CoChat
Sign Up
Cited by 309Memory and Neural MechanismsSchizophrenia research and treatmentNeural and Behavioral Psychology Studies

Hippocampal-Prefrontal Interactions in Cognition, Behavior and Psychiatric Disease

Open access
Sigurdsson, Torfi, Duvarci, Sevil·2016·Frontiers in Systems Neuroscience
DOI 10.3389/fnsys.2015.00190PMC PMC4727104
Open this paper in CoChat — free accountOpen PDF

Abstract

The hippocampus and prefrontal cortex (PFC) have long been known to play a central role in various behavioral and cognitive functions. More recently, electrophysiological and functional imaging studies have begun to examine how interactions between the two structures contribute to behavior during various tasks. At the same time, it has become clear that hippocampal-prefrontal interactions are disrupted in psychiatric disease and may contribute to their pathophysiology. These impairments have most frequently been observed in schizophrenia, a disease that has long been associated with hippocampal and prefrontal dysfunction. Studies in animal models of the illness have also begun to relate disruptions in hippocampal-prefrontal interactions to the various risk factors and pathophysiological mechanisms of the illness. The goal of this review is to summarize what is known about the role of hippocampal-prefrontal interactions in normal brain function and compare how these interactions are disrupted in schizophrenia patients and animal models of the disease. Outstanding questions for future research on the role of hippocampal-prefrontal interactions in both healthy brain function and disease states are also discussed.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.3389/fnsys.2015.00190

Cites

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • The maturation of PV+ interneurons is crucial for the development of oscillatory activity across the neocortex and hippocampus.

    “In addition, the maturation of PV+ interneurons is crucial for the development of oscillatory activity across the neocortex and hippocampus.”

    From Developmental timing and critical windows for the treatment of psychiatric disorders (2016) · cites this paper as [39]

  • Fast-spiking PV+ interneurons synchronize local assemblies of pyramidal cells in the gamma frequency, which contributes to the emergence of functional interactions between the hippocampus and the prefrontal cortex.

    “Fast-spiking PV+ interneurons synchronize local assemblies of pyramidal cells in the gamma frequency, which contributes to the emergence of functional interactions between the hippocampus and the prefrontal cortex 39 .”

    From Developmental timing and critical windows for the treatment of psychiatric disorders (2016) · cites this paper as [39]

  • Normal gamma rhythms and hippocampal-prefrontal synchrony are critical for multiple cognitive tasks that are disrupted in schizophrenia.

    “In humans, normal gamma rhythms and hippocampal-prefrontal synchrony are critical for multiple cognitive tasks that are disrupted in schizophrenia 28,39 ,”

    From Developmental timing and critical windows for the treatment of psychiatric disorders (2016) · cites this paper as [39]

