Anatomical substrates for direct interactions between hippocampus, medial prefrontal cortex, and the thalamic nucleus reuniens

Brain Structure and Function

Volumn 219, Issue 3, 2014, Pages 911-929

  Varela, C ^a   Kumar, S ^a   Yang, J Y ^a   Wilson, M A ^a  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

Hippocampus; Memory consolidation; Prefrontal cortex; Reuniens; Thalamus; Theta

Indexed keywords

CHOLERA TOXIN B SUBUNIT; TRACER;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTERIOR POSTERIOR AXIS; ARTICLE; BRAIN CELL; CELL LABELING; CHROMATOPHORE; CONTROLLED STUDY; DENTATE GYRUS; ELECTROENCEPHALOGRAM; FEEDBACK SYSTEM; HIPPOCAMPAL CA1 REGION; HIPPOCAMPUS; LIMBIC SYSTEM; MALE; MEDIAL PREFRONTAL CORTEX; NEUROANATOMY; NONHUMAN; PREFRONTAL CORTEX; PRIORITY JOURNAL; RAT; SENSORY NERVE; SUBICULUM; THALAMIC NUCLEUS REUNIENS; THALAMUS NUCLEUS; ANATOMY AND HISTOLOGY; ANIMAL; CYTOLOGY; LONG EVANS RAT; MEMORY; NERVE CELL; NERVE TRACT; PHYSIOLOGY;

ANIMALS; HIPPOCAMPUS; MALE; MEMORY; NEURAL PATHWAYS; NEURONS; PREFRONTAL CORTEX; RATS, LONG-EVANS; THALAMIC NUCLEI;

EID: 84902377298     PISSN: 18632653     EISSN: 18632661     Source Type: Journal    
DOI: 10.1007/s00429-013-0543-5     Document Type: Article

References (69)

