Attention enhances the retrieval and stability of visuospatial and olfactory representations in the dorsal hippocampus

PLoS Biology

Volumn 7, Issue 6, 2009, Pages

  Muzzio, Isabel A ^a,e   Levita, Liat ^a,f   Kulkarni, Jayant ^a   Monaco, Joseph ^a   Kentros, Clifford ^b   Stead, Matthew ^c   Abbott, Larry F ^a   Kandel, Eric R ^a,d  

^a College of Physicians and Surgeons ^*  (United States)

^b UNIVERSITY OF OREGON   (United States)

^c MAYO CLINIC   (United States)

^d Och Spine at New York Presbyterian Hospitals   (United States)

^e UNIVERSITY OF PENNSYLVANIA   (United States)

^f WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL FOOD; ARTICLE; ATTENTION; AUDITORY ORIENTATION; BEHAVIORAL SCIENCE; CONTROLLED STUDY; CORTICAL SYNCHRONIZATION; DEPTH PERCEPTION; EVOKED RESPONSE; GAMMA RHYTHM; HIPPOCAMPUS; MALE; MOUSE; NONHUMAN; TASK PERFORMANCE; ACTION POTENTIAL; ANIMAL; ASSOCIATION; BEHAVIOR; BIOLOGICAL MODEL; C57BL MOUSE; CYTOLOGY; MEMORY; MOTIVATION; ODOR; OLFACTORY SYSTEM; PHYSIOLOGY; PSYCHOMOTOR PERFORMANCE; PYRAMIDAL NERVE CELL; REACTION TIME; REWARD; VISION;

ANIMALIA; MUS;

ACTION POTENTIALS; ANIMALS; ATTENTION; CUES; GOALS; HIPPOCAMPUS; MALE; MEMORY; MICE; MICE, INBRED C57BL; MODELS, NEUROLOGICAL; ODORS; OLFACTORY PATHWAYS; PSYCHOMOTOR PERFORMANCE; PYRAMIDAL CELLS; REACTION TIME; REWARD; SPATIAL BEHAVIOR; VISUAL PERCEPTION;

EID: 67649994263     PISSN: 15449173     EISSN: 15457885     Source Type: Journal    
DOI: 10.1371/journal.pbio.1000140     Document Type: Article

References (72)