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

The citation lists haven’t been fetched yet

References 166 · Cited by 309

Research works printed but not linked: 135

  1. Adhikari, A., Topiwala, M. A., and Gordon, J. A. (2010). Synchronized activity between the ventral hippocampus and the medial prefrontal cortex during anxiety. Neuron 65, 257-269. doi: 10.1016/j.neuron.2009. 12.002 · DOI · Paper page
  2. Adhikari, A., Topiwala, M. A., and Gordon, J. A. (2011). Single units in the medial prefrontal cortex with anxiety-related firing patterns are preferentially influenced by ventral hippocampal activity. Neuron 71, 898-910. doi: 10.1016/j. neuron.2011.07.027 · DOI · Paper page
  3. Amann, L. C., Gandal, M. J., Halene, T. B., Ehrlichman, R. S., White, S. L., McCarren, H. S., et al. (2010). Mouse behavioral endophenotypes for schizophrenia. Brain Res. Bull. 83, 147-161. doi: 10.1016/j.brainresbull.2010. 04.008 · DOI
  4. Arguello, P. A., and Gogos, J. A. (2010). Cognition in mouse models of schizophrenia susceptibility genes. Schizophr. Bull. 36, 289-300. doi: 10. 1093/schbul/sbp153 · DOI
  5. Bähner, F., Demanuele, C., Schweiger, J., Gerchen, M. F., Zamoscik, V., Ueltzhöffer, K., et al. (2015). Hippocampal-dorsolateral prefrontal coupling as a species-conserved cognitive mechanism: a human translational imaging study. Neuropsychopharmacology 40, 1674-1681. doi: 10.1038/npp. 2015. · DOI
  6. Bannerman, D. M., Rawlins, J. N. P., McHugh, S. B., Deacon, R. M. J., Yee, B. K., Bast, T., et al. (2004). Regional dissociations within the hippocampus-memory and anxiety. Neurosci. Biobehav. Rev. 28, 273-283. doi: 10.1016/j.neubiorev. 2004.03.004 · DOI · Paper page
  7. Barbas, H., and Blatt, G. J. (1995). Topographically specific hippocampal projections target functionally distinct prefrontal areas in the rhesus monkey. Hippocampus 5, 511-533. doi: 10.1002/hipo.450050604 · DOI
  8. Barch, D. M., and Ceaser, A. (2012). Cognition in schizophrenia: core psychological and neural mechanisms. Trends Cogn. Sci. 16, 27-34. doi: 10. 1016/j.tics.2011.11.015 · DOI
  9. Benetti, S., Mechelli, A., Picchioni, M., Broome, M., Williams, S., and McGuire, P. (2009). Functional integration between the posterior hippocampus and prefrontal cortex is impaired in both first episode schizophrenia and the at risk mental state. Brain 132(Pt. 9), 2426-2436. doi: 10.1093/brain/awp098 · DOI
  10. Brandon, N. J., and Sawa, A. (2011). Linking neurodevelopmental and synaptic theories of mental illness through DISC1. Nat. Rev. Neurosci. 12, 707-722. doi: 10.1038/nrn3120 · DOI
  11. Brincat, S. L., and Miller, E. K. (2015). Frequency-specific hippocampal-prefrontal interactions during associative learning. Nat. Neurosci. 18, 576-581. doi: 10. 1038/nn.3954 · DOI
  12. Buckner, R. L., Krienen, F. M., and Yeo, B. T. T. (2013). Opportunities and limitations of intrinsic functional connectivity MRI. Nat. Neurosci. 16, 832-837. doi: 10.1038/nn.3423 · DOI · Paper page
  13. Buzsáki, G. (2002). Theta oscillations in the hippocampus. Neuron 33, 325-340. doi: 10.1016/s0896-6273(02)00586-x · DOI · Paper page
  14. Buzsáki, G., and Moser, E. I. (2013). Memory, navigation and theta rhythm in the hippocampal-entorhinal system. Nat. Neurosci. 16, 130-138. doi: 10.1038/nn. 3304 · DOI · Paper page
  15. Buzsáki, G., and Wang, X.-J. (2012). Mechanisms of gamma oscillations. Annu. Rev. Neurosci. 35, 203-225. doi: 10.1146/annurev-neuro-062111-150444 · DOI · Paper page
  16. Canetta, S. E., and Brown, A. S. (2012). Prenatal infection, maternal immune activation, and risk for schizophrenia. Transl. Neurosci. 3, 320-327. doi: 10. 2478/s13380-012-0045-6 · DOI
  17. Cassel, J.-C., Pereira de Vasconcelos, A., Loureiro, M., Cholvin, T., Dalrymple- Alford, J. C., and Vertes, R. P. (2013). The reuniens and rhomboid nuclei: neuroanatomy, electrophysiological characteristics and behavioral implications. Prog. Neurobiol. 111, 34-52. doi: 10.1016/j.pneurobio.2013. 08.006 · DOI
  18. Chung, K., and Deisseroth, K. (2013). CLARITY for mapping the nervous system. Nat. Methods 10, 508-513. doi: 10.1038/nmeth.2481 · DOI · Paper page
  19. Churchwell, J. C., and Kesner, R. P. (2011). Hippocampal-prefrontal dynamics in spatial working memory: interactions and independent parallel processing. Behav. Brain Res. 225, 389-395. doi: 10.1016/j.bbr.2011.07.045 · DOI
  20. Colgin, L. L. (2011). Oscillations and hippocampal-prefrontal synchrony. Curr. Opin. Neurobiol. 21, 467-474. doi: 10.1016/j.conb.2011.04.006 · DOI · Paper page