1. Berendse HW, Groenewegen HJ (1991) Restricted cortical termination fields of the midline and intralaminar thalamic nuclei in the rat. Neuroscience 42:73-102
2. Buzsáki G (2002) Theta oscillations in the hippocampus. Neuron 33:325-340
3. Cenquizca LA, Swanson LW (2006) An analysis of direct hippocampal cortical field CA1 axonal projections to diencephalon in the rat. J Comp Neurol 497:101-114. doi:10.1002/cne.20985 (Pubitemid 43844571)
4. Condé F, Audinat E, Maire-Lepoivre E, Crépel F (1990) Afferent connections of the medial frontal cortex of the rat. A study using retrograde transport of fluorescent dyes. I. Thalamic afferents. Brain Res Bull 24:341-354
5. Conte WL, Kamishina H, Reep RL (2009) The efficacy of the fluorescent conjugates of cholera toxin subunit B for multiple retrograde tract tracing in the central nervous system. Brain Struct Funct 213:367-373. doi:10.1007/s00429- 009-0212-x
6. Davidson TJ, Kloosterman F, Wilson MA (2009) Hippocampal replay of extended experience. Neuron 63:497-507. doi:10.1016/j.neuron.2009.07.027
7. Deng C, Rogers LJ (1999) Differential sensitivities of the two visual pathways of the chick to labelling by fluorescent retrograde tracers. J Neurosci Methods 89:75-86 (Pubitemid 29349661)
8. Dolleman-Van Der Weel MJ, Witter MP (1996) Projections from the nucleus reuniens thalami to the entorhinal cortex, hippocampal field CA1, and the subiculum in the rat arise from different populations of neurons. J Comp Neurol 364:637-650. doi:10.1002/(SICI)1096-9861(19960122)364:4〈637:AID- CNE3〉3.0. CO;2-4
9. Ego-Stengel V, Wilson MA (2010) Disruption of ripple-associated hippocampal activity during rest impairs spatial learning in the rat. Hippocampus 20:1-10. doi:10.1002/hipo.20707
10. Fanselow MS, Dong H-W (2010) Are the dorsal and ventral hippocampus functionally distinct structures? Neuron 65:7-19. doi:10.1016/j.neuron.2009.11. 031
11. Fenno L, Yizhar O, Deisseroth K (2011) The development and application of optogenetics. Annu Rev Neurosci 34:389-412. doi:10.1146/annurev-neuro-061010- 113817
12. Foster DJ, Wilson MA (2006) Reverse replay of behavioural sequences in hippocampal place cells during the awake state. Nature 440:680-683. doi:10.1038/nature04587
13. Girardeau G, Benchenane K, Wiener SI et al (2009) Selective suppression of hippocampal ripples impairs spatial memory. Nat Neurosci 12:1222-1223. doi:10.1038/nn.2384
14. Goshen I, Brodsky M, Prakash R et al (2011) Dynamics of retrieval strategies for remote memories. Cell 147:678-689. doi:10.1016/j.cell.2011.09.033
15. Halassa MM, Siegle JH, Ritt JT et al (2011) Selective optical drive of thalamic reticular nucleus generates thalamic bursts and cortical spindles. Nat Neurosci 14:1118-1120. doi:10.1038/nn.2880
16. Herkenham M (1978) The connections of the nucleus reuniens thalami: evidence for a direct thalamo-hippocampal pathway in the rat. J Comp Neurol 177:589-610. doi:10.1002/cne.901770405
17. Hoover WB, Vertes RP (2007) Anatomical analysis of afferent projections to the medial prefrontal cortex in the rat. Brain Struct Funct 212:149-179. doi:10.1007/s00429-007-0150-4 (Pubitemid 47394494)
18. Hoover WB, Vertes RP (2011) Collateral projections from nucleus reuniens of thalamus to hippocampus and medial prefrontal cortex in the rat: a single and double retrograde fluorescent labeling study. Brain Struct Funct. doi:10.1007/s00429-011-0345-6
19. Hyman JM, Zilli EA, Paley AM, Hasselmo ME (2005) Medial prefrontal cortex cells show dynamic modulation with the hippocampal theta rhythm dependent on behavior. Hippocampus 15:739-749. doi:10.1002/hipo.20106 (Pubitemid 41300824)
20. Hyman JM, Zilli EA, Paley AM, Hasselmo ME (2010) Working memory performance correlates with prefrontal-hippocampal theta interactions but not with prefrontal neuron firing rates. Front Integr Neurosci 4:2. doi:10.3389/neuro.07.002.2010
21. Jay TM, Witter MP (1991) Distribution of hippocampal CA1 and subicular efferents in the prefrontal cortex of the rat studied by means of anterograde transport of phaseolus vulgaris-leucoagglutinin. J Comp Neurol 313:574-586. doi:10.1002/cne.903130404
22. Jay TM, Thierry A-M, Wiklund L, Glowinski J (1992) Excitatory amino acid pathway from the hippocampus to the prefrontal cortex. Contribution of AMPA receptors in hippocampoprefrontal cortex transmission. Eur J Neurosci 4:1285-1295 (Pubitemid 23044623)
23. Jones EG (2007) The thalamus. Cambridge University Press, London
