consequence of this is that within a single theta cycle (blue-shaded rectangle, for example) the cells fire in the same sequence in time as their triggering is organized in space: thus converting a spatial code into a temporal one.

There have been conflicting theories of how neurons in and around the hippocampus give rise to theta waves and consequently give rise to phase precession. As these mechanisms became better understood, the existence of phase precession was increasingly accepted by researchers. [10] This, in turn, gave rise to the question of whether phase precession could be observed in any other regions of the brain, with other kinds of cell circuits, or whether phase precession was a peculiar property of hippocampal tissue. [10] The finding that theta wave phase precession is also a property of grid cells in the entorhinal cortex demonstrated that the phenomenon exists in other parts of the brain that also mediate information about movement. [11]

Theta wave phase precession in the hippocampus also plays a role in some brain functions that are unrelated to spatial location. When rats were trained to jump up to the rim of a box, place cells displayed phase precession much as they do during movement along a path, but a subset of the place cells showed phase precession that was related to initiating the jump, independently of spatial location, and not related to the position during the jump. [12]

Phase precession in the entorhinal cortex has been hypothesized to arise from an attractor network process, so that two sequential neural representations within a single cycle of the theta oscillation can be temporally linked to each other downstream in the hippocampus, as episodic memories. [13]

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 is a major component of the brain of humans and other vertebrates. Humans and other mammals have two hippocampi, one in each side of the brain. The hippocampus is part of the limbic system, and plays important roles in the consolidation of information from short-term memory to long-term memory, and in spatial memory that enables navigation. The hippocampus is located in the allocortex, with neural projections into the neocortex, in humans as well as other primates. The hippocampus, as the medial pallium, is a structure found in all vertebrates. In humans, it contains two main interlocking parts: the hippocampus proper, and the dentate gyrus.

<span class="mw-page-title-main">Place cell</span> Place-activated hippocampus cells found in some mammals

A place cell is a kind of pyramidal neuron in the hippocampus that becomes active when an animal enters a particular place in its environment, which is known as the place field. Place cells are thought to act collectively as a cognitive representation of a specific location in space, known as a cognitive map. Place cells work with other types of neurons in the hippocampus and surrounding regions to perform this kind of spatial processing. They have been found in a variety of animals, including rodents, bats, monkeys and humans.

<span class="mw-page-title-main">Subiculum</span> Most inferior part of the hippocampal formation

The subiculum is the most inferior component of the hippocampal formation. It lies between the entorhinal cortex and the CA1 subfield of the hippocampus proper.

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">Hippocampal formation</span> Region of the temporal lobe in mammalian brains

The hippocampal formation is a compound structure in the medial temporal lobe of the brain. It forms a c-shaped bulge on the floor of the temporal horn of the lateral ventricle. There is no consensus concerning which brain regions are encompassed by the term, with some authors defining it as the dentate gyrus, the hippocampus proper and the subiculum; and others including also the presubiculum, parasubiculum, and entorhinal cortex. The hippocampal formation is thought to play a role in memory, spatial navigation and control of attention. The neural layout and pathways within the hippocampal formation are very similar in all mammals.

<span class="mw-page-title-main">Grid cell</span>

A grid cell is a type of neuron within the entorhinal cortex that fires at regular intervals as an animal navigates an open area, allowing it to understand its position in space by storing and integrating information about location, distance, and direction. Grid cells have been found in many animals, including rats, mice, bats, monkeys, and humans.

<span class="mw-page-title-main">Michael Hasselmo</span> American neuroscientist

Michael Hasselmo is an American neuroscientist and professor in the Department of Psychological and Brain Sciences at Boston University. He is the director of the Center for Systems Neuroscience and is editor-in-chief of Hippocampus (journal). Hasselmo studies oscillatory dynamics and neuromodulatory regulation in cortical mechanisms for memory guided behavior and spatial navigation using a combination of neurophysiological and behavioral experiments in conjunction with computational modeling. In addition to his peer-reviewed publications, Hasselmo wrote the book How We Remember: Brain Mechanisms of Episodic Memory.

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.