  21. Condé, F., Maire-lepoivre, E., Audinat, E., and Crépel, F. (1995). Afferent connections of the medial frontal cortex of the rat. II. Cortical and subcortical afferents. J. Comp. Neurol. 352, 567-593. doi: 10.1002/cne.903520407 · DOI
  22. Cousijn, H., Tunbridge, E. M., Rolinski, M., Wallis, G., Colclough, G. L., Woolrich, M. W., et al. (2015). Modulation of hippocampal theta and hippocampal-prefrontal cortex function by a schizophrenia risk gene. Hum. Brain Mapp. 36, 2387-2395. doi: 10.1002/hbm.22778 · DOI
  23. Crabtree, G. W., and Gogos, J. A. (2014). Synaptic plasticity, neural circuits and the emerging role of altered short-term information processing in schizophrenia. Front. Synaptic Neurosci. 6:28. doi: 10.3389/fnsyn.2014.00028 · DOI
  24. Dawson, N., Kurihara, M., Thomson, D. M., Winchester, C. L., McVie, A., Hedde, J. R., et al. (2015). Altered functional brain network connectivity and glutamate system function in transgenic mice expressing truncated disrupted-in-schizophrenia 1. Transl. Psychiatry 5:e569. doi: 10.1038/tp. 2015.60 · DOI
  25. Del Pino, I., García-Frigola, C., Dehorter, N., Brotons-Mas, J. R., Alvarez- Salvado, E., Martínez de Lagrán, M., et al. (2013). Erbb4 deletion from fast-spiking interneurons causes schizophrenia-like phenotypes. Neuron 79, 1152-1168. doi: 10.1016/j.neuron.2013.07.010 · DOI · Paper page
  26. Dickerson, D. D., and Bilkey, D. K. (2013). Aberrant neural synchrony in the maternal immune activation model: using translatable measures to explore targeted interventions. Front. Behav. Neurosci. 7:217. doi: 10.3389/fnbeh.2013. 00217 · DOI
  27. Dickerson, D. D., Overeem, K. A., Wolff, A. R., Williams, J. M., Abraham, W. C., and Bilkey, D. K. (2014). Association of aberrant neural synchrony and altered GAD67 expression following exposure to maternal immune activation, a risk factor for schizophrenia. Transl. Psychiatry 4:e418. doi: 10.1038/tp.2014. · DOI
  28. Dickerson, D. D., Restieaux, A. M., and Bilkey, D. K. (2012). Clozapine administration ameliorates disrupted long-range synchrony in a neurodevelopmental animal model of schizophrenia. Schizophr. Res. 135, 112-115. doi: 10.1016/j.schres.2011.12.016 · DOI
  29. Dickerson, D. D., Wolff, A. R., and Bilkey, D. K. (2010). Abnormal long- range neural synchrony in a maternal immune activation animal model of schizophrenia. J. Neurosci. 30, 12424-12431. doi: 10.1523/JNEUROSCI.3046- 10.2010 · DOI
  30. Drew, L. J., Crabtree, G. W., Markx, S., Stark, K. L., Chaverneff, F., Xu, B., et al. (2011). The 22q11.2 microdeletion: fifteen years of insights into the genetic and neural complexity of psychiatric disorders. Int. J. Dev. Neurosci. 29, 259-281. doi: 10.1016/j.ijdevneu.2010.09.007 · DOI
  31. Dudchenko, P. A. (2004). An overview of the tasks used to test working memory in rodents. Neurosci. Biobehav. Rev. 28, 699-709. doi: 10.1016/j.neubiorev.2004. 09.002 · DOI
  32. Eichenbaum, H., and Cohen, N. J. (2014). Can we reconcile the declarative memory and spatial navigation views on hippocampal function? Neuron 83, 764-770. doi: 10.1016/j.neuron.2014.07.032 · DOI
  33. Esslinger, C., Kirsch, P., Haddad, L., Mier, D., Sauer, C., Erk, S., et al. (2011). Cognitive state and connectivity effects of the genome-wide significant psychosis variant in ZNF804A. Neuroimage 54, 2514-2523. doi: 10.1016/j. neuroimage.2010.10.012 · DOI
  34. Euston, D. R., Gruber, A. J., and McNaughton, B. L. (2012). The role of medial prefrontal cortex in memory and decision making. Neuron 76, 1057-1070. doi: 10.1016/j.neuron.2012.12.002 · DOI · Paper page
  35. Finn, A. S., Sheridan, M. A., Kam, C. L. H., Hinshaw, S., and D'Esposito, M. (2010). Longitudinal evidence for functional specialization of the neural circuit supporting working memory in the human brain. J. Neurosci. 30, 11062-11067. doi: 10.1523/JNEUROSCI.6266-09.2010 · DOI · Paper page
  36. Fletcher, P. (1998). The missing link: a failure of fronto-hippocampal integration in schizophrenia. Nat. Neurosci. 1, 266-267. doi: 10.1038/1078 · DOI
  37. Fornito, A., and Bullmore, E. T. (2012). Connectomic intermediate phenotypes for psychiatric disorders. Front. Psychiatry 3:32. doi: 10.3389/fpsyt.2012.00032 · DOI
  38. Fox, M. D., and Raichle, M. E. (2007). Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging. Nat. Rev. Neurosci. 8, 700-711. doi: 10.1038/nrn2201 · DOI · Paper page
  39. Frohlich, J., and van Horn, J. D. (2014). Reviewing the ketamine model for schizophrenia. J. Psychopharmacol. 28, 287-302. doi: 10. 1177/0269881113512909 · DOI · Paper page
  40. Fuster, J. (2015). The Prefrontal Cortex. New York: Academic Press.