1. Ferbinteanu J, Kennedy PJ, Shapiro ML (2006) Episodic memory-from brain to mind. Hippocampus 16: 691-703.
2. Smith DM, Mizumori SJ (2006) Hippocampal place cells, context, and episodic memory. Hippocampus 16: 716-729.
3. Fernandes MA, Moscovitch M, Ziegler M, Grady C (2005) Brain regions associated with successful and unsuccessful retrieval of verbal episodic memory as revealed by divided attention. Neuropsychologia 43: 1115-1127.
4. Schacter DL (1996) Illusory memories: a cognitive neuroscience analysis. Proc Natl Acad Sci U S A 93: 13527-13533.
5. Neves G, Cooke SF, Bliss TV (2008) Synaptic plasticity, memory and the hippocampus: a neural network approach to causality. Nat Rev Neurosci 9: 65-75.
6. Ferbinteanu J, Shapiro ML (2003) Prospective and retrospective memory coding in the hippocampus. Neuron 40: 1227-1239.
7. Frank LM, Brown EN, Wilson M (2000) Trajectory encoding in the hippocampus and entorhinal cortex. Neuron 27: 169-178.
8. Lee I, Griffin AL, Zilli EA, Eichenbaum H, Hasselmo ME (2006) Gradual translocation of spatial correlates of neuronal firing in the hippocampus toward prospective reward locations. Neuron 51: 639-650.
9. 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.
10. Agnihotri NT, Hawkins RD, Kandel ER, Kentros C (2004) The long-term stability of new hippocampal place fields requires new protein synthesis. Proc Natl Acad Sci U S A 101: 3656-3661.
11. Kentros C, Hargreaves E, Hawkins RD, Kandel ER, Shapiro M, et al. (1998) Abolition of long-term stability of new hippocampal place cell maps by NMDA receptor blockade. Science 280: 2121-2126.
12. Rotenberg A, Abel T, Hawkins RD, Kandel ER, Muller RU (2000) Parallel instabilities of long-term potentiation, place cells, and learning caused by decreased protein kinase A activity. J Neurosci 20: 8096-8102.
13. Rotenberg A, Mayford M, Hawkins RD, Kandel ER, Muller RU (1996) Mice expressing activated CaMKII lack low frequency LTP and do not form stable place cells in the CA1 region of the hippocampus. Cell 87: 1351-1361.
14. Thompson LT, Best PJ (1990) Long-term stability of the place-field activity of single units recorded from the dorsal hippocampus of freely behaving rats. Brain Res 509: 299-308.
15. Deadwyler SA, Bunn T, Hampson RE (1996) Hippocampal ensemble activity during spatial delayed-nonmatch-to-sample performance in rats. J Neurosci 16: 354-372.
16. Hampson RE, Simeral JD, Deadwyler SA (1999) Distribution of spatial and nonspatial information in dorsal hippocampus. Nature 402: 610-614.
17. McEchron MD, Disterhoft JF (1999) Hippocampal encoding of non-spatial trace conditioning. Hippocampus 9: 385-396.
18. Sakurai Y (1996) Hippocampal and neocortical cell assemblies encode memory processes for different types of stimuli in the rat. J Neurosci 16: 2809-2819.
19. Wiener SI, Paul CA, Eichenbaum H (1989) Spatial and behavioral correlates of hippocampal neuronal activity. J Neurosci 9: 2737-2763.
20. Wood ER, Dudchenko PA, Eichenbaum H (1999) The global record of memory in hippocampal neuronal activity. Nature 397: 613-616.
21. Weiss C, Kronforst-Collins MA, Disterhoft JF (1996) Activity of hippocampal pyramidal neurons during trace eyeblink conditioning. Hippocampus 6: 192-209.
22. Markus EJ, Barnes CA, McNaughton BL, Gladden VL, Skaggs WE (1994) Spatial information content and reliability of hippocampal CA1 neurons: effects of visual input. Hippocampus 4: 410-421.
23. Narayanan RT, Seidenbecher T, Kluge C, Bergado J, Stork O, et al. (2007) Dissociated theta phase synchronization in amygdalo- hippocampal circuits during various stages of fear memory. Eur J Neurosci 25: 1823-1831.
24. Meier R, Haussler U, Aertsen A, Deransart C, Depaulis A, et al. (2007) Short-term changes in bilateral hippocampal coherence precede epileptiform events. Neuroimage 38: 138-149.
25. Seidenbecher T, Laxmi TR, Stork O, Pape HC (2003) Amygdalar and hippocampal theta rhythm synchronization during fear memory retrieval. Science 301: 846-850.
26. Caplan JB, Madsen JR, Raghavachari S, Kahana MJ (2001) Distinct patterns of brain oscillations underlie two basic parameters of human maze learning. J Neurophysiol 86: 368-380.
27. Kentros CG, Agnihotri NT, Streater S, Hawkins RD, Kandel ER (2004) Increased attention to spatial context increases both place field stability and spatial memory. Neuron 42: 283-295.
28. Olypher AV, Lansky P, Fenton AA (2002) Properties of the extra-positional signal in hippocampal place cell discharge derived from the overdispersion in location-specific firing. Neuroscience 111: 553-566.
29. Womelsdorf T, Fries P (2006) Neuronal coherence during selective attentional processing and sensory-motor integration. J Physiol Paris 100: 182-193.
30. Womelsdorf T, Fries P (2007) The role of neuronal synchronization in selective attention. Curr Opin Neurobiol 17: 154-160.
31. O'Keefe J (1979) A review of the hippocampal place cells. Prog Neurobiol 13: 419-439.
32. Suzuki SS, Smith GK (1985) Single-cell activity and synchronous bursting in the rat hippocampus during waking behavior and sleep. Exp Neurol 89: 71-89.
33. Leutgeb S, Leutgeb JK, Barnes CA, Moser EI, McNaughton BL, et al. (2005) Independent codes for spatial and episodic memory in hippocampal neuronal ensembles. Science 309: 619-623.
34. Bostock E, Muller RU, Kubie JL (1991) Experience-dependent modifications of hippocampal place cell firing. Hippocampus 1: 193-205.
35. Knierim JJ, Kudrimoti HS, McNaughton BL (1995) Place cells, head direction cells, and the learning of landmark stability. J Neurosci 15: 1648-1659.
36. Muller RU, Kubie JL (1987) The effects of changes in the environment on the spatial firing of hippocampal complex-spike cells. J Neurosci 7: 1951-1968.