The trisynaptic circuit, or trisynaptic loop is a relay of synaptic transmission in the hippocampus. The circuit was initially described by the neuroanatomist Santiago Ramon y Cajal, in the early twentieth century, using the Golgi staining method. After the discovery of the trisynaptic circuit, a series of research has been conducted to determine the mechanisms driving this circuit. Today, research is focused on how this loop interacts with other parts of the brain, and how it influences human physiology and behaviour. For example, it has been shown that disruptions within the trisynaptic circuit lead to behavioural changes in rodent and feline models.

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

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 primate brains, including humans, 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">Boundary cell</span>

Boundary cells are neurons found in the hippocampal formation that respond to the presence of an environmental boundary at a particular distance and direction from an animal. The existence of cells with these firing characteristics were first predicted on the basis of properties of place cells. Boundary cells were subsequently discovered in several regions of the hippocampal formation: the subiculum, presubiculum and entorhinal cortex.

<span class="mw-page-title-main">Edvard Moser</span> Norwegian psychologist and neuroscientist

Edvard Ingjald Moser is a Norwegian psychologist and neuroscientist, who is a professor at the Norwegian University of Science and Technology (NTNU) in Trondheim. In 2005, he and his then-wife May-Britt Moser discovered grid cells in the brain's medial entorhinal cortex. Grid cells are specialized neurons that provide the brain with a coordinate system and a metric for space. In 2018, he discovered a neural network that expresses a person's sense of time in experiences and memories located in the brain's lateral entorhinal cortex.

<span class="mw-page-title-main">May-Britt Moser</span> Norwegian psychologist and neuroscientist

May-Britt Moser is a Norwegian psychologist and neuroscientist, who is a Professor of Psychology and Neuroscience at the Norwegian University of Science and Technology (NTNU). She and her former husband, Edvard Moser, shared half of the 2014 Nobel Prize in Physiology or Medicine, awarded for work concerning the grid cells in the entorhinal cortex, as well as several additional space-representing cell types in the same circuit that make up the positioning system in the brain. Together with Edvard Moser she established the Moser research environment at NTNU, which they lead. Since 2012 she has headed the Centre for Neural Computation.

<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.

Sharp waves and ripples (SWRs) are oscillatory patterns produced by extremely synchronised activity of neurons in the mammalian hippocampus and neighbouring regions which occur spontaneously in idle waking states or during NREM sleep. They can be observed with a variety of imaging methods, such as EEG. They are composed of large amplitude sharp waves in local field potential and produced by tens of thousands of neurons firing together within 30–100 ms window. They are some of the most synchronous oscillations patterns in the brain, making them susceptible to pathological patterns such as epilepsy.They have been extensively characterised and described by György Buzsáki and have been shown to be involved in memory consolidation in NREM sleep and the replay of memories acquired during wakefulness.

<span class="mw-page-title-main">Phase resetting in neurons</span> Behavior observed in neurons

Phase resetting in neurons is a behavior observed in different biological oscillators and plays a role in creating neural synchronization as well as different processes within the body. Phase resetting in neurons is when the dynamical behavior of an oscillation is shifted. This occurs when a stimulus perturbs the phase within an oscillatory cycle and a change in period occurs. The periods of these oscillations can vary depending on the biological system, with examples such as: (1) neural responses can change within a millisecond to quickly relay information; (2) In cardiac and respiratory changes that occur throughout the day, could be within seconds; (3) circadian rhythms may vary throughout a series of days; (4) rhythms such as hibernation may have periods that are measured in years. This activity pattern of neurons is a phenomenon seen in various neural circuits throughout the body and is seen in single neuron models and within clusters of neurons. Many of these models utilize phase response (resetting) curves where the oscillation of a neuron is perturbed and the effect the perturbation has on the phase cycle of a neuron is measured.

<span class="mw-page-title-main">John O'Keefe (neuroscientist)</span> American–British neuroscientist

John O'Keefe, is an American-British neuroscientist, psychologist and a professor at the Sainsbury Wellcome Centre for Neural Circuits and Behaviour and the Research Department of Cell and Developmental Biology at University College London. He discovered place cells in the hippocampus, and that they show a specific kind of temporal coding in the form of theta phase precession. He shared the Nobel Prize in Physiology or Medicine in 2014, together with May-Britt Moser and Edvard Moser; he has received several other awards. He has worked at University College London for his entire career, but also held a part-time chair at the Norwegian University of Science and Technology at the behest of his Norwegian collaborators, the Mosers.

