Medial entorhinal grid cells and head direction cells rotate with a T-maze more often during less recently experienced rotations

Cerebral Cortex

Volumn 24, Issue 6, 2014, Pages 1630-1644

  Gupta, Kishan ^a   Beer, Nathan J ^a   Keller, Lauren A ^a   Hasselmo, Michael E ^a  

^a BOSTON UNIVERSITY   (United States)

Author keywords

Entorhinal cortex; Experience; Fragmentation; Grid cells; Head direction cells

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; ASSOCIATION; BRAIN CELL; CELL SELECTION; CELL TYPE; CONTROLLED STUDY; ENTORHINAL CORTEX; GRID CELL; HEAD MOVEMENT; LEARNING; MALE; MEDIAL ENTORHINAL CORTEX; NERVE CELL; NONHUMAN; OPEN FIELD TEST; PRIORITY JOURNAL; RAT; RECORDING; SPATIAL ANALYSIS; T-MAZE TEST; TASK PERFORMANCE; TUNING CURVE; ACTION POTENTIAL; ANIMAL; DEPTH PERCEPTION; ELECTRODE IMPLANT; ENVIRONMENT; EXPLORATORY BEHAVIOR; HEAD; LONG EVANS RAT; MAZE TEST; ORIENTATION; PHYSIOLOGY; ROTATION; TIME;

ACTION POTENTIALS; ANIMALS; CUES; ELECTRODES, IMPLANTED; ENTORHINAL CORTEX; ENVIRONMENT; EXPLORATORY BEHAVIOR; HEAD; MALE; MAZE LEARNING; NEURONS; ORIENTATION; RATS, LONG-EVANS; ROTATION; SPACE PERCEPTION; TIME FACTORS;

EID: 84899142446     PISSN: 10473211     EISSN: 14602199     Source Type: Journal    
DOI: 10.1093/cercor/bht020     Document Type: Article

References (56)

