Coherence between Rat Sensorimotor System and Hippocampus Is Enhanced during Tactile Discrimination

PLoS Biology

Volumn 14, Issue 2, 2016, Pages

  Grion, Natalia ^a   Akrami, Athena ^a,b,c   Zuo, Yangfang ^a,d   Stella, Federico ^a,e   Diamond, Mathew E ^a  

^a SISSA   (Italy)

^b PRINCETON UNIVERSITY   (United States)

^c HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^d INSTITUTE OF GEOLOGY AND GEOPHYSICS   (China)

^e INSTITUTE OF SCIENCE AND TECHNOLOGY AUSTRIA   (Austria)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; BRAIN REGION; CONSENSUS DEVELOPMENT; CONTROLLED STUDY; DECISION MAKING; ELECTRIC POTENTIAL; HIPPOCAMPUS; MAMMAL; MEMORY; NERVE CELL; NONHUMAN; OSCILLATION; PALPATION; RAT; RHYTHM; SOMATOSENSORY CORTEX; STIMULUS; TACTILE DISCRIMINATION; VIBRISSA; ANIMAL; HIPPOCAMPAL CA1 REGION; MALE; PHYSIOLOGY; THETA RHYTHM; TOUCH; WISTAR RAT;

ANIMALS; CA1 REGION, HIPPOCAMPAL; MALE; RATS, WISTAR; SOMATOSENSORY CORTEX; THETA RHYTHM; TOUCH PERCEPTION; VIBRISSAE;

EID: 84959464617     PISSN: 15449173     EISSN: 15457885     Source Type: Journal    
DOI: 10.1371/journal.pbio.1002384     Document Type: Article

References (73)