24. Jones MW, Wilson MA (2005) Theta rhythms coordinate hippocampal- prefrontal interactions in a spatial memory task. PLoS Biol 3:e402. doi:10.1371/journal.pbio.0030402
25. Joseph KC, Kim SU, Stieber A, Gonatas NK (1978) Endocytosis of cholera toxin into neuronal GERL. Proc Natl Acad Sci USA 75:2815-2819 (Pubitemid 8374999)
26. Kealy J, Commins S (2011) The rat perirhinal cortex: a review of anatomy, physiology, plasticity, and function. Prog Neurobiol 93:522-548. doi:10.1016/j.pneurobio.2011.03.002
27. Krettek JE, Price JL (1977) The cortical projections of the mediodorsal nucleus and adjacent thalamic nuclei in the rat. J Comp Neurol 171:157-191. doi:10.1002/cne.901710204 (Pubitemid 8016024)
28. Lee MG, Chrobak JJ, Sik A et al (1994) Hippocampal theta activity following selective lesion of the septal cholinergic system. Neuroscience 62:1033-1047. doi:10.1016/0306-4522(94)90341-7 (Pubitemid 24335599)
29. Louie K, Wilson MA (2001) Temporally structured replay of awake hippocampal ensemble activity during rapid eye movement sleep. Neuron 29:145-156 (Pubitemid 32108728)
30. Loureiro M, Cholvin T, Lopez J, et al. (2012) The ventral midline thalamus (reuniens and rhomboid nuclei) contributes to the persistence of spatial memory in rats. J Neurosci 32:9947-9959. doi:10.1523/JNEUROSCI.0410-12. 2012
31. Maviel T, Durkin TP, Menzaghi F, Bontempi B (2004) Sites of neocortical reorganization critical for remote spatial memory. Science 305:96-99. doi:10.1126/science.1098180 (Pubitemid 38869380)
32. McKenna JT, Vertes RP (2004) Afferent projections to nucleus reuniens of the thalamus. J Comp Neurol 480:115-142. doi:10.1002/cne.20342 (Pubitemid 39536621)
33. Moga MM, Weis RP, Moore RY (1995) Efferent projections of the paraventricular thalamic nucleus in the rat. J Comp Neurol 359:221-238. doi:10.1002/cne.903590204
34. Namura S, Takada M, Kikuchi H, Mizuno N (1994) Topographical organization of subicular neurons projecting to subcortical regions. Brain Res Bull 35:221-231 (Pubitemid 24274683)
35. Nyakas C, Luiten PG, Spencer DG, Traber J (1987) Detailed projection patterns of septal and diagonal band efferents to the hippocampus in the rat with emphasis on innervation of CA1 and dentate gyrus. Brain Res Bull 18:533-545
36. Oka H, Yoshida K (1985) Septohippocampal connections to field CA1 of the rat identified with field potential analysis and retrograde labeling by horseradish peroxidase. Neurosci Lett 58:19-24 (Pubitemid 15234346)
37. Otake K, Nakamura Y (1998) Single midline thalamic neurons projecting to both the ventral striatum and the prefrontal cortex in the rat. Neuroscience 86:635-649 (Pubitemid 28293940)
38. Paxinos G, Watson C (1986) The rat brain in stereotaxic coordinates. Academic Press, London
39. Peyrache A, Battaglia FP, Destexhe A (2011) Inhibition recruitment in prefrontal cortex during sleep spindles and gating of hippocampal inputs. Proc Natl Acad Sci USA 108:17207-17212. doi:10.1073/pnas.1103612108
40. Quinn JJ, Ma QD, Tinsley MR et al (2008) Inverse temporal contributions of the dorsal hippocampus and medial prefrontal cortex to the expression of long-term fear memories. Learn Mem 15:368-372. doi:10.1101/lm.813608 (Pubitemid 351629601)
41. Risold PY, Thompson RH, Swanson LW (1997) The structural organization of connections between hypothalamus and cerebral cortex. Brain Res Brain Res Rev 24:197-254 (Pubitemid 27461312)
42. Rogan SC, Roth BL (2011) Remote control of neuronal signaling. Pharmacol Rev 63:291-315. doi:10.1124/pr.110.003020
43. Schofield BR, Schofield RM, Sorensen KA, Motts SD (2007) On the use of retrograde tracers for identification of axon collaterals with multiple fluorescent retrograde tracers. Neuroscience 146:773-783. doi:10.1016/j. neuroscience.2007.02.026 (Pubitemid 46617070)
44. Shibata H (1993) Efferent projections from the anterior thalamic nuclei to the cingulate cortex in the rat. J Comp Neurol 330:533-542. doi:10.1002/cne.903300409
45. Siapas AG, Wilson MA (1998) Coordinated interactions between hippocampal ripples and cortical spindles during slow-wave sleep. Neuron 21:1123-1128 (Pubitemid 29018081)
46. Siapas AG, Lubenov EV, Wilson MA (2005) Prefrontal phase locking to hippocampal theta oscillations. Neuron 46:141-151. doi:10.1016/j.neuron.2005.02. 028 (Pubitemid 40488318)
47. Sigurdsson T, Stark KL, Karayiorgou M et al (2010) Impaired hippocampal-prefrontal synchrony in a genetic mouse model of schizophrenia. Nature 464:763-767. doi:10.1038/nature08855
