Place cell

Place cells are neurons in the hippocampus that exhibit a high rate of firing whenever an animal is in a specific location in an environment corresponding to the cell's "place field". These neurons are distinct from other neurons with spatial firing properties, such as grid cells, border cells, head direction cells, and spatial view cells. In the CA1 and CA3 hippocampal subfields, place cells are believed to be pyramidal cells, while those in the dentate gyrus are believed to be granule cells.[2]

Place cells were first described in rats by O'Keefe and Dostrovsky.[3] Based on this discovery, O'Keefe and Nadel hypothesized that the primary function of the rat hippocampus is to form a cognitive map of the rat's environment.[4] Ekstrom and colleagues have found cells with similar properties in the human hippocampus, using extracellular recordings from epilepsy patients undergoing invasive monitoring of their brain activity.[5]

Contents

Place fields

Place cells show increased frequency of firing when an animal is in a specific area referred to as the cell's place field. The firing rate increase can be quite dramatic, from virtually zero outside the field to as much as 100 Hz (for brief periods) in the middle of the place field. When a rat forages randomly in an environment, place fields are only weakly modulated by the direction the rat faces, or not at all. However, when an animal engages in stereotyped behaviour (e.g. shuttling between goal locations), place cells tend to be active in the place field on passes in one direction only.[6]

On initial exposure to a new environment, place fields become established within minutes. The place fields of cells tend to be stable over repeated exposures to the same environment. In a different environment, however, a cell may have a completely different place field or no place field at all. This phenomenon is referred to as "remapping". In any particular environment, roughly 40-50% of the hippocampal place cells will be active.[7][8]

In an environment with few or no directional cues (for instance, a circular environment surrounded by black curtains), place fields will tend to have a fixed radial position, but the entire set of place fields may rotate around the maze as predicted by a theory that rats are slowly losing their orientation.[9] If a polarizing cue is introduced (commonly a large white rectangle of paper), place fields will tend to have fixed positions relative to the cue. If the cue is moved while the animal can see it, place fields will tend to remain unaffected; however, if the animal is briefly removed from the environment then the cue is moved and the animal returned, the place fields will rotate so as to maintain their position relative to the cue card. Although visual cues seem to be the primary determinant of place cell firing, it is worth noting that firing persists in the dark, suggesting that proprioception or other senses contribute as well.

In an environment in which a rat is constrained to walk along a linear track, place fields will often have a directional component in addition to a place component. A place cell that fires at a particular location while the rat walks in one direction along the track will not necessarily fire as the rat visits that location from the other direction. If the rat frequently turns around at the same point, however, place fields there will often be independent of direction.

The size of place fields and their signal to noise ratio varies depending on the region of brain in consideration. In the hippocampus, place fields are smallest and sharpest at the dorsal pole, becoming larger toward the ventral pole.[10] This may reflect the topography of projections to the hippocampus. For example, the ventral hippocampus receives much more input from the amygdala, while dorsal hippocampus is more preferentially innervated by entorhinal cortex.

Spatial modulated cells are also found in the entorhinal cortex, which feed input from neocortex into the hippocampus. Neurons in the lateral entorhinal cortex exhibit little spatial selectivity,[11] while neurons of the medial entorhinal (MEA) cortex exhibit multiple "place fields" that are arranged in an hexagonal pattern, and are therefore called "grid cells". These fields and spacing between fields increase from the dorso-lateral MEA to the ventro-medial MEA.[12][13]

Phase precession

The hippocampus is one of many brain structures that can show a characteristic 4–12 Hz oscillation, theta rhythm, in an EEG recording. The oscillation has been observed in all mammalian species tested. In both rats and humans, it is associated with real or virtual movement through space.

When a neuron discharges, it can be said to fire in relation to the current phase of a theta cycle (0-360 degrees). When a rat enters a cell's place field, the cell will initially discharge when perisomatic inhibition is weakest. For theta recorded in the CA1 pyramidal cell layer, this approximately corresponds with the peak of the oscillation. On each following cycle as the rat progresses through the field, the cell will discharge at earlier and earlier phases,[14] typically stopping just before the trough of the cycle (as recorded in CA1 stratum pyramidale). In other words, the place cell produces a rhythmic discharge of a slightly higher frequency than the ongoing theta oscillation.

Because place fields of different cells overlap, at any particular time the rat will be at different distances in different fields, so each place cell will fire at a different phase of theta, allowing the rat's position to be determined with good precision. This potentially provides an alternative temporal code for location. Phase precession also results in the compression of temporal sequences of place cell firing — a phenomenon believed to facilitate synaptic plasticity.[1] There is evidence that phase precession is related to depolarisation of the neuron, such that the firing rate and firing phase of the cell are tightly coupled,[15][16] However, phase precession can also be robustly independent of firing rate in freely moving animals.[17] This caveat of phase precession, which alludes to the potential neural mechanisms underlying it, requires further investigation before arriving at a definitive answer.