1. Tiesinga P, Fellous J-M, Sejnowski TJ, Regulation of spike timing in visual cortical circuits. Nat Rev Neurosci. 2008;9(2):97–107. doi: 10.1038/nrn231518200026
2. Burchell TR, Faulkner HJ, Whittington MA, Gamma frequency oscillations gate temporally coded afferent inputs in the rat hippocampal slice. Neuroscience letters. 1998;255(3):151–4. 9832195
3. Tiesinga PHE, Sejnowski TJ, Rapid temporal modulation of synchrony by competition in cortical interneuron networks. Neural computation. 2004;16(2):251–75. 15006096
4. Wang XJ, Neurophysiological and computational principles of cortical rhythms in cognition. Physiol Rev. 2010;90(3):1195–268. doi: 10.1152/physrev.00035.200820664082
5. Buzsáki G, Draguhn A, Neuronal Oscillations in Cortical Networks. Science. 2004;304(5679):1926–9. 15218136
6. Jones MW, Wilson MA, Theta Rhythms Coordinate Hippocampal–Prefrontal Interactions in a Spatial Memory Task. PLoS Biol. 2005;3(12).
7. Tabuchi Et, Mulder Ab, Wiener Si, Position and behavioral modulation of synchronization of hippocampal and accumbens neuronal discharges in freely moving rats. Hippocampus. 2000;10(6):717–28. 11153717
8. Tort ABL, Kramer MA, Thorn C, Gibson DJ, Kubota Y, Graybiel AM, et al. Dynamic cross-frequency couplings of local field potential oscillations in rat striatum and hippocampus during performance of a T-maze task. Proceedings of the National Academy of Sciences. 2008;105(51):20517–22.
9. DeCoteau WE, Thorn C, Gibson DJ, Courtemanche R, Mitra P, Kubota Y, et al. Oscillations of Local Field Potentials in the Rat Dorsal Striatum During Spontaneous and Instructed Behaviors. Journal of Neurophysiology. 2007;97(5):3800–5. 17329629
10. Terada S, Takahashi S, Sakurai Y, Oscillatory interaction between amygdala and hippocampus coordinates behavioral modulation based on reward expectation. Frontiers in Behavioral Neuroscience. 2013;7:177. doi: 10.3389/fnbeh.2013.0017724348352
11. Hasselmo ME, What is the function of hippocampal theta rhythm?—Linking behavioral data to phasic properties of field potential and unit recording data. Hippocampus. 2005;15(7):936–49. 16158423
12. Vertes RP, Hippocampal theta rhythm: A tag for short-term memory. Hippocampus. 2005;15(7):923–35. 16149083
13. Siegle JH, Wilson MA, Enhancement of encoding and retrieval functions through theta phase-specific manipulation of hippocampus. eLife. 2014;3.
14. Benchenane K, Peyrache A, Khamassi M, Tierney PL, Gioanni Y, Battaglia FP, et al. Coherent Theta Oscillations and Reorganization of Spike Timing in the Hippocampal- Prefrontal Network upon Learning. Neuron. 2010;66(6):921–36. doi: 10.1016/j.neuron.2010.05.01320620877
15. Diamond ME, Arabzadeh E, Whisker sensory system—From receptor to decision. Progress in Neurobiology. 2013;103(0):28–40.
16. Prescott TJ, Diamond ME, Wing AM, Active touch sensing. Philosophical Transactions of the Royal Society B: Biological Sciences. 2011;366(1581):2989–95.
17. Diamond ME, von Heimendahl M, Arabzadeh E, Whisker-Mediated Texture Discrimination. PLoS Biol. 2008;6(8):e220. doi: 10.1371/journal.pbio.006022018752356
18. Gray JA, Medial septal lesions, hippocampal theta rhythm and the control of vibrissal movement in the freely moving rat. Electroencephalography and Clinical Neurophysiology. 1971;30(3):189–97. 4103140
19. Semba K, Komisaruk BR, Neural substrates of two different rhythmical vibrissal movements in the rat. Neuroscience. 1984;12(3):761–74. 6472619
20. Komisaruk BR, Synchrony between limbic system theta activity and rhythmical behavior in rats. Journal of Comparative and Physiological Psychology. 1970;70(3, Pt.1):482–92.
21. Berg RW, Whitmer D, Kleinfeld D, Exploratory Whisking by Rat Is Not Phase Locked to the Hippocampal Theta Rhythm. The Journal of Neuroscience. 2006;26(24):6518–22. 16775139
22. Burwell RD, Amaral DG, Cortical afferents of the perirhinal, postrhinal, and entorhinal cortices of the rat. The Journal of comparative neurology. 1998;398(2):179–205. 9700566
23. Itskov PM, Vinnik E, Diamond ME, Hippocampal Representation of Touch-Guided Behavior in Rats: Persistent and Independent Traces of Stimulus and Reward Location. PLoS ONE. 2011;6(1): e16462. doi: 10.1371/journal.pone.001646221305039
24. Perkon I, Košir A, Itskov PM, Tasič J, Diamond ME, Unsupervised quantification of whisking and head movement in freely moving rodents. Journal of Neurophysiology. 2011;105(4):1950–62. doi: 10.1152/jn.00764.201021307326
