Интегративные функции ретросплениальной коры: данные анатомии, коннектомики и клеточной электрофизиологии у крыс

Olga A. Mineeva1, Dmitrii V. Bezryadnov1, Sergey A. Chekhov1, Оlga E. Svarnik2, Konstantin V. Anokhin1
1ФГБНУ «Институт нормальной физиологии им. П.К. Анохина», Москва, Россия; 2ФГБУН «Институт психологии РАН», Москва, Россия

Аннотация


Обзор посвящен интегративным функциям ретросплениальной коры, значительная доля нейронов которой обладает специализацией относительно положения и перемещения организма в пространстве. Разбираются современные данные об анатомии и связях ретросплениальной коры у крыс, а также о поведенческой специализации ее нейронов, обнаруженной с помощью мультиэлектродной регистрации клеточной активности. Паттерн связей ретросплениальной коры позволяет рассматривать ее как своеобразное связующее звено между областями мозга, специфически ответственными за пространственную навигацию и ассоциативными областями коры, не имеющими пространственной настройки. Этой уникальной особенностью анатомических связей ретросплениальной коры, по-видимому, объясняется присутствие в ней нейронов не только с пространственными, но и с более сложными поведенческими специализациями, которые рассмотрены в данном обзоре. Подобные сложно специализированные клетки вероятно должны ассоциировать комбинацию пространственной и непространственной информации, и раскрытие механизмов этой ассоциации может принести новое в понимание принципов организации когнитивных функций коры головного мозга.

 


Ключевые слова

ретросплениальная кора; коннектомика; нейронная активность; поведенческая специализация нейронов; пространственная память; интеграция информации

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Литература

Alivisatos A.P. Andrews A.M., Boyden E.S. et al. Nanotools for neuroscience and brain activity mapping. ACS Publications 2013; 7: 1850–1866. DOI: 10.1021/nn4012847. PMID: 23514423.

Kim C.K., Adhikari A., Deisseroth K. Integration of optogenetics with complementary methodologies in systems neuroscience. Nat Rev Neurosci 2017; 18: 222–235. DOI: 10.1038/nrn.2017.15. PMID: 28303019.

Luo L., Callaway E.M., Svoboda K. Genetic dissection of neural circuits: a decade of progress. Neuron 2018; 98: 256–281. DOI: 10.1016/j.neuron.2018.05.004. PMID: 29772206.

Rivnay J., Wang H., Fenno L. et al. Next-generation probes, particles, and proteins for neural interfacing. Sci Adv 2017; 3: P. e1601649. DOI: 10.1126/sciadv.1601649. PMID: 28630894.

Kandel E. A place and a grid in the sun. Cell 2014; 159: 1239–1242. DOI: 10.1016/j.cell.2014.11.033. PMID: 25480286.

Langmoen I.A., Apuzzo M.L. The brain on itself: nobel laureates and the history of fundamental nervous system function. Neurosurgery 2007; 61: 891–908. DOI: 10.1227/01.neu.0000303185.49555.a9. PMID: 18091266.

Yuste R. From the neuron doctrine to neural networks. Nat Rev Neurosci 2015; 16: 487–497. DOI: 10.1038/nrn3962. PMID: 26152865.

O’Keefe J., Dostrovsky J. The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat. Brain Res 1971; 34: 171–175. DOI: http://dx.doi.org/10.1016/0006-8993(71)90358-1. PMID: 5124915.

Taube J.S., Muller R.U., Ranck J.B. Head-direction cells recorded from the postsubiculum in freely moving rats. I. Description and quantitative analysis. J Neurosci 1990; 10: 420–435. DOI: https://doi.org/10.1523/JNEUROSCI.10-02-00420.1990. PMID: 2303851.

Hafting T., Fyhn M., Molden S. et al. Microstructure of a spatial map in the entorhinal cortex. Nature 2005; 436: 801–806. DOI: 10.1038/nature03721. PMID: 15965463.

Mitchell A.S., Czajkowski R., Zhang N. et al. Retrosplenial cortex and its role in spatial cognition. Brain Neurosci Adv 2018; 2: 2398212818757098. DOI: https://doi.org/10.1177/2398212818757098. PMID: 30221204.

Lavenex P., Amaral D.G. Hippocampal-neocortical interaction: a hierarchy of associativity. Hippocampus 2000; 10: 420–430. DOI: 10.1002/1098-1063(2000)10:4<420::AID-HIPO8>3.0.CO;2-5. PMID: 10985281.

Sewards T.V., Sewards M.A. Input and output stations of the entorhinal cortex: superficial vs. deep layers or lateral vs. medial divisions? Brain Res Brain Res Rev 2003; 42: 243–251. DOI: https://doi.org/10.1016/S0165-0173(03)00175-9. PMID: 12791442.

Harker K.T., Whishaw I.Q. Impaired place navigation in place and matching-to-place swimming pool tasks follows both retrosplenial cortex lesions and cingulum bundle lesions in rats. Hippocampus 2004; 14: 224–231. DOI: 10.1002/hipo.10159. PMID: 15098727.