Lisa Giocomo is an American neuroscientist who is a Professor in the Department of Neurobiology at Stanford University School of Medicine. Giocomo probes the molecular and cellular mechanisms underlying cortical neural circuits involved in spatial navigation and memory.

References

  1. 1 2 O'Keefe J, Recce ML (July 1993). "Phase relationship between hippocampal place units and the EEG theta rhythm". Hippocampus. 3 (3): 317–30. doi:10.1002/hipo.450030307. PMID   8353611. S2CID   6539236.
  2. ↑ "The Nobel Prize in Physiology or Medicine 2014: John O'Keefe – Biographical". Nobelprize.org. Archived from the original on 29 September 2017. Retrieved 27 January 2018.
  3. 1 2 Moser EI, Kropff E, Moser MB (19 February 2008). "Place cells, grid cells, and the brain's spatial representation system". Annual Review of Neuroscience. 31: 69–89. doi:10.1146/annurev.neuro.31.061307.090723. PMID   18284371.
  4. ↑ Bures J, Fenton AA, Kaminsky Y, Zinyuk L (January 1997). "Place cells and place navigation". Proceedings of the National Academy of Sciences of the United States of America. 94 (1): 343–50. Bibcode:1997PNAS...94..343B. doi: 10.1073/pnas.94.1.343 . PMC   19339 . PMID   8990211.
  5. 1 2 O'Keefe J, Burgess N (6 September 2005). "Dual phase and rate coding in hippocampal place cells: theoretical significance and relationship to entorhinal grid cells". Hippocampus. 15 (7): 853–66. doi:10.1002/hipo.20115. PMC   2677681 . PMID   16145693.
  6. 1 2 Burgess N, O'Keefe J (1996). "Neuronal computations underlying the firing of place cells and their role in navigation". Hippocampus. 6 (6): 749–62. CiteSeerX   10.1.1.17.344 . doi:10.1002/(SICI)1098-1063(1996)6:6<749::AID-HIPO16>3.0.CO;2-0. PMID   9034860. S2CID   3162072.
  7. 1 2 Skaggs WE, McNaughton BL, Wilson MA, Barnes CA (1996). "Theta phase precession in hippocampal neuronal populations and the compression of temporal sequences". Hippocampus. 6 (2): 149–72. doi:10.1002/(SICI)1098-1063(1996)6:2<149::AID-HIPO6>3.0.CO;2-K. PMID   8797016. S2CID   15813385.
  8. ↑ Bohbot VD, Copara MS, Gotman J, Ekstrom AD (February 2017). "Low-frequency theta oscillations in the human hippocampus during real-world and virtual navigation". Nature Communications. 8: 14415. Bibcode:2017NatCo...814415B. doi:10.1038/ncomms14415. PMC   5316881 . PMID   28195129.
  9. ↑ Bose A, Recce M (19 June 2001). "Phase precession and phase-locking of hippocampal pyramidal cells". Hippocampus. 11 (3): 204–15. doi:10.1002/hipo.1038. PMID   11769305. S2CID   14194416.
  10. 1 2 3 Buzsáki G (2006). Rhythms of the Brain. Oxford University Press. pp. 308–26. ISBN   978-0195301069. Archived from the original on 26 February 2018.
  11. ↑ Hafting T, Fyhn M, Bonnevie T, Moser MB, Moser EI (June 2008). "Hippocampus-independent phase precession in entorhinal grid cells". Nature. 453 (7199): 1248–52. Bibcode:2008Natur.453.1248H. doi:10.1038/nature06957. PMID   18480753. S2CID   597353.
  12. ↑ Lenck-Santini PP, Fenton AA, Muller RU (July 2008). "Discharge properties of hippocampal neurons during performance of a jump avoidance task". The Journal of Neuroscience. 28 (27): 6773–86. doi:10.1523/JNEUROSCI.5329-07.2008. PMC   2636898 . PMID   18596153.
  13. ↑ Kovács KA (September 2020). "Episodic Memories: How do the Hippocampus and the Entorhinal Ring Attractors Cooperate to Create Them?". Frontiers in Systems Neuroscience. 14: 68. doi: 10.3389/fnsys.2020.559186 . PMC   7511719 . PMID   33013334.
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