25. Rivas J, Gaztelu JM, García-Austt E, Changes in hippocampal cell discharge patterns and theta rhythm spectral properties as a function of walking velocity in the guinea pig. Exp Brain Res. 1996;108(1):113–8. 8721159
26. Sławińska U, Kasicki S, The frequency of rat's hippocampal theta rhythm is related to the speed of locomotion. Brain Res. 1998;796(1–2):327–31. 9689489
27. Kleinfeld D, Deschenes M, Wang F, Moore JD, More than a rhythm of life: breathing as a binder of orofacial sensation. Nat Neurosci. 2014;17(5):647–51. doi: 10.1038/nn.369324762718
28. Fee MS, Mitra PP, Kleinfeld D, Central Versus Peripheral Determinants of Patterned Spike Activity in Rat Vibrissa Cortex During Whisking. Journal of Neurophysiology. 1997;78(2):1144–9. 9307141
29. Curtis JC, Kleinfeld D, Phase-to-rate transformations encode touch in cortical neurons of a scanning sensorimotor system. Nat Neurosci. 2009;12(4):492–501. doi: 10.1038/nn.228319270688
30. Quian Quiroga R, Panzeri S, Extracting information from neuronal populations: information theory and decoding approaches. Nat Rev Neurosci. 2009;10(3):173–85. doi: 10.1038/nrn257819229240
31. Hill Daniel N, Curtis John C, Moore Jeffrey D, Kleinfeld D, Primary Motor Cortex Reports Efferent Control of Vibrissa Motion on Multiple Timescales. Neuron. 2011;72(2):344–56. doi: 10.1016/j.neuron.2011.09.02022017992
32. Jadhav SP, Feldman DE, Texture coding in the whisker system. Curr Opin Neurobiol. 2010;20(3):313–8. doi: 10.1016/j.conb.2010.02.01420299205
33. Macrides F, Temporal relationships between hippocampal slow waves and exploratory sniffing in hamsters. Behav Biol. 1975;14(3):295–308. 1137549
34. Williams JM, Givens B, Stimulation-induced reset of hippocampal theta in the freely performing rat. Hippocampus. 2003;13(1):109–16. 12625462
35. von Heimendahl M, Itskov PM, Arabzadeh E, Diamond ME, Neuronal Activity in Rat Barrel Cortex Underlying Texture Discrimination. PLoS Biol. 2007;5(11).
36. Zuo Y, Perkon I, Diamond ME, Whisking and whisker kinematics during a texture classification task. Philosophical Transactions of the Royal Society B: Biological Sciences. 2011;366(1581):3058–69.
37. Zuo Y, Safaai H, Notaro G, Mazzoni A, Panzeri S, Diamond Mathew E, Complementary Contributions of Spike Timing and Spike Rate to Perceptual Decisions in Rat S1 and S2 Cortex. Current Biology. 2015;25(3):357–63. doi: 10.1016/j.cub.2014.11.06525619766
38. Macrides F, Eichenbaum HB, Forbes WB, Temporal relationship between sniffing and the limbic theta rhythm during odor discrimination reversal learning. The Journal of Neuroscience. 1982;2(12):1705–17. 7143047
39. Jeewajee A, Lever C, Burton S, O'Keefe J, Burgess N, Environmental novelty is signaled by reduction of the hippocampal theta frequency. Hippocampus. 2008;18(4):340–8. 18081172
40. McFarland WL, Teitelbaum H, Hedges EK, Relationship between hippocampal theta activity and running speed in the rat. Journal of comparative and physiological psychology. 1975;88(1):324. 1120805
41. Givens B, Stimulus-evoked resetting of the dentate theta rhythm: relation to working memory. Neuroreport. 1996;8(1):159–63. 9051772
42. McCartney H, Johnson AD, Weil ZM, Givens B, Theta reset produces optimal conditions for long-term potentiation. Hippocampus. 2004;14(6):684–7. 15318327
43. Rajkai C, Lakatos P, Chen CM, Pincze Z, Karmos G, Schroeder CE, Transient cortical excitation at the onset of visual fixation. Cereb Cortex. 2008;18(1):200–9. 17494059
44. Hyman JM, Wyble BP, Goyal V, Rossi CA, Hasselmo ME, Stimulation in hippocampal region CA1 in behaving rats yields long-term potentiation when delivered to the peak of theta and long-term depression when delivered to the trough. J Neurosci. 2003;23(37):11725–31. 14684874
45. Colgin LL, Denninger T, Fyhn M, Hafting T, Bonnevie T, Jensen O, et al. Frequency of gamma oscillations routes flow of information in the hippocampus. Nature. 2009;462(7271):353–7. doi: 10.1038/nature0857319924214
46. Manns JR, Zilli EA, Ong KC, Hasselmo ME, Eichenbaum H, Hippocampal CA1 spiking during encoding and retrieval: relation to theta phase. Neurobiol Learn Mem. 2007;87(1):9–20. 16839788
47. Kleinfeld D, Deschênes M, Neuronal Basis for Object Location in the Vibrissa Scanning Sensorimotor System. Neuron. 2011;72(3):455–68. doi: 10.1016/j.neuron.2011.10.00922078505
48. Buzsáki G, Theta Oscillations in the Hippocampus. Neuron. 2002;33(3):325–40. 11832222