Pothuizen H.H.J., Davies M., Aggleton J.P., Vann S.D. Effects of selective granular retrosplenial cortex lesions on spatial working memory in rats. Behav Brain Res 2010; 208: 566–575. DOI: 10.1016/j.bbr.2010.01.001. PMID: 20074589.

Vann S.D., Aggleton J.P. Extensive cytotoxic lesions of the rat retrosplenial cortex reveal consistent deficits on tasks that tax allocentric spatial memory. Behav Neurosci 2002; 116: 85–94. DOI: DOI: 10.1037//0735-7044.116.1.85. PMID: 11895186.

Cooper B.G., Mizumori S.J. Retrosplenial cortex inactivation selectively impairs navigation in darkness. Neuroreport 1999; 10: 625–630. PMID: 10208601.

Elduayen C., Save E. The retrosplenial cortex is necessary for path integration in the dark. Behav Brain Res 2014; 272: 303–307. DOI: 10.1016/j.bbr.2014.07.009. PMID: 25026093.

Miller A.M.P., Vedder L.C., Law L.M., Smith D.M. Cues, context, and long-term memory: the role of the retrosplenial cortex in spatial cognition. Front Hum Neurosci 2014; 8: 586. DOI: 10.3389/fnhum.2014.00586. PMID: 25140141.

Epstein R.A., Patai E.Z., Julian J.B., Spiers H.J. The cognitive map in humans: spatial navigation and beyond. Nat Neurosci 2017; 20: 1504–1513. DOI: 10.1038/nn.4656. PMID: 29073650.

Epstein R.A. Parahippocampal and retrosplenial contributions to human spatial navigation. Trends Cogn Sci 2008; 12: 388–396. DOI: 10.1016/j.tics.2008.07.004. PMID: 18760955.

An Y., Varma V.R., Varma S. et al. Evidence for brain glucose dysregulation in Alzheimer’s disease. Alzheimers Dement. 2018; 14: 318–329. DOI: 10.1016/j.jalz.2017.09.011. PMID: 29055815.

Minoshima S., Giordani B., Berent S. et al. Metabolic reduction in the posterior cingulate cortex in very early Alzheimer’s disease. Ann Neurol 1997; 42: 85–94. DOI: 10.1002/ana.410420114. PMID: 9225689.

Nestor P.J., Fryer T.D., Ikeda M., Hodges J.R. Retrosplenial cortex (BA 29/30) hypometabolism in mild cognitive impairment (prodromal Alzheimer’s disease). Eur J Neurosci 2003; 18: 2663–2667. DOI: https://doi.org/10.1046/j.1460-9568.2003.02999.x. PMID: 14622168.

Pengas G., Hodges J.R., Watson P., Nestor P.J. Focal posterior cingulate atrophy in incipient Alzheimer’s disease. Neurobiol Aging 2010; 31: 25–33. DOI: 10.1016/j.neurobiolaging.2008.03.014. PMID: 18455838.

Pengas G., Williams G.B., Acosta-Cabronero J. et al. The relationship of topographical memory performance to regional neurodegeneration in Alzheimer’s disease. Front Aging Neurosci 2012; 4: 17. DOI: 10.3389/fnagi.2012.00017. PMID: 22783190.

Teipel S., Grothe M.J., Alzheimer’s Disease Neuroimaging Initiative. Does posterior cingulate hypometabolism result from disconnection or local pathology across preclinical and clinical stages of Alzheimer’s disease? Eur J Nucl Med Mol Imaging 2016; 43: 526–536. DOI: 10.1007/s00259-015-3222-3. PMID: 26555082.

Tu S., Wong S., Hodges J.R. et al. Lost in spatial translation — A novel tool to objectively assess spatial disorientation in Alzheimer’s disease and frontotemporal dementia. Cortex J Devoted Study Nerv Syst Behav 2015; 67: 83–94. DOI: 10.1016/j.cortex.2015.03.016. PMID: 25913063.

Villain N., Desgranges B., Viader F. et al. Relationships between hippocampal atrophy, white matter disruption, and gray matter hypometabolism in Alzheimer’s disease. J Neurosci 2008; 28: 6174–6181. DOI: 10.1523/JNEUROSCI.1392-08.2008. PMID: 18550759.

Yasuno F., Kazui H., Yamamoto A. et al. Resting-state synchrony between the retrosplenial cortex and anterior medial cortical structures relates to memory complaints in subjective cognitive impairment. Neurobiol Aging 2015; 36: 2145–2152. DOI: 10.1016/j.neurobiolaging.2015.03.006. PMID: 25862421.

Sugar J., Witter M.P., van Strien N.M., Cappaert N.L. The retrosplenial cortex: intrinsic connectivity and connections with the (para)hippocampal region in the rat. An interactive connectome. Front Neuroinformatics 2011; 5: 7. DOI: 10.3389/fninf.2011.00007. PMID: 21847380.

Paxinos G., Watson C. The Rat Brain in Stereotaxic Coordinates in Stereotaxic Coordinates. London: Elsevier, 2007.

