A prefrontal-thalamo-hippocampal circuit for goal-directed spatial navigation

Nature

Volumn 522, Issue 7554, 2015, Pages 50-55

  Ito, Hiroshi T ^a   Zhang, Sheng Jia ^a   Witter, Menno P ^a   Moser, Edvard I ^a   Moser, May Britt ^a  

^a NORWEGIAN UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Norway)

Author keywords

[No Author keywords available]

Indexed keywords

BRAIN; LESION; NEUROLOGY; RODENT; TRAJECTORY;

ADENO ASSOCIATED VIRUS; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL ACTIVITY; CONTROLLED STUDY; DORSAL ANTERIOR CINGULATE CORTEX; ELECTROENCEPHALOGRAM; HIPPOCAMPAL CA1 REGION; HIPPOCAMPAL CA3 REGION; HIPPOCAMPUS; INFORMATION PROCESSING; MALE; MAZE TEST; MEDIAL PREFRONTAL CORTEX; NONHUMAN; OPTOGENETICS; PREFRONTAL CORTEX; PRIORITY JOURNAL; RAT; REUNIENS NUCLEUS; SPATIAL ORIENTATION; SPIKE WAVE; TASK PERFORMANCE; TASK POSITIVE NETWORK; THALAMUS; THALAMUS NUCLEUS; ACTION POTENTIAL; ANIMAL; CYTOLOGY; LONG EVANS RAT; MOTIVATION; NERVE CELL; NERVE TRACT; PHYSIOLOGY; THALAMUS MIDLINE NUCLEUS;

RATTUS;

ACTION POTENTIALS; ANIMALS; CA1 REGION, HIPPOCAMPAL; CA3 REGION, HIPPOCAMPAL; GOALS; MALE; MAZE LEARNING; MIDLINE THALAMIC NUCLEI; NEURAL PATHWAYS; NEURONS; OPTOGENETICS; PREFRONTAL CORTEX; RATS; RATS, LONG-EVANS; SPATIAL NAVIGATION; THALAMUS;

EID: 84930632582     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature14396     Document Type: Article

References (52)