  41. Gardner, R. J., Kersanté, F., Jones, M. W., and Bartsch, U. (2014). Neural oscillations during non-rapid eye movement sleep as biomarkers of circuit dysfunction in schizophrenia. Eur. J. Neurosci. 39, 1091-1106. doi: 10.1111/ejn. 12533 · DOI
  42. Gass, N., Schwarz, A. J., Sartorius, A., Schenker, E., Risterucci, C., Spedding, M., et al. (2014). Sub-anesthetic ketamine modulates intrinsic BOLD connectivity within the hippocampal-prefrontal circuit in the rat. Neuropsychopharmacology 39, 895-906. doi: 10.1038/npp.2013.290 · DOI
  43. Genzel, L., Dresler, M., Cornu, M., Jäger, E., Konrad, B., Adamczyk, M., et al. (2015). Medial prefrontal-hippocampal connectivity and motor memory consolidation in depression and schizophrenia. Biol. Psychiatry 77, 177-186. doi: 10.1016/j.biopsych.2014.06.004 · DOI
  44. Glahn, D. C., Ragland, J. D., Abramoff, A., Barrett, J., Laird, A. R., Bearden, C. E., et al. (2005). Beyond hypofrontality: a quantitative meta-analysis of functional neuroimaging studies of working memory in schizophrenia. Hum. Brain Mapp. 25, 60-69. doi: 10.1002/hbm.20138 · DOI
  45. Godsil, B. P., Kiss, J. P., Spedding, M., and Jay, T. M. (2013). The hippocampal-prefrontal pathway: the weak link in psychiatric disorders? Eur. Neuropsychopharmacol. 23, 1165-1181. doi: 10.1016/j.euroneuro.2012.10.018 · DOI
  46. Gregoriou, G. G., Gotts, S. J., Zhou, H., and Desimone, R. (2009). Long-range neural coupling through synchronization with attention. Prog. Brain Res. 176, 35-45. doi: 10.1016/s0079-6123(09)17603-3 · DOI
  47. Grimm, O., Gass, N., Weber-Fahr, W., Sartorius, A., Schenker, E., Spedding, M., et al. (2015). Acute ketamine challenge increases resting state prefrontal- hippocampal connectivity in both humans and rats. Psychopharmacology 232, 4231-4241. doi: 10.1007/s00213-015-4022-y · DOI
  48. Gruart, A., Leal-Campanario, R., López-Ramos, J. C., and Delgado-García, J. M. (2015). Functional basis of associative learning and their relationships with long-term potentiation evoked in the involved neural circuits: lessons from studies in behaving mammals. Neurobiol. Learn. Mem. 124, 3-18. doi: 10. 1016/j.nlm.2015.04.006 · DOI
  49. Gurung, R., and Prata, D. P. (2015). What is the impact of genome-wide supported risk variants for schizophrenia and bipolar disorder on brain structure and function? A systematic review. Psychol. Med. 45, 2461-2480. doi: 10.1017/s0033291715000537 · DOI
  50. Harris, A. Z., and Gordon, J. A. (2015). Long-range neural synchrony in behavior. Annu. Rev. Neurosci. 38, 171-194. doi: 10.1146/annurev-neuro-071714-034111 · DOI
  51. Harrison, P. J. (2015). Recent genetic findings in schizophrenia and their therapeutic relevance. J. Psychopharmacol. 29, 85-96. doi: 10. 1177/0269881114553647 · DOI
  52. Harrison, P. J., and Law, A. J. (2006). Neuregulin 1 and schizophrenia: genetics, gene expression and neurobiology. Biol. Psychiatry 60, 132-140. doi: 10.1016/j. biopsych.2005.11.002 · DOI
  53. N. R. Swerdlow (Heidelberg: Springer), 529-553.
  54. Heckers, S., Rauch, S. L., Goff, D., Savage, C. R., Schacter, D. L., Fischman, A. J., et al. (1998). Impaired recruitment of the hippocampus during conscious recollection in schizophrenia. Nat. Neurosci. 1, 318-323. doi: 10. 1038/1137 · DOI · Paper page
  55. Heidbreder, C. A., and Groenewegen, H. J. (2003). The medial prefrontal cortex in the rat: evidence for a dorso-ventral distinction based upon functional and anatomical characteristics. Neurosci. Biobehav. Rev. 27, 555-579. doi: 10.1016/j. neubiorev.2003.09.003 · DOI · Paper page
  56. Henseler, I., Falkai, P., and Gruber, O. (2010). Disturbed functional connectivity within brain networks subserving domain-specific subcomponents of working memory in schizophrenia: relation to performance and clinical symptoms. J. Psychiatr. Res. 44, 364-372. doi: 10.1016/j.jpsychires.2009.09.003 · DOI
  57. Hoover, W. B., and Vertes, R. P. (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 · DOI · Paper page
  58. Hugues, S., Chessel, A., Lena, I., Marsault, R., and Garcia, R. (2006). Prefrontal infusion of PD098059 immediately after fear extinction training blocks extinction-associated prefrontal synaptic plasticity and decreases prefrontal ERK2 phosphorylation. Synapse 60, 280-287. doi: 10.1002/syn.20291 · DOI
  59. Hyman, J. M., Hasselmo, M. E., and Seamans, J. K. (2011). What is the functional relevance of prefrontal cortex entrainment to hippocampal theta rhythms? Front. Neurosci. 5:24. doi: 10.3389/fnins.2011.00024 · DOI
  60. Hyman, J. M., Zilli, E. A., Paley, A. M., and Hasselmo, M. E. (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 · DOI
  61. Hyman, J. M., Zilli, E. A., Paley, A. M., and Hasselmo, M. E. (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 · DOI
