Phase precession: Difference between revisions
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Although simple [[rate coding]] 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 the other cells in the [[neural ensemble|local population]].<ref name=Dual>{{cite journal | vauthors = O'Keefe J, Burgess N | title = Dual phase and rate coding in hippocampal place cells: theoretical significance and relationship to entorhinal grid cells | journal = Hippocampus | volume = 15 | issue = 7 | pages = 853–66 | date = 6 September 2005 | pmid = 16145693 | doi = 10.1002/hipo.20115 }}</ref><ref name=Computations>{{cite journal | vauthors = Burgess N, O'Keefe J | title = Neuronal computations underlying the firing of place cells and their role in navigation | journal = Hippocampus | volume = 6 | issue = 6 | pages = 749–62 | date = 1996 | pmid = 9034860 | doi = 10.1002/(SICI)1098-1063(1996)6:6<749::AID-HIPO16>3.0.CO;2-0 }}</ref> As the larger population of cells fire occasionally outside of their individual place fields, the firing patterns are organized to occur synchronously to form [[waveform|wavelike]] [[voltage]] oscillations. These oscillations are measurable in [[local field potential]]s and [[electroencephalography]] (EEG). In the [[Region I of hippocampus proper|CA1 region]] of the hippocampus, where the place cells are located, these firing patterns give rise to [[theta wave]]s.<ref name=Theta>{{cite journal | vauthors = Skaggs WE, McNaughton BL, Wilson MA, Barnes CA | title = Theta phase precession in hippocampal neuronal populations and the compression of temporal sequences | journal = Hippocampus | volume = 6 | issue = 2 | pages = 149–72 | date = 1996 | pmid = 8797016 | doi = 10.1002/(SICI)1098-1063(1996)6:2<149::AID-HIPO6>3.0.CO;2-K }}</ref> Theta oscillations have classically been described in rats, but evidence is emerging that they also occur in humans.<ref>{{cite journal | vauthors = Bohbot VD, Copara MS, Gotman J, Ekstrom AD | title = Low-frequency theta oscillations in the human hippocampus during real-world and virtual navigation | journal = Nature Communications | volume = 8 | pages = 14415 | date = February 2017 | pmid = 28195129 | pmc = 5316881 | doi = 10.1038/ncomms14415 }}</ref> |
Although simple [[rate coding]] 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 the other cells in the [[neural ensemble|local population]].<ref name=Dual>{{cite journal | vauthors = O'Keefe J, Burgess N | title = Dual phase and rate coding in hippocampal place cells: theoretical significance and relationship to entorhinal grid cells | journal = Hippocampus | volume = 15 | issue = 7 | pages = 853–66 | date = 6 September 2005 | pmid = 16145693 | doi = 10.1002/hipo.20115 }}</ref><ref name=Computations>{{cite journal | vauthors = Burgess N, O'Keefe J | title = Neuronal computations underlying the firing of place cells and their role in navigation | journal = Hippocampus | volume = 6 | issue = 6 | pages = 749–62 | date = 1996 | pmid = 9034860 | doi = 10.1002/(SICI)1098-1063(1996)6:6<749::AID-HIPO16>3.0.CO;2-0 }}</ref> As the larger population of cells fire occasionally outside of their individual place fields, the firing patterns are organized to occur synchronously to form [[waveform|wavelike]] [[voltage]] oscillations. These oscillations are measurable in [[local field potential]]s and [[electroencephalography]] (EEG). In the [[Region I of hippocampus proper|CA1 region]] of the hippocampus, where the place cells are located, these firing patterns give rise to [[theta wave]]s.<ref name=Theta>{{cite journal | vauthors = Skaggs WE, McNaughton BL, Wilson MA, Barnes CA | title = Theta phase precession in hippocampal neuronal populations and the compression of temporal sequences | journal = Hippocampus | volume = 6 | issue = 2 | pages = 149–72 | date = 1996 | pmid = 8797016 | doi = 10.1002/(SICI)1098-1063(1996)6:2<149::AID-HIPO6>3.0.CO;2-K }}</ref> Theta oscillations have classically been described in rats, but evidence is emerging that they also occur in humans.<ref>{{cite journal | vauthors = Bohbot VD, Copara MS, Gotman J, Ekstrom AD | title = Low-frequency theta oscillations in the human hippocampus during real-world and virtual navigation | journal = Nature Communications | volume = 8 | pages = 14415 | date = February 2017 | pmid = 28195129 | pmc = 5316881 | doi = 10.1038/ncomms14415 }}</ref> |
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[[File:eeg theta.svg|thumb|right|350px|alt=A wavelike curvy line, with time in seconds labeled at the bottom| |
[[File:eeg theta.svg|thumb|right|350px|alt=A wavelike curvy line, with time in seconds labeled at the bottom|An [[Electroencephalography|EEG]] [[theta wave]]]] |