1. O'Keefe, J. & Nadel, L. The Hippocampus as a Cognitive Map (Oxford Univ. Press, 1978).
2. Moser, E. I., Kropff, E. & Moser, M. B. Place cells, grid cells, and the brain's spatial representation system. Annu. Rev. Neurosci. 31, 69-89 (2008).
3. Burgess, J., Recce, M. & O'Keefe, J. A model of hippocampal function. Neural Netw. 7, 1065-1081 (1994).
4. Redish, A. D. Beyond the Cognitive Map (The MIT Press, 1999).
5. Foster, D. J., Morris, R. G. & Dayan, P. A model of hippocampally dependent navigation, using the temporal difference learning rule. Hippocampus 10, 1-16 (2000).
6. Wood, E. R., Dudchenko, P. A., Robitsek, R. J. & Eichenbaum, H. Hippocampal neurons encode information about different types ofmemory episodes occurring in the same location. Neuron 27, 623-633 (2000).
7. Frank, L. M., Brown, E. N.&Wilson, M. Trajectory encoding in the hippocampus and entorhinal cortex. Neuron 27, 169-178 (2000).
8. Ferbinteanu, J. & Shapiro, M. L. Prospective and retrospective memory coding in the hippocampus. Neuron 40, 1227-1239 (2003).
9. Catanese, J., Viggiano, A., Cerasti, E., Zugaro, M. B. & Wiener, S. I. Retrospectively and prospectively modulated hippocampal place responses are differentially distributed along a common path in a continuous T-maze. J. Neurosci. 34, 13163-13169 (2014).
10. Johnson, A. & Redish, A. D. Neural ensembles in CA3 transiently encode paths forward of the animal at a decision point. J. Neurosci. 27, 12176-12189 (2007).
11. Pfeiffer, B. E. & Foster, D. J. Hippocampal placefficell sequences depict future paths to remembered goals. Nature 497, 74-79 (2013).
12. Kim, J. N. & Shadlen, M. N. Neural correlates of a decision in the dorsolateral prefrontal cortex of the macaque. Nature Neurosci. 2, 176-185 (1999).
13. Hok, V., Save, E., Lenck-Santini, P. P. & Poucet, B. Coding for spatial goals in the prelimbic/infralimbic area of the rat frontal cortex. Proc. Natl Acad. Sci. USA 102, 4602-4607 (2005).
14. Fujisawa, S., Amarasingham, A., Harrison, M. T. & Buzsaki, G. Behavior-dependent short-term assembly dynamics in the medial prefrontal cortex. Nature Neurosci. 11, 823-833 (2008).
15. Vertes, R. P., Hoover, W. B., Szigeti-Buck, K. & Leranth, C. Nucleus reuniens of the midline thalamus: link between the medial prefrontal cortex and the hippocampus. Brain Res. Bull. 71, 601-609 (2007).
16. Jones, B. F. & Witter, M. P. Cingulate cortex projections to the parahippocampal region and hippocampal formation in the rat. Hippocampus 17, 957-976 (2007).
17. Herkenham, M. The connections of the nucleus reuniens thalami: evidence for a direct thalamo-hippocampal pathway in the rat. J. Comp. Neurol. 177, 589-609 (1978).
18. Dolleman-van Der Weel, M. J.&Witter, M. P. Projections fromthe nucleus reuniens thalami to the entorhinal cortex, hippocampal field CA1, and the subiculumin the rat arise from different populations of neurons. J. Comp. Neurol. 364, 637-650 (1996).
19. Cassel, J. C. et al. The reuniens andrhomboid nuclei: neuroanatomy, electrophysiological characteristics and behavioral implications. Prog. Neurobiol. 111, 34-52 (2013).
20. Baeg, E. H. et al. Dynamics ofpopulation code for workingmemory in the prefrontal cortex. Neuron 40, 177-188 (2003).
21. Ainge, J. A., van der Meer, M. A., Langston, R. F. & Wood, E. R. Exploring the role of context-dependent hippocampal activity in spatial alternation behavior. Hippocampus 17, 988-1002 (2007).
22. Anderson, M. I. & Jeffery, K. J. Heterogeneous modulation of place cell firing by changes in context. J. Neurosci. 23, 8827-8835 (2003).
23. Leutgeb, S., Leutgeb, J. K., Treves, A., Moser, M. B. & Moser, E. I. Distinct ensemble codes in hippocampal areas CA3 and CA1. Science 305, 1295-1298 (2004).
24. Leutgeb, S. et al. Independent codes for spatial and episodic memory in hippocampal neuronal ensembles. Science 309, 619-623 (2005).
25. Wouterlood, F. G., Saldana, E. & Witter, M. P. Projection from the nucleus reuniens thalamito the hippocampal region: light and electron microscopic tracing study in the rat with the anterograde tracer Phaseolus vulgaris-leucoagglutinin. J. Comp. Neurol. 296, 179-203 (1990).