37. Wiener SI, Korshunov VA, Garcia R, Berthoz A (1995) Inertial, substratal and landmark cue control of hippocampal CA1 place cell activity. Eur J Neurosci 7: 2206-2219.
38. Niebur E, Koch C, Rosin C (1993) An oscillation-based model for the neuronal basis of attention. Vision Res 33: 2789-2802.
39. Fell J, Klaver P, Lehnertz K, Grunwald T, Schaller C, et al. (2001) Human memory formation is accompanied by rhinal-hippocampal coupling and decoupling. Nat Neurosci 4: 1259-1264.
40. Sederberg PB, Kahana MJ, Howard MW, Donner EJ, Madsen JR (2003) Theta and gamma oscillations during encoding predict subsequent recall. J Neurosci 23: 10809-10814.
41. Johnson A, Redish AD (2007) Neural ensembles in CA3 transiently encode paths forward of the animal at a decision point. J Neurosci 27: 12176-12189.
42. Tallon-Baudry C (2003) Oscillatory synchrony and human visual cognition. J Physiol Paris 97: 355-363.
43. Vinogradova OS (2001) Hippocampus as comparator: role of the two input and two output systems of the hippocampus in selection and registration of information. Hippocampus 11: 578-598.
44. Ward LM (2003) Synchronous neural oscillations and cognitive processes. Trends Cogn Sci 7: 553-559.
45. Buzsaki G (2002) Theta oscillations in the hippocampus. Neuron 33: 325-340.
46. Fries P, Schroder JH, Roelfsema PR, Singer W, Engel AK (2002) Oscillatory neuronal synchronization in primary visual cortex as a correlate of stimulus selection. J Neurosci 22: 3739-3754.
47. Taylor K, Mandon S, Freiwald WA, Kreiter AK (2005) Coherent oscillatory activity in monkey area v4 predicts successful allocation of attention. Cereb Cortex 15: 1424-1437.
48. McNaughton BL, Barnes CA, O'Keefe J (1983) The contributions of position, direction, and velocity to single unit activity in the hippocampus of freely-moving rats. Exp Brain Res 52: 41-49.
49. Smith DM, Mizumori SJ (2006) Learning-related development of context-specific neuronal responses to places and events: the hippocampal role in context processing. J Neurosci 26: 3154-3163.
50. Eichenbaum H, Kuperstein M, Fagan A, Nagode J (1987) Cue-sampling and goal-approach correlates of hippocampal unit activity in rats performing an odor-discrimination task. J Neurosci 7: 716-732.
51. Hampson RE, Heyser CJ, Deadwyler SA (1993) Hippocampal cell firing correlates of delayed-match-to-sample performance in the rat. Behav Neurosci 107: 715-739.
52. Wood ER, Dudchenko PA, Robitsek RJ, Eichenbaum H (2000) Hippocampal neurons encode information about different types of memory episodes occurring in the same location. Neuron 27: 623-633.
53. Chun MM, Turk-Browne NB (2007) Interactions between attention and memory. Curr Opin Neurobiol 17: 177-184.
54. Desimone R (1996) Neural mechanisms for visual memory and their role in attention. Proc Natl Acad Sci U S A 93: 13494-13499.
55. Mackintosh NJ (1965) Selective Attention in Animal Discrimination Learning. Psychol Bull 64: 124-150.
56. Summerfield JJ, Lepsien J, Gitelman DR, Mesulam MM, Nobre AC (2006) Orienting attention based on long-term memory experience. Neuron 49: 905-916.
57. Zentall TR, Riley DA (2000) Selective attention in animal discrimination learning. J Gen Psychol 127: 45-66.
58. Fries P, Reynolds JH, Rorie AE, Desimone R (2001) Modulation of oscillatory neuronal synchronization by selective visual attention. Science 291: 1560-1563.
59. Womelsdorf T, Fries P, Mitra PP, Desimone R (2006) Gamma-band synchronization in visual cortex predicts speed of change detection. Nature 439: 733-736.
60. Abel T, Nguyen PV, Barad M, Deuel TA, Kandel ER, et al. (1997) Genetic demonstration of a role for PKA in the late phase of LTP and in hippocampus-based long-term memory. Cell 88: 615-626.
61. Davis S, Butcher SP, Morris RG (1992) The NMDA receptor antagonist D-2-amino-5-phosphonopentanoate (D-AP5) impairs spatial learning and LTP in vivo at intracerebral concentrations comparable to those that block LTP in vitro. J Neurosci 12: 21-34.
62. Nguyen PV, Kandel ER (1996) A macromolecular synthesis-dependent late phase of long-term potentiation requiring cAMP in the medial perforant pathway of rat hippocampal slices. J Neurosci 16: 3189-3198.
63. Axmacher N, Mormann F, Fernandez G, Elger CE, Fell J (2006) Memory formation by neuronal synchronization. Brain Res Rev 52: 170-182.
64. Klimesch W, Freunberger R, Sauseng P, Gruber W (2008) A short review of slow phase synchronization and memory: evidence for control processes in different memory systems? Brain Res 1235: 31-44.
65. Holscher C, Anwyl R, Rowan MJ (1997) Stimulation on the positive phase of hippocampal theta rhythm induces long-term potentiation that can Be depotentiated by stimulation on the negative phase in area CA1 in vivo. J Neurosci 17: 6470-6477.
66. Huerta PT, Lisman JE (1996) Low-frequency stimulation at the troughs of theta-oscillation induces long-term depression of previously potentiated CA1 synapses. J Neurophysiol 75: 877-884.
67. Wespatat V, Tennigkeit F, Singer W (2004) Phase sensitivity of synaptic modifications in oscillating cells of rat visual cortex. J Neurosci 24: 9067-9075.
68. Dan Y, Poo MM (2004) Spike timing-dependent plasticity of neural circuits. Neuron 44: 23-30.
69. Markram H, Lubke J, Frotscher M, Sakmann B (1997) Regulation of synaptic efficacy by coincidence of postsynaptic APs and EPSPs. Science 275: 213-215.
70. Thompson DJ (1982) Spectrum analysis of harmonic functions. Proceedings of the IEEE 70: 1097-1115.
71. Percival DB, Walden AT (1993) Spectral analysis of physical applications. University Press.
72. Mehta MR, Barnes CA, McNaughton BL (1997) Experience-dependent, asymmetric expansion of hippocampal place fields. Proc Natl Acad Sci U S A 94: 8918-8921.