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In 1993, O'Keefe and Recce discovered a relationship between the theta wave and the firing patterns of individual place cells.<ref name="OKeefe1993"/> 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 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 moved 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 became synchronous again with the wave, aligned now with one wave maximum earlier than before. They termed this advancement relative to the wave phase "phase [[Spin wave#Theory|precession]]". Subsequent studies showed that each time a rat entered a completely different area and the phase fields would be [[Phase resetting in neurons|remapped]], place cells would again become phase-locked to the theta rhythm.<ref>{{cite journal | vauthors = Bose A, Recce M | title = Phase precession and phase-locking of hippocampal pyramidal cells | journal = Hippocampus | volume = 11 | issue = 3 | pages = 204–15 | date = 19 June 2001 | pmid = 11769305 | doi = 10.1002/hipo.1038 }}</ref> It is now widely accepted that the anti-phase cell firing that results from phase precession is itself an important component of information [[Phase response curve|coding]] about place.<ref name="Moser 69–77"/><ref name=Dual/><ref name=Computations/><ref name=Theta/> |
In 1993, O'Keefe and Recce discovered a relationship between the theta wave and the firing patterns of individual place cells.<ref name="OKeefe1993"/> 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 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 moved 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 became synchronous again with the wave, aligned now with one wave maximum earlier than before. They termed this advancement relative to the wave phase "phase [[Spin wave#Theory|precession]]". Subsequent studies showed that each time a rat entered a completely different area and the phase fields would be [[Phase resetting in neurons|remapped]], place cells would again become phase-locked to the theta rhythm.<ref>{{cite journal | vauthors = Bose A, Recce M | title = Phase precession and phase-locking of hippocampal pyramidal cells | journal = Hippocampus | volume = 11 | issue = 3 | pages = 204–15 | date = 19 June 2001 | pmid = 11769305 | doi = 10.1002/hipo.1038 }}</ref> It is now widely accepted that the anti-phase cell firing that results from phase precession is itself an important component of information [[Phase response curve|coding]] about place.<ref name="Moser 69–77"/><ref name=Dual/><ref name=Computations/><ref name=Theta/> |
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Revision as of 22:46, 27 January 2018
Phase precession is a neurophysiological process in which the firing of action potentials by individual neurons is timed in relation to the phase of neural oscillations of the surrounding cells. In hippocampal place cells, phase precession is believed to play a major role in the neural coding of information. John O'Keefe won the 2014 Nobel Prize in Physiology or Medicine partly for co-discovering this phenomenon with Michael Recce.[1][2]
Place cells
Pyramidal cells in the hippocampus called place cells play a significant role in self-location during movement.[3] As a rat moves along a path, individual place cells fire at an increased rate at specific locations along the path, termed place fields. There is a maximal firing rate, with action potentials occurring in rapid bursts, at the position encoded by that cell, and only occasional firing at other positions.[4] Within a relatively small path, the same cells are repeatedly activated as the animal returns to the same position.
Although simple rate coding 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 the other cells in the local population.[5][6] As the larger population of cells fire occasionally outside of their individual place fields, the firing patterns are organized to occur synchronously to form 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 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 moved 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 became synchronous again with the wave, aligned now with one wave maximum earlier than before. They 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 phase 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 itself an important component of information coding about place.[3][5][6][7]
References
- ^ a b 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.
- ^ "The Nobel Prize in Physiology or Medicine 2014". www.nobelprize.org.
- ^ a b Moser EI, Kropff E, Moser MB (2008-02-19). "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.
- ^ 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. doi:10.1073/pnas.94.1.343. PMC 19339. PMID 8990211.
- ^ a b 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. PMID 16145693.
- ^ a b Burgess N, O'Keefe J (1996). "Neuronal computations underlying the firing of place cells and their role in navigation". Hippocampus. 6 (6): 749–62. doi:10.1002/(SICI)1098-1063(1996)6:6<749::AID-HIPO16>3.0.CO;2-0. PMID 9034860.
- ^ a b 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.
- ^ 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. doi:10.1038/ncomms14415. PMC 5316881. PMID 28195129.
- ^ 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.