26. Sommer, M. A.&Wurtz, R. H. Influence of the thalamus on spatial visual processing in frontal cortex. Nature 444, 374-377 (2006).
27. Sherman, S. M. & Guillery, R. W. Exploring the Thalamus and its Role in Cortical Function. (MIT Press, 2006).
28. Xu, W. & Sudhof, T. C. A neural circuit for memory specificity and generalization. Science 339, 1290-1295 (2013).
29. Vertes, R. P., Linley, S. B., Groenewegen, H. J. & Witter, M. P. in The Rat Nervous System 4th edn (ed. G. Paxinos) Ch. 16 (Elsevier Academic Press, 2014).
30. Hembrook, J. R. & Mair, R. G. Lesions of reuniens and rhomboid thalamic nuclei impair radial maze win-shift performance. Hippocampus 21, 815-826 (2011).
31. Andersen, R. A. & Mountcastle, V. B. The influence of the angle of gaze upon the excitability of the light-sensitive neurons of the posterior parietal cortex. J. Neurosci. 3, 532-548 (1983).
32. Sargolini, F. et al. Conjunctive representation of position, direction, and velocity in entorhinal cortex. Science 312, 758-762 (2006).
33. Komorowski, R. W., Manns, J. R. & Eichenbaum, H. Robust conjunctive item-place coding by hippocampal neurons parallels learning what happens where. J. Neurosci. 29, 9918-9929 (2009).
34. Warden, M. R.& Miller, E. K. Task-dependent changes in short-termmemory in the prefrontal cortex. J. Neurosci. 30, 15801-15810 (2010).
35. Rigotti, M. et al. The importance of mixed selectivity in complex cognitive tasks. Nature 497, 585-590 (2013).
36. Gradinaru, V., Thompson, K. R. & Deisseroth, K. eNpHR: a Natronomonas halorhodopsin enhanced for optogenetic applications.Brain Cell Biol. 36, 129-139(2008).
37. Gradinaru, V. et al. Molecular and cellular approaches for diversifying and extending optogenetics. Cell 141, 154-165 (2010).
38. Zhang, S. J. et al. Optogenetic dissection of entorhinal-hippocampal functional connectivity. Science 340, 1232627 (2013).
39. Bower, M. R., Euston, D. R. & McNaughton, B. L. Sequential-context-dependent hippocampal activity is not necessary to learn sequences with repeated elements. J. Neurosci. 25, 1313-1323 (2005).
40. Shimazaki, H. & Shinomoto, S. Kernel bandwidth optimization in spike rate estimation. J. Comput. Neurosci. 29, 171-182 (2010).
41. Boser, B. E., Guyon, I. M. & Vapnik, V. N. A training algorithm for optimal margin classifiers. Proceedings of the fifth annualworkshop onComputational learning theory 144-152 (1992).
42. Chang, C. C. & Lin, C. J. LIBSVM: a library for support vector machines. ACMTrans. Intell. Syst. Technol. 2, 3, Article 27, (2011).
43. Skaggs, W. E., McNaughton, B. L., Wilson, M. A. & Barnes, C. A. Theta phase precession in hippocampal neuronal populations and the compression of temporal sequences. Hippocampus 6, 149-172 (1996).
44. Dolleman-Van der Weel, M. J. & Witter, M. P. Nucleus reuniens thalami innervates gamma aminobutyric acid positive cells in hippocampal field CA1 of the rat. Neurosci. Lett. 278, 145-148 (2000).
45. Euston, D. R. & McNaughton, B. L. Apparent encoding of sequential context in rat medial prefrontal cortex is accounted for by behavioral variability. J. Neurosci. 26, 13143-13155 (2006).
46. Lu, L. et al. Impaired hippocampal rate coding after lesions of the lateral entorhinal cortex. Nature Neurosci. 16, 1085-1093 (2013).
47. Hyman, J. M., Ma, L., Balaguer-Ballester, E., Durstewitz, D. & Seamans, J. K. Contextual encoding by ensembles ofmedial prefrontal cortex neurons. Proc. Natl Acad. Sci. USA 109, 5086-5091 (2012).
48. Whitlock, J. R., Pfuhl, G., Dagslott, N., Moser, M. B. & Moser, E. I. Functional split between parietal and entorhinal cortices in the rat. Neuron 73, 789-802 (2012).
49. Salinas, E. & Abbott, L. F. Coordinate transformations in the visual system: how to generate gain fields and what to compute with them. Prog. Brain Res. 130, 175-190 (2001).
50. Salinas, E.& Sejnowski, T. J. Gainmodulation in the central nervous system: where behavior,neurophysiology, andcomputationmeet.Neuroscientist 7,430-440 (2001).
51. Cohen, Y. E. & Andersen, R. A. A common reference frame for movement plans in the posterior parietal cortex. Nature Rev. Neurosci. 3, 553-562 (2002).
52. Moser, E. I. et al. Grid cells and cortical representation. Nature Rev. Neurosci. 15, 466-481 (2014).