48. Sirota A, Csicsvari J, Buhl D, Buzsáki G (2003) Communication between neocortex and hippocampus during sleep in rodents. Proc Natl Acad Sci USA 100:2065-2069. doi:10.1073/pnas.0437938100 (Pubitemid 36254574)
49. Squire LR, Clark RE, Knowlton BJ (2001) Retrograde amnesia. Hippocampus 11:50-55. doi:10.1002/1098-1063(2001)11:1〈50::AID-HIPO1019〉3.0.CO;2-G (Pubitemid 32201373)
50. Steffenach H-A, Witter M, Moser M-B, Moser EI (2005) Spatial memory in the rat requires the dorsolateral band of the entorhinal cortex. Neuron 45:301-313. doi:10.1016/j.neuron.2004.12.044 (Pubitemid 40128123)
51. Steriade M, Domich L, Oakson G, Deschênes M (1987) The deafferented reticular thalamic nucleus generates spindle rhythmicity. J Neurophysiol 57:260-273 (Pubitemid 17036266)
52. Stoeckel K, Schwab M, Thoenen H (1977) Role of gangliosides in the uptake and retrograde axonal transport of cholera and tetanus toxin as compared to nerve growth factor and wheat germ agglutinin. Brain Res 132:273-285 (Pubitemid 8159412)
53. Su HS, Bentivoglio M (1990) Thalamic midline cell populations projecting to the nucleus accumbens, amygdala, and hippocampus in the rat. J Comp Neurol 297:582-593. doi:10.1002/cne.902970410
54. Suh J, Rivest AJ, Nakashiba T et al (2011) Entorhinal cortex layer III input to the hippocampus is crucial for temporal association memory. Science 334:1415-1420. doi:10.1126/science.1210125
55. Swanson LW (1981) A direct projection from Ammon's horn to prefrontal cortex in the rat. Brain Res 217:150-154
56. Thompson SM, Robertson RT (1987) Organization of subcortical pathways for sensory projections to the limbic cortex. I. Subcortical projections to the medial limbic cortex in the rat. J Comp Neurol 265:175-188. doi:10.1002/cne. 902650203 (Pubitemid 17160244)
57. Van der Werf YD, Witter MP, Groenewegen HJ (2002) The intralaminar and midline nuclei of the thalamus. Anatomical and functional evidence for participation in processes of arousal and awareness. Brain Res Brain Res Rev 39:107-140 (Pubitemid 35341095)
58. van Groen T, Wyss JM (1992) Projections from the lateral dorsal nucleus of the thalamus to the limbic and visual cortices in the rat. J Comp Neurol 324:427-448. doi:10.1002/cne.903240310
59. van Groen T, Wyss JM (1995) Projections from the anterodorsal and anteroventral nucleus of the thalamus to the limbic cortex in the rat. J Comp Neurol 358:584-604. doi:10.1002/cne.903580411
60. Vertes RP (2004) Differential projections of the infralimbic and prelimbic cortex in the rat. Synapse 51:32-58. doi:10.1002/syn.10279
61. Vertes RP, Hoover WB (2008) Projections of the paraventricular and parataenial nuclei of the dorsal midline thalamus in the rat. J Comp Neurol 508:212-237. doi:10.1002/cne.21679 (Pubitemid 351562034)
62. Vertes RP, Hoover WB, Viana Di Prisco G (2004) Theta rhythm of the hippocampus: subcortical control and functional significance. Behav Cogn Neurosci Rev 3:173-200. doi:10.1177/1534582304273594
63. Vertes RP, Hoover WB, Do Valle AC et al (2006) Efferent projections of reuniens and rhomboid nuclei of the thalamus in the rat. J Comp Neurol 499:768-796. doi:10.1002/cne.21135 (Pubitemid 44730519)
64. Vertes RP, Hoover WB, Szigeti-Buck K, Leranth C (2007) Nucleus reuniens of the midline thalamus: link between the medial prefrontal cortex and the hippocampus. Brain Res Bull 71:601-609. doi:10.1016/j.brainresbull.2006.12.002 (Pubitemid 46209526)
65. Vidal-Gonzalez I, Vidal-Gonzalez B, Rauch SL, Quirk GJ (2006) Microstimulation reveals opposing influences of prelimbic and infralimbic cortex on the expression of conditioned fear. Learn Mem 13:728-733. doi:10.1101/lm.306106 (Pubitemid 44871673)
66. Wilson MA, McNaughton BL (1994) Reactivation of hippocampal ensemble memories during sleep. Science 265:676-679 (Pubitemid 24268281)
67. Wouterlood FG, Saldana E, Witter MP (1990) Projection from the nucleus reuniens thalami to 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. doi:10.1002/cne.902960202 (Pubitemid 20169520)
68. Wyss JM, Swanson LW, Cowan WM (1979) A study of subcortical afferents to the hippocampal formation in the rat. Neuroscience 4:463-476 (Pubitemid 9142686)
69. Yamano M, Luiten PG (1989) Direct synaptic contacts of medial septal efferents with somatostatin immunoreactive neurons in the rat hippocampus. Brain Res Bull 22:993-1001 (Pubitemid 19231355)