  62. Javitt, D. C., and Zukin, S. R. (1991). Recent advances in the phencyclidine model of schizophrenia. Am. J. Psychiatry 148, 1301-1308. doi: 10.1176/ajp.148.10. 1301 · DOI · Paper page
  63. Jones, M. W., and Wilson, M. A. (2005a). Theta rhythms coordinate hippocampal- prefrontal interactions in a spatial memory task. PLoS Biol. 3:e402. doi: 10. 1371/journal.pbio.0030402 · DOI · Paper page
  64. Jones, M. W., and Wilson, M. A. (2005b). Phase precession of medial prefrontal cortical activity relative to the hippocampal theta rhythm. Hippocampus 15, 867-873. doi: 10.1002/hipo.20119 · DOI
  65. Karayiorgou, M., Simon, T. J., and Gogos, J. A. (2010). 22q11.2 microdeletions: linking DNA structural variation to brain dysfunction and schizophrenia. Nat. Rev. Neurosci. 11, 402-416. doi: 10.1038/nrn2841 · DOI · Paper page
  66. Kesner, R. P., and Churchwell, J. C. (2011). An analysis of rat prefrontal cortex in mediating executive function. Neurobiol. Learn. Mem. 96, 417-431. doi: 10. 1016/j.nlm.2011.07.002 · DOI
  67. Layfield, D. M., Patel, M., Hallock, H., and Griffin, A. L. (2015). Inactivation of the nucleus reuniens/rhomboid causes a delay-dependent impairment of spatial working memory. Neurobiol. Learn. Mem. 125, 163-167. doi: 10.1016/j.nlm. 2015.09.007 · DOI
  68. Lee, H., Dvorak, D., Kao, H.-Y., Duffy, Á. M., Scharfman, H. E., and Fenton, A. A. (2012). Early cognitive experience prevents adult deficits in a neurodevelopmental schizophrenia model. Neuron 75, 714-724. doi: 10.1016/j. neuron.2012.06.016 · DOI · Paper page
  69. Li, M., Long, C., and Yang, L. (2015). Hippocampal-prefrontal circuit and disrupted functional connectivity in psychiatric and neurodegenerative disorders. Biomed. Res. Int. 2015:810548. doi: 10.1155/2015/ 810548 · DOI
  70. Liang, M., Zhou, Y., Jiang, T., Liu, Z., Tian, L., Liu, H., et al. (2006). Widespread functional disconnectivity in schizophrenia with resting-state functional magnetic resonance imaging. Neuroreport 17, 209-213. doi: 10.1097/01.wnr. 0000198434.06518. · DOI
  71. Likhtik, E., Stujenske, J. M., Topiwala, M. A., Harris, A. Z., and Gordon, J. A. (2014). Prefrontal entrainment of amygdala activity signals safety in learned fear and innate anxiety. Nat. Neurosci. 17, 106-113. doi: 10.1038/nn. 3582 · DOI · Paper page
  72. Liu, B., Zhang, X., Hou, B., Li, J., Qiu, C., Qin, W., et al. (2014). The impact of MIR137 on dorsolateral prefrontal-hippocampal functional connectivity in healthy subjects. Neuropsychopharmacology 39, 2153-2160. doi: 10.1038/npp. 2014. · DOI
  73. Lodge, D. J., and Grace, A. A. (2009). Gestational methylazoxymethanol acetate administration: a developmental disruption model of schizophrenia. Behav. Brain Res. 204, 306-312. doi: 10.1016/j.bbr.2009.01.031 · DOI
  74. Maren, S., Phan, K. L., and Liberzon, I. (2013). The contextual brain: implications for fear conditioning, extinction and psychopathology. Nat. Rev. Neurosci. 14, 417-428. doi: 10.1038/nrn3492 · DOI · Paper page
  75. McDonald, C., and Murray, R. M. (2000). Early and late environmental risk factors for schizophrenia. Brain Res. Brain Res. Rev. 31, 130-137. doi: 10.1016/s0165- 0173(99)00030-2 · DOI
  76. Mei, L., and Nave, K.-A. (2014). Neuregulin-ERBB signaling in the nervous system and neuropsychiatric diseases. Neuron 83, 27-49. doi: 10.1016/j.neuron.2014. 06.007 · DOI
  77. Meyer-Lindenberg, A. (2010). From maps to mechanisms through neuroimaging of schizophrenia. Nature 468, 194-202. doi: 10.1038/nature09569 · DOI
  78. Meyer-Lindenberg, A. S., Olsen, R. K., Kohn, P. D., Brown, T., Egan, M. F., Weinberger, D. R., et al. (2005). Regionally specific disturbance of dorsolateral prefrontal-hippocampal functional connectivity in schizophrenia. Arch. Gen. Psychiatry 62, 379-386. doi: 10.1001/archpsyc.62.4.379 · DOI · Paper page
  79. Meyer-Lindenberg, A., and Weinberger, D. R. (2006). Intermediate phenotypes and genetic mechanisms of psychiatric disorders. Nat. Rev. Neurosci. 7, 818-827. doi: 10.1038/nrn1993 · DOI · Paper page
  80. Millar, J. K., Wilson-Annan, J. C., Anderson, S., Christie, S., Taylor, M. S., Semple, C. A., et al. (2000). Disruption of two novel genes by a translocation co-segregating with schizophrenia. Hum. Mol. Genet. 9, 1415-1423. doi: 10. 1093/hmg/9.9.1415 · DOI · Paper page
  81. Miller, E. K., and Cohen, J. D. (2001). An integrative theory of prefrontal cortex function. Annu. Rev. Neurosci. 24, 167-202. doi: 10.1146/annurev.neuro. 24.1.167 · DOI · Paper page