1. Barry C, Ginzberg LL, O'Keefe J, Burgess N. 2012. Grid cell firing patterns signal environmental novelty by expansion. Proc Natl Acad Sci USA. 109:17687-92.
2. Barry C, Hayman R, Burgess N, Jeffery KJ. 2007. Experience-dependent rescaling of entorhinal grids. Nat Neurosci. 10:682-684.
3. Berens P. 2009. CircStat: a MATLAB toolbox for circular statistics. J Stat Softw. 31:1-21.
4. Brandon MP, Bogaard AR, Andrews CM, Hasselmo ME. 2012. Head direction cells in the postsubiculum do not show replay of prior waking sequences during sleep. Hippocampus. 22:604-618.
5. Brandon MP, Bogaard AR, Libby CP, Connerney MA, Gupta K, Hassel-mo ME. 2011. Reduction of theta rhythm dissociates grid cell spatial periodicity from directional tuning. Science. 332:595-599.
6. Brown JE, Skaggs WE. 2002. Concordant and discordant coding of spatial location in populations of hippocampal CA1 pyramidal cells. J Neurophysiol. 88:1605-1613.
7. Burgess N, O'Keefe J. 2011. Models of place and grid cell firing and theta rhythmicity. Curr Opin Neurobiol. 21:734-744.
8. Cheung A, Sturzl W, Zeil J, Cheng K. 2008. The information content of panoramic images II: view-based navigation in nonrectangular experimental arenas. J Exp Psychol Anim Behav Process. 34:15-30.
9. Clark BJ, Harris MJ, Taube JS. 2012. Control of anterodorsal thalamic head direction cells by environmental boundaries: comparison with conflicting distal landmarks. Hippocampus. 22:172-187.
10. Clark BJ, Taube JS. 2011. Intact landmark control and angular path integration by head direction cells in the anterodorsal thalamus after lesions of the medial entorhinal cortex. Hippocampus. 21:767-782.
11. Derdikman D, Whitlock JR, Tsao A, Fyhn M, Hafting T, Moser MB, Moser EI. 2009. Fragmentation of grid cell maps in a multicom-partment environment. Nat Neurosci. 12:1325-1332.
12. Dudchenko PA, Davidson M. 2002. Rats use a sense of direction to alternate on T-mazes located in adjacent rooms. Anim Cogn. 5:115-118.
13. Dudchenko PA, Zinyuk LE. 2005. The formation of cognitive maps of adjacent environments: evidence from the head direction cell system. Behav Neurosci. 119:1511-1523.
14. Fenton AA, Lytton WW, Barry JM, Lenck-Santini PP, Zinyuk LE, Kubik S, Bures J, Poucet B, Muller RU, Olypher AV. 2010. Attention-like modulation of hippocampus place cell discharge. J Neurosci. 30:4613-4625.
15. Fyhn M, Molden S, Witter MP, Moser EI, Moser MB. 2004. Spatial representation in the entorhinal cortex. Science. 305:1258-1264.
16. Golob EJ, Taube JS. 1997. Head direction cells and episodic spatial information in rats without a hippocampus. Proc Natl Acad Sci USA. 94:7645-7650.
17. Goodridge JP, Taube JS. 1997. Interaction between the postsubiculum and anterior thalamus in the generation of head direction cell activity. J Neurosci. 17:9315-9330.
18. Gothard KM, Skaggs WE, McNaughton BL. 1996. Dynamics of mismatch correction in the hippocampal ensemble code for space: interaction between path integration and environmental cues. J Neurosci. 16:8027-8040.
19. Gothard KM, Skaggs WE, Moore KM, McNaughton BL. 1996. Binding of hippocampal CA1 neural activity to multiple reference frames in a landmark-based navigation task. J Neurosci. 16:823-835.
20. Graham M, Good MA, McGregor A, Pearce JM. 2006. Spatial learning based on the shape of the environment is influenced by properties of the objects forming the shape. J Exp Psychol Anim Behav Process. 32:44-59.
21. Gupta K, Keller LA, Hasselmo ME. 2012. Reduced spiking in entorh-inal cortex during the delay period of a cued spatial response task. Learn Mem. 19:219-230.
22. Hafting T, Fyhn M, Molden S, Moser MB, Moser EI. 2005. Microstruc-ture of a spatial map in the entorhinal cortex. Nature. 436:801-806.
23. Hargreaves EL, Yoganarasimha D, Knierim JJ. 2007. Cohesiveness of spatial and directional representations recorded from neural ensembles in the anterior thalamus, parasubiculum, medial entorh-inal cortex, and hippocampus. Hippocampus. 17:826-841.
24. Huang Y, Brandon MP, Griffin AL, Hasselmo ME, Eden UT. 2009. Decoding movement trajectories through a T-maze using point process filters applied to place field data from rat hippocampal region CA1. Neural Comput. 21:3305-3334.
25. Knierim JJ. 2002. Dynamic interactions between local surface cues, distal landmarks, and intrinsic circuitry in hippocampal place cells. J Neurosci. 22:6254-6264.
26. Knierim JJ, Hamilton DA. 2011. Framing spatial cognition: neural representations of proximal and distal frames of reference and their roles in navigation. Physiol Rev. 91:1245-1279.
27. Knierim JJ, Kudrimoti HS, McNaughton BL. 1995. Place cells, head direction cells, and the learning of landmark stability. J Neurosci. 15:1648-1659.
28. Knight R, Hayman R, Lin Ginzberg L, Jeffery K. 2011. Geometric cues influence head direction cells only weakly in nondisoriented rats. J Neurosci. 31:15681-15692.