49. Fries P, A mechanism for cognitive dynamics: neuronal communication through neuronal coherence. Trends in Cognitive Sciences. 2005;9(10):474–80. 16150631
50. Womelsdorf T, Schoffelen JM, Oostenveld R, Singer W, Desimone R, Engel AK, et al. Modulation of Neuronal Interactions Through Neuronal Synchronization. Science. 2007;316(5831):1609–12. 17569862
51. Sirota A, Montgomery S, Fujisawa S, Isomura Y, Zugaro M, Buzsáki G, Entrainment of Neocortical Neurons and Gamma Oscillations by the Hippocampal Theta Rhythm. Neuron. 2008;60(4):683–97. doi: 10.1016/j.neuron.2008.09.01419038224
52. Fell J, Klaver P, Lehnertz K, Grunwald T, Schaller C, Elger CE, et al. Human memory formation is accompanied by rhinal–hippocampal coupling and decoupling. Nature Neuroscience. 2001;4(12):1259–64. 11694886
53. Gray CM, König P, Engel AK, Singer W, Oscillatory responses in cat visual cortex exhibit inter-columnar synchronization which reflects global stimulus properties. Nature. 1989;338(6213):334–7. 2922061
54. Womelsdorf T, Vinck M, Leung LS, Everling S, Selective theta-synchronization of choice-relevant information subserves goal-directed behavior. Front Hum Neurosci. 2010;4:210. doi: 10.3389/fnhum.2010.0021021119780
55. Kay LM, Theta oscillations and sensorimotor performance. Proceedings of the National Academy of Sciences of the United States of America. 2005;102(10):3863–8. 15738424
56. Prescott TJ, Mitchinson B, Grant RA, Vibrissal behavior and function. Scholarpedia. 2011;6(10):6642.
57. Ledberg A, Robbe D, Locomotion-Related Oscillatory Body Movements at 6–12 Hz Modulate the Hippocampal Theta Rhythm. PLoS ONE. 2011;6(11):e27575. doi: 10.1371/journal.pone.002757522102910
58. Moore JD, Deschênes M, Furuta T, Huber D, Smear MC, Demers M, et al. Hierarchy of orofacial rhythms revealed through whisking and breathing. Nature. 2013;497(7448):205–10. doi: 10.1038/nature1207623624373
59. Diamond ME, von Heimendahl M, Knutsen PM, Kleinfeld D, Ahissar E, 'Where' and 'what' in the whisker sensorimotor system. Nature Reviews Neuroscience. 2008;9(8):601–12. doi: 10.1038/nrn241118641667
60. Kleinfeld D, Berg RW, O'Connor SM, Invited Review Anatomical loops and their electrical dynamics in relation to whisking by rat. Somatosensory & Motor Research. 1999;16(2):69–88.
61. Bland BH, Oddie SD, Anatomical, Electrophysiological and Pharmacological Studies of Ascending Brainstem Hippocampal Synchronizing Pathways. Neuroscience & Biobehavioral Reviews. 1998;22(2):259–73.
62. Shammah-Lagnado SJ, Negrao N, Silva BA, Ricardo JA, Afferent connections of the nuclei reticularis pontis oralis and caudalis: a horseradish peroxidase study in the rat. Neuroscience. 1987;20(3):961–89. 2439943
63. Semba K, Fibiger HC, Afferent connections of the laterodorsal and the pedunculopontine tegmental nuclei in the rat: a retro- and antero-grade transport and immunohistochemical study. J Comp Neurol. 1992;323(3):387–410. 1281170
64. Paxinos G, Watson C, The rat brain in stereotaxic coordinates. 5th ed.Amsterdam; Boston: Elsevier Academic Press; 2005. xliii, 166 p. p.
65. Redish A, Schmitzer-Torbert N. MClust Spike Sorting Toolbox, version 3.0. http://redishlab.neuroscience.umn.edu/MClust/MClust.html
66. Harris KD. KlustaKwik.Automatic Cluster Analysis, version 2.0. http://sourceforge.net/projects/klustakwik
67. Oostenveld R, Fries P, Maris E, Schoffelen JM, FieldTrip: Open source software for advanced analysis of MEG, EEG, and invasive electrophysiological data. Computational intelligence and neuroscience. 2011;2011:156869. doi: 10.1155/2011/15686921253357
68. Percival DB, Walden AT, Press CU, Spectral analysis for physical applications: multitaper and conventional univariate techniques. United Kingdom1993.
69. Quian Quiroga R, Kraskov A, Kreuz T, Grassberger P, Performance of different synchronization measures in real data: A case study on electroencephalographic signals. Physical Review E. 2002;65(4):041903.
70. Rosenblum MG, Pikovsky AS, Kurths J, Phase Synchronization of Chaotic Oscillators. Physical Review Letters. 1996;76(11):1804–7. 10060525
71. Pikovsky A, Rosenblum M, Kurths J, Synchronization: A Universal Concept in Nonlinear Sciences (Cambridge Nonlinear Science Series). 2003.
72. Mardia KV, Jupp PE, Directional Statistics. John Wiley and Sons Ltd, 2000, pp 94–98
73. Berens P, CircStat: a MATLAB toolbox for circular statistics. J Stat Softw. 2009;31(10):1–21.