  82. Modinos, G., Allen, P., Grace, A. A., and McGuire, P. (2015). Translating the MAM model of psychosis to humans. Trends Neurosci. 38, 129-138. doi: 10.1016/j. tins.2014.12.005 · DOI · Paper page
  83. Moore, H., Jentsch, J. D., Ghajarnia, M., Geyer, M. A., and Grace, A. A. (2006). A neurobehavioral systems analysis of adult rats exposed to methylazoxymethanol acetate on E17: implications for the neuropathology of schizophrenia. Biol. Psychiatry 60, 253-264. doi: 10.1016/j.biopsych.2006. 01.003 · DOI
  84. Moser, E. I., Witter, M. P., and Moser, M.-B. (2010). ''Entorhinal cortex,'' in Handbook of Brain Microcircuits, eds G. M. Shepherd and S. Grillner (Oxford: Oxford University Press), 175-190.
  85. Mukai, J., Tamura, M., Fénelon, K., Rosen, A. M., Spellman, T. J., Kang, R., et al. (2015). Molecular substrates of altered axonal growth and brain connectivity in a mouse model of schizophrenia. Neuron 86, 680-695. doi: 10.1016/j.neuron. 2015.04.003 · DOI · Paper page
  86. Navawongse, R., and Eichenbaum, H. (2013). Distinct pathways for rule-based retrieval and spatial mapping of memory representations in hippocampal neurons. J. Neurosci. 33, 1002-1013. doi: 10.1523/JNEUROSCI.3891-12.2013 · DOI
  87. Nestler, E. J., and Hyman, S. E. (2010). Animal models of neuropsychiatric disorders. Nat. Neurosci. 13, 1161-1169. doi: 10.1038/nn.2647 · DOI · Paper page
  88. O'Donnell, P. (2012). Cortical disinhibition in the neonatal ventral hippocampal lesion model of schizophrenia: new vistas on possible therapeutic approaches. Pharmacol. Ther. 133, 19-25. doi: 10.1016/j.pharmthera.2011.07.005 · DOI
  89. O'Donovan, M. C., Craddock, N., Norton, N., Williams, H., Peirce, T., Moskvina, V., et al. (2008). Identification of loci associated with schizophrenia by genome-wide association and follow-up. Nat. Genet. 40, 1053-1055. doi: 10. 1038/ng.201 · DOI · Paper page
  90. O'Neill, P.-K., Gordon, J. A., and Sigurdsson, T. (2013). Theta oscillations in the medial prefrontal cortex are modulated by spatial working memory and synchronize with the hippocampus through its ventral subregion. J. Neurosci. 33, 14211-14224. doi: 10.1523/JNEUROSCI.2378-13.2013 · DOI
  91. Öngür, D., and Price, J. L. (2000). The organization of networks within the orbital and medial prefrontal cortex of rats, monkeys and humans. Cereb. Cortex 10, 206-219. doi: 10.1093/cercor/10.3.206 · DOI · Paper page
  92. Paulus, F. M., Bedenbender, J., Krach, S., Pyka, M., Krug, A., Sommer, J., et al. (2014). Association of rs1006737 in CACNA1C with alterations in prefrontal activation and fronto-hippocampal connectivity. Hum. Brain Mapp. 35, 1190-1200. doi: 10.1002/hbm.22244 · DOI
  93. Paulus, F. M., Krach, S., Bedenbender, J., Pyka, M., Sommer, J., Krug, A., et al. (2013). Partial support for ZNF804A genotype-dependent alterations in prefrontal connectivity. Hum. Brain Mapp. 34, 304-313. doi: 10.1002/hbm. 21434 · DOI
  94. Peters, J., Dieppa-Perea, L. M., Melendez, L. M., and Quirk, G. J. (2010). Induction of fear extinction with hippocampal-infralimbic BDNF. Science 328, 1288-1290. doi: 10.1126/science.1186909 · DOI · Paper page
  95. Peyrache, A., Khamassi, M., Benchenane, K., Wiener, S. I., and Battaglia, F. P. (2009). Replay of rule-learning related neural patterns in the prefrontal cortex during sleep. Nat. Neurosci. 12, 919-926. doi: 10.1038/nn.2337 · DOI · Paper page
  96. Phillips, K. G., Bartsch, U., McCarthy, A. P., Edgar, D. M., Tricklebank, M. D., Wafford, K. A., et al. (2012). Decoupling of sleep-dependent cortical and hippocampal interactions in a neurodevelopmental model of schizophrenia. Neuron 76, 526-533. doi: 10.1016/j.neuron.2012.09.016 · DOI
  97. Popa, D., Duvarci, S., Popescu, A. T., Léna, C., and Paré, D. (2010). Coherent amygdalocortical theta promotes fear memory consolidation during paradoxical sleep. Proc. Natl. Acad. Sci. U S A 107, 6516-6519. doi: 10. 1073/pnas.0913016107 · DOI · Paper page
  98. Powell, S. B., Weber, M., and Geyer, M. A. (2012). Genetic models of sensorimotor gating: relevance to neuropsychiatric disorders. Curr. Top. Behav. Neurosci. 12, 251-318. doi: 10.1007/7854_2011_195 · DOI
  99. Preston, A. R., and Eichenbaum, H. (2013). Interplay of hippocampus and prefrontal cortex in memory. Curr. Biol. 23, R764-R773. doi: 10.1016/j.cub. 2013.05.041 · DOI · Paper page
  100. Preuss, T. M. (1995). Do rats have prefrontal cortex? The rose-woolsey- akert program reconsidered. J. Cogn. Neurosci. 7, 1-24. doi: 10.1162/jocn. 1995.7.1.1 · DOI · Paper page
  101. Rajasethupathy, P., Sankaran, S., Marshel, J. H., Kim, C. K., Ferenczi, E., Lee, S. Y., et al. (2015). Projections from neocortex mediate top-down control of memory retrieval. Nature 526, 653-659. doi: 10.1038/nature 15389 · DOI · Paper page