29. Koenig J, Linder AN, Leutgeb JK, Leutgeb S. 2011. The spatial periodicity of grid cells is not sustained during reduced theta oscillations. Science. 332:592-595.
30. Komorowski RW, Manns JR, Eichenbaum H. 2009. Robust conjunctive item-place coding by hippocampal neurons parallels learning what happens where. J Neurosci. 29:9918-9929.
31. Langston RF, Ainge JA, Couey JJ, Canto CB, Bjerknes TL, Witter MP, Moser EI, Moser MB. 2010. Development of the spatial representation system in the rat. Science. 328:1576-1580.
32. Lee I, Yoganarasimha D, Rao G, Knierim JJ. 2004. Comparison of population coherence of place cells in hippocampal subfields CA1 and CA3. Nature. 430:456-459.
33. Lever C, Burton S, Jeewajee A, O'Keefe J, Burgess N. 2009. Boundary vector cells in the subiculum of the hippocampal formation. J Neurosci. 29:9771-9777.
34. Lipton PA, White JA, Eichenbaum H. 2007. Disambiguation of overlapping experiences by neurons in the medial entorhinal cortex. J Neurosci. 27:5787-5795.
35. McNaughton BL, Barnes CA, Gerrard JL, Gothard K, Jung MW, Knierim JJ, Kudrimoti H, Qin Y, Skaggs WE, Suster M et al. 1996. Deciphering the hippocampal polyglot: the hippocampus as a path integration system. J Exp Biol. 199:173-185.
36. Nitz D. 2009. Parietal cortex, navigation, and the construction of arbitrary reference frames for spatial information. Neurobiol Learn Mem. 91:179-185.
37. O'Keefe J, Dostrovsky J. 1971. The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat. Brain Res. 34:171-175.
38. Renaudineau S, Poucet B, Save E. 2007. Flexible use of proximal objects and distal cues by hippocampal place cells. Hippocampus. 17:381-395.
39. Sargolini F, Fyhn M, Hafting T, McNaughton BL, Witter MP, Moser MB, Moser EI. 2006. Conjunctive representation of position, direction, and velocity in entorhinal cortex. Science. 312:758-762.
40. Schmitzer-Torbert N, Jackson J, Henze D, Harris K, Redish AD. 2005. Quantitative measures of cluster quality for use in extracellular recordings. Neuroscience. 131:1-11.
41. Shapiro ML, Tanila H, Eichenbaum H. 1997. Cues that hippocampal place cells encode: dynamic and hierarchical representation of local and distal stimuli. Hippocampus. 7:624-642.
42. Skaggs WE, McNaughton BL. 1998. Spatial firing properties of hippo-campal CA1 populations in an environment containing two visually identical regions. J Neurosci. 18:8455-8466.
43. Solstad T, Boccara CN, Kropff E, Moser MB, Moser EI. 2008. Representation of geometric borders in the entorhinal cortex. Science. 322:1865-1868.
44. Stackman RW, Golob EJ, Bassett JP, Taube JS. 2003. Passive transport disrupts directional path integration by rat head direction cells. J Neurophysiol. 90:2862-2874.
45. Sturzl W, Cheung A, Cheng K, Zeil J. 2008. The information content of panoramic images I: the rotational errors and the similarity of views in rectangular experimental arenas. J Exp Psychol Anim Behav Process. 34:1-14.
46. Taube JS, Burton HL. 1995. Head direction cell activity monitored in a novel environment and during a cue conflict situation. J Neuro-physiol. 74:1953-1971.
47. Taube JS, Muller RU, Ranck JB Jr. 1990a. Head-direction cells recorded from the postsubiculum in freely moving rats. I. Description and quantitative analysis. J Neurosci. 10: 420-435.
48. Taube JS, Muller RU, Ranck JB Jr. 1990b. Head-direction cells recorded from the postsubiculum in freely moving rats. II. Effects of environmental manipulations. J Neurosci. 10:436-447.
49. Touretzky DS, Redish AD. 1996. Theory of rodent navigation based on interacting representations of space. Hippocampus. 6:247-270.
50. Whitlock JR, Derdikman D. 2012. Head direction maps remain stable despite grid map fragmentation. Front Neural Circuits. 6:9.
51. Wills TJ, Cacucci F, Burgess N, O'Keefe J. 2010. Development of the hippocampal cognitive map in preweanling rats. Science. 328:1573-1576.
52. Wood ER, Dudchenko PA, Robitsek RJ, Eichenbaum H. 2000. Hippo-campal neurons encode information about different types of memory episodes occurring in the same location. Neuron. 27:623-633.
53. Yoganarasimha D, Yu X, Knierim JJ. 2006. Head direction cell representations maintain internal coherence during conflicting proximal and distal cue rotations: comparison with hippocampal place cells. J Neurosci. 26:622-631.
54. Young BJ, Fox GD, Eichenbaum H. 1994. Correlates of hippocampal complex-spike cell activity in rats performing a nonspatial radial maze task. J Neurosci. 14:6553-6563.
55. Zugaro MB, Arleo A, Dejean C, Burguiere E, Khamassi M, Wiener SI. 2004. Rat anterodorsal thalamic head direction neurons depend upon dynamic visual signals to select anchoring landmark cues. Eur J Neurosci. 20:530-536.
56. Zugaro MB, Berthoz A, Wiener SI. 2001. Background, but not foreground, spatial cues are taken as references for head direction responses by rat anterodorsal thalamus neurons. J Neurosci. 21: RC154.