References

  1. ^ a b Skaggs WE, McNaughton BL (March 1996). "Replay of neuronal firing sequences in rat hippocampus during sleep following spatial experience". Science 271 (5257): 1870–3. Bibcode 1996Sci...271.1870S. doi:10.1126/science.271.5257.1870. PMID 8596957. http://www.sciencemag.org/cgi/pmidlookup?view=long&pmid=8596957. 
  2. ^ Moser, E.; Kropff, E.; Moser, M. (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. ISSN 0147-006X. PMID 18284371.  edit
  3. ^ O'Keefe J, Dostrovsky J (November 1971). "The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat". Brain Res. 34 (1): 171–5. doi:10.1016/0006-8993(71)90358-1. PMID 5124915. http://linkinghub.elsevier.com/retrieve/pii/0006-8993(71)90358-1. 
  4. ^ O'Keefe, John, Nadel, Lynn (1978). The Hippocampus as a Cognitive Map. Oxford University Press. ISBN 0-19-857206-9. http://www.cognitivemap.net. 
  5. ^ Ekstrom AD, Kahana MJ, Caplan JB, et al. (September 2003). "Cellular networks underlying human spatial navigation". Nature 425 (6954): 184–8. doi:10.1038/nature01964. PMID 12968182. 
  6. ^ Markus EJ, Qin YL, Leonard B, Skaggs WE, McNaughton BL, Barnes CA (November 1995). "Interactions between location and task affect the spatial and directional firing of hippocampal neurons". J. Neurosci. 15 (11): 7079–94. PMID 7472463. http://www.jneurosci.org/cgi/pmidlookup?view=long&pmid=7472463. 
  7. ^ Wilson MA, McNaughton BL (August 1993). "Dynamics of the hippocampal ensemble code for space". Science 261 (5124): 1055–8. Bibcode 1993Sci...261.1055W. doi:10.1126/science.8351520. PMID 8351520. http://www.sciencemag.org/cgi/pmidlookup?view=long&pmid=8351520. 
  8. ^ Guzowski JF, Knierim JJ, Moser EI (November 2004). "Ensemble dynamics of hippocampal regions CA3 and CA1". Neuron 44 (4): 581–4. doi:10.1016/j.neuron.2004.11.003. PMID 15541306. http://linkinghub.elsevier.com/retrieve/pii/S0896627304007172. 
  9. ^ Knierim JJ, Kudrimoti HS, McNaughton BL (March 1995). "Place cells, head direction cells, and the learning of landmark stability". J. Neurosci. 15 (3 Pt 1): 1648–59. PMID 7891125. http://www.jneurosci.org/cgi/pmidlookup?view=long&pmid=7891125. 
  10. ^ Jung MW, Wiener SI, McNaughton BL (December 1994). "Comparison of spatial firing characteristics of units in dorsal and ventral hippocampus of the rat". J. Neurosci. 14 (12): 7347–56. PMID 7996180. http://www.jneurosci.org/cgi/pmidlookup?view=long&pmid=7996180. 
  11. ^ Hargreaves EL, Rao G, Lee I, Knierim JJ (June 2005). "Major dissociation between medial and lateral entorhinal input to dorsal hippocampus". Science 308 (5729): 1792–4. Bibcode 2005Sci...308.1792H. doi:10.1126/science.1110449. PMID 15961670. http://www.sciencemag.org/cgi/pmidlookup?view=long&pmid=15961670. 
  12. ^ Fyhn M, Molden S, Witter MP, Moser EI, Moser MB (August 2004). "Spatial representation in the entorhinal cortex". Science 305 (5688): 1258–64. Bibcode 2004Sci...305.1258F. doi:10.1126/science.1099901. PMID 15333832. http://www.sciencemag.org/cgi/pmidlookup?view=long&pmid=15333832. 
  13. ^ Hafting T, Fyhn M, Molden S, Moser MB, Moser EI (August 2005). "Microstructure of a spatial map in the entorhinal cortex". Nature 436 (7052): 801–6. Bibcode 2005Natur.436..801H. doi:10.1038/nature03721. PMID 15965463. 
  14. ^ 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. 
  15. ^ Harris KD, Henze DA, Hirase H, et al. (June 2002). "Spike train dynamics predicts theta-related phase precession in hippocampal pyramidal cells". Nature 417 (6890): 738–41. doi:10.1038/nature00808. PMID 12066184. 
  16. ^ Mehta MR, Lee AK, Wilson MA (June 2002). "Role of experience and oscillations in transforming a rate code into a temporal code". Nature 417 (6890): 741–6. doi:10.1038/nature00807. PMID 12066185. 
  17. ^ Huxter J, Burgess N, O'Keefe J (October 2003). "Independent rate and temporal coding in hippocampal pyramidal cells". Nature 425 (6960): 828–32. doi:10.1038/nature02058. PMC 2677642. PMID 14574410. http://www.pubmedcentral.nih.gov/articlerender.fcgi?tool=pmcentrez&artid=2677642. 

External links