  102. Rasetti, R., Sambataro, F., Chen, Q., Callicott, J. H., Mattay, V. S., and Weinberger, D. R. (2011). Altered cortical network dynamics: a potential intermediate phenotype for schizophrenia and association with ZNF804A. Arch. Gen. Psychiatry 68, 1207-1217. doi: 10.1001/archgenpsychiatry.2011.103 · DOI
  103. Remondes, M., and Wilson, M. A. (2013). Cingulate-hippocampus coherence and trajectory coding in a sequential choice task. Neuron 80, 1277-1289. doi: 10. 1016/j.neuron.2013.08.037 · DOI
  104. Rissman, J., Gazzaley, A., and D'Esposito, M. (2008). Dynamic adjustments in prefrontal, hippocampal and inferior temporal interactions with increasing visual working memory load. Cereb. Cortex 18, 1618-1629. doi: 10. 1093/cercor/bhm195 · DOI
  105. Rosen, A. M., Spellman, T., and Gordon, J. A. (2015). Electrophysiological endophenotypes in rodent models of schizophrenia and psychosis. Biol. Psychiatry 77, 1041-1049. doi: 10.1016/j.biopsych.2015.03.021 · DOI
  106. Rosene, D. L., and Van Hoesen, G. W. (1977). Hippocampal efferents reach widespread areas of cerebral cortex and amygdala in the rhesus monkey. Science 198, 315-317. doi: 10.1126/science.410102 · DOI
  107. Sauer, J.-F., Strüber, M., and Bartos, M. (2015). Impaired fast-spiking interneuron function in a genetic mouse model of depression. Elife 4:e04979. doi: 10. 7554/eLife.04979 · DOI
  108. Schobel, S. A., Chaudhury, N. H., Khan, U. A., Paniagua, B., Styner, M. A., Asllani, I., et al. (2013). Imaging patients with psychosis and a mouse model establishes a spreading pattern of hippocampal dysfunction and implicates glutamate as a driver. Neuron 78, 81-93. doi: 10.1016/j.neuron.2013.02.011 · DOI · Paper page
  109. Schölvinck, M. L., Maier, A., Ye, F. Q., Duyn, J. H., and Leopold, D. A. (2010). Neural basis of global resting-state fMRI activity. Proc. Natl. Acad. Sci. U S A 107, 10238-10243. doi: 10.1073/pnas.09131 10107 · DOI · Paper page
  110. Shmuel, A., and Leopold, D. A. (2008). Neuronal correlates of spontaneous fluctuations in fMRI signals in monkey visual cortex: implications for functional connectivity at rest. Hum. Brain Mapp. 29, 751-761. doi: 10. 1002/hbm.20580 · DOI · Paper page
  111. Siapas, A. G., Lubenov, E. V., and Wilson, M. A. (2005). Prefrontal phase locking to hippocampal theta oscillations. Neuron 46, 141-151. doi: 10.1016/j.neuron. 2005.02.028 · DOI · Paper page
  112. Sigurdsson, T. (2015). Neural circuit dysfunction in schizophrenia: insights from animal models. Neuroscience doi: 10.1016/j.neuroscience.2015.06.059 [Epub ahead of print]. · DOI
  113. Sigurdsson, T., Stark, K. L., Karayiorgou, M., Gogos, J. A., and Gordon, J. A. (2010). Impaired hippocampal-prefrontal synchrony in a genetic mouse model of schizophrenia. Nature 464, 763-767. doi: 10.1038/nature08855 · DOI · Paper page
  114. Small, S. A., Schobel, S. A., Buxton, R. B., Witter, M. P., and Barnes, C. A. (2011). A pathophysiological framework of hippocampal dysfunction in ageing and disease. Nat. Rev. Neurosci. 12, 585-601. doi: 10.1038/ nrn3085 · DOI
  115. Sotres-Bayon, F., Sierra-Mercado, D., Pardilla-Delgado, E., and Quirk, G. J. (2012). Gating of fear in prelimbic cortex by hippocampal and amygdala inputs. Neuron 76, 804-812. doi: 10.1016/j.neuron.2012.09.028 · DOI
  116. Spellman, T. J., and Gordon, J. A. (2015). Synchrony in schizophrenia: a window into circuit-level pathophysiology. Curr. Opin. Neurobiol. 30C, 17-23. doi: 10. 1016/j.conb.2014.08.009 · DOI
  117. Stark, K. L., Xu, B., Bagchi, A., Lai, W.-S., Liu, H., Hsu, R., et al. (2008). Altered brain microRNA biogenesis contributes to phenotypic deficits in a 22q11- deletion mouse model. Nat. Genet. 40, 751-760. doi: 10.1038/ng.138 · DOI · Paper page
  118. St Clair, D., Blackwood, D., Muir, W., Carothers, A., Walker, M., Spowart, G., et al. (1990). Association within a family of a balanced autosomal translocation with major mental illness. Lancet 336, 13-16. doi: 10.1016/0140-6736(90) 91520-k · DOI · Paper page
  119. Strange, B. A., Witter, M. P., Lein, E. S., and Moser, E. I. (2014). Functional organization of the hippocampal longitudinal axis. Nat. Rev. Neurosci. 15, 655-669. doi: 10.1038/nrn3785 · DOI · Paper page
  120. Thierry, A. M., Gioanni, Y., Dégénétais, E., and Glowinski, J. (2000). Hippocampo- prefrontal cortex pathway: anatomical and electrophysiological characteristics. Hippocampus 10, 411-419. doi: 10.1002/1098-1063(2000)10:4<411::aid- hipo7>3.0.co;2-a Tost, H., Bilek, E., and Meyer-Lindenberg, A. (2012). Brain connectivity in psychiatric imaging genetics. Neuroimage 62, 2250-2260. doi: 10.1016/j. neuroimage.2011.11.007 · DOI
  121. Tye, K. M., and Deisseroth, K. (2012). Optogenetic investigation of neural circuits underlying brain disease in animal models. Nat. Rev. Neurosci. 13, 251-266. doi: 10.1038/nrn3171 · DOI · Paper page
  122. Uhlhaas, P. J., and Singer, W. (2006). Neural synchrony in brain disorders: relevance for cognitive dysfunctions and pathophysiology. Neuron 52, 155-168. doi: 10.1016/j.neuron.2006.09.020 · DOI · Paper page
  123. Uhlhaas, P. J., and Singer, W. (2012). Neuronal dynamics and neuropsychiatric disorders: toward a translational paradigm for dysfunctional large-scale networks. Neuron 75, 963-980. doi: 10.1016/j.neuron.2012.09.004 · DOI · Paper page
  124. Uylings, H. B., and van Eden, C. G. (1990). Qualitative and quantitative comparison of the prefrontal cortex in rat and in primates, including humans. Prog. Brain Res. 85, 31-62. doi: 10.1016/S0079-6123(08)62675-8 · DOI
  125. Varela, F., Lachaux, J. P., Rodriguez, E., and Martinerie, J. (2001). The brainweb: phase synchronization and large-scale integration. Nat. Rev. Neurosci. 2, 229-239. doi: 10.1038/35067550 · DOI · Paper page
  126. Vertes, R. P. (2006). Interactions among the medial prefrontal cortex, hippocampus and midline thalamus in emotional and cognitive processing in the rat. Neuroscience 142, 1-20. doi: 10.1016/j.neuroscience.2006.06.027 · DOI
  127. Volk, D. W., and Lewis, D. A. (2010). ''Prefrontal cortical circuits in schizophrenia,'' in Behavioral Neurobiology of Schizophrenia and Its Treatment, ed. N. R. Swerdlow (Berlin, Heidelberg: Springer), 485-508.
  128. Wang, G.-W., and Cai, J.-X. (2006). Disconnection of the hippocampal-prefrontal cortical circuits impairs spatial working memory performance in rats. Behav. Brain Res. 175, 329-336. doi: 10.1016/j.bbr.2006.09.002 · DOI
  129. Weinberger, D. R., Berman, K. F., Suddath, R., and Torrey, E. F. (1992). Evidence of dysfunction of a prefrontal-limbic network in schizophrenia: a magnetic resonance imaging and regional cerebral blood flow study of discordant monozygotic twins. Am. J. Psychiatry 149, 890-897. doi: 10.1176/ajp. 149.7.890 · DOI
  130. Wierzynski, C. M., Lubenov, E. V., Gu, M., and Siapas, A. G. (2009). State- dependent spike-timing relationships between hippocampal and prefrontal circuits during sleep. Neuron 61, 587-596. doi: 10.1016/j.neuron.2009.01.011 · DOI · Paper page
  131. Winton-Brown, T. T., Fusar-Poli, P., Ungless, M. A., and Howes, O. D. (2014). Dopaminergic basis of salience dysregulation in psychosis. Trends Neurosci. 37, 85-94. doi: 10.1016/j.tins.2013.11.003 · DOI · Paper page
  132. Yamamoto, J., Suh, J., Takeuchi, D., and Tonegawa, S. (2014). Successful execution of working memory linked to synchronized high-frequency gamma oscillations. Cell 157, 845-857. doi: 10.1016/j.cell.2014.04.009 · DOI
  133. Yoon, T., Okada, J., Jung, M. W., and Kim, J. J. (2008). Prefrontal cortex and hippocampus subserve different components of working memory in rats. Learn. Mem. 15, 97-105. doi: 10.1101/lm.850808 · DOI
  134. Yu, J. Y., and Frank, L. M. (2015). Hippocampal-cortical interaction in decision making. Neurobiol. Learn. Mem. 117, 34-41. doi: 10.1016/j.nlm.2014.02.002 · DOI
  135. Zhou, Y., Shu, N., Liu, Y., Song, M., Hao, Y., Liu, H., et al. (2008). Altered resting- state functional connectivity and anatomical connectivity of hippocampus in schizophrenia. Schizophr. Res. 100, 120-132. doi: 10.1016/j.schres.2007.11.039 · DOI

Authors
Sigurdsson, T., & Duvarci, S.
Affiliations
Goethe University Frankfurt (DE)
Corresponding author
Sigurdsson, Torfi
ORCID
Venue
Frontiers in Systems Neuroscience
Publisher
Frontiers Media SA
Published
2016-01-26
Volume
9
Pages
190-190
ISSN
1662-5137 (ISSN-L)
DOI
10.3389/fnsys.2015.00190
PMC
PMC4727104
OpenAlex
W2279555465
Cited by
309
References
166
Citations by year
2026: 17 · 2025: 43 · 2024: 39 · 2023: 33 · 2022: 39 · 2021: 44 · 2020: 29 · 2019: 18 · 2018: 20 · 2017: 18 · 2016: 9
FWCI
2.29
Type
journal article
Language
en
Open access
Licence
cc-by
Locations
  • Frontiers in Systems Neuroscience (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
Deutsche Forschungsgemeinschaft (SI 1942/1-1, DU 1433/1)
Topics
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
  • Health Sciences › Medicine › Psychiatry and Mental health › Schizophrenia research and treatment
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
Keywords
hippocampus, prefrontal cortex, schizophrenia, animal models of schizophrenia, cognitive function, behavioral functioning, risk factors

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review