Lau C., Ng L., Thompson C. et al. Exploration and visualization of gene expression with neuroanatomy in the adult mouse brain. BMC Bioinformatics 2008; 9: 153. DOI: 10.1186/1471-2105-9-153. PMID: 18366675.

Wyss J.M., Van Groen T., Sripanidkulchai K. Dendritic bundling in layer I of granular retrosplenial cortex: intracellular labeling and selectivity of innervation. J Comp Neurol 1990; 295: 33–42. DOI: 10.1002/cne.902950104. PMID: 2341634.

Jones B.F., Groenewegen H.J., Witter M.P. Intrinsic connections of the cingulate cortex in the rat suggest the existence of multiple functionally segregated networks. Neuroscience 2005; 133: 193–207. DOI: 10.1016/j.neuroscience.2005.01.063. PMID: 15893643.

Shibata H., Honda Y., Sasaki H., Naito J. Organization of intrinsic connections of the retrosplenial cortex in the rat. Anat Sci Int 2009; 84: 280–292. DOI: 10.1007/s12565-009-0035-0. PMID: 19322631.

Van Groen T., Wyss J.M. Connections of the retrosplenial granular b cortex in the rat. J Comp Neurol 2003; 463: 249–263. DOI: 10.1002/cne.10757. PMID: 12820159.

Van Groen T., Wyss J.M. Connections of the retrosplenial granular a cortex in the rat. J Comp Neurol 1990; 300: 593–606. DOI: 10.1002/cne.903000412. PMID: 2273095.

Miyashita T., Rockland K.S. GABAergic projections from the hippocampus to the retrosplenial cortex in the rat. Eur J Neurosci 2007; 26: 1193–1204. DOI: 10.1111/j.1460-9568.2007.05745.x. PMID: 17767498.

Shibata H. Terminal distribution of projections from the retrosplenial area to the retrohippocampal region in the rat, as studied by anterograde transport of biotinylated dextran amine. Neurosci Res 1994; 20: 331–336. DOI: https://doi.org/10.1016/0168-0102(94)90055-8. PMID: 7532841.

Naber P.A., Witter M.P. Subicular efferents are organized mostly as parallel projections: a double-labeling, retrograde-tracing study in the rat. J Comp Neurol 1998; 393: 284–297. DOI: https://doi.org/10.1002/(SICI)1096-9861(19980413)393:3<284::AID-CNE2>3.0.CO;2-Y. PMID: 9548550.

Köhler C. Intrinsic projections of the retrohippocampal region in the rat brain. I. The subicular complex. J Comp Neurol 1985; 236: 504–522. DOI: 10.1002/cne.902360407. PMID: 3902916.

Vogt B.A., Miller M.W. Cortical connections between rat cingulate cortex and visual, motor, and postsubicular cortices. J Comp Neurol 1983; 216: 192–210. DOI: 10.1002/cne.902160207. PMID: 6863602.

Jun J.J., Steinmetz N.A., Siegle J.H. et al. Fully integrated silicon probes for high-density recording of neural activity. Nature 2017; 551: 232–236. DOI: 10.1038/nature24636. PMID: 29120427.

Beggs J.M., Moyer J.R. Jr, McGann J.P., Brown T.H. Prolonged synaptic integration in perirhinal cortical neurons. J Neurophysiol 2000; 83: 3294–3298. DOI: 10.1152/jn.2000.83.6.3294. PMID: 10848549.

McGann J.P., Moyer J.R., Brown T.H. Predominance of late-spiking neurons in layer VI of rat perirhinal cortex. J Neurosci 2001; 21: 4969–4976. DOI: https://doi.org/10.1523/JNEUROSCI.21-14-04969.2001. PMID: 11438572.

Kurotani T., Miyashita T., Wintzer M. et al. Pyramidal neurons in the superficial layers of rat retrosplenial cortex exhibit a late-spiking firing property. Brain Struct Funct 2013; 218: 239–254. DOI: 10.1007/s00429-012-0398-1. PMID: 22383041.

Alexander A.S., Nitz D.A. Retrosplenial cortex maps the conjunction of internal and external spaces. Nat Neurosci 2015; 18: 1143–1151. DOI: 10.1038/nn.4058. PMID: 26147532.

Chen L.L., Lin L.H., Green E.J. et al. Head-direction cells in the rat posterior cortex. I. Anatomical distribution and behavioral modulation. Exp Brain Res 1994; 101: 8–23. DOI: https://doi.org/10.1007/BF00243212. PMID: 7843305.

Chen L.L., Lin L.H., Barnes C.A., McNaughton B.L. Head-direction cells in the rat posterior cortex. II. Contributions of visual and ideothetic information to the directional firing. Exp Brain Res 1994; 101: 24–34. DOI: 10.1007/BF00243213. PMID: 7843299.

Cho J., Sharp P.E. Head direction, place, and movement correlates for cells in the rat retrosplenial cortex. Behav Neurosci 2001; 115: 3–25. PMID: 11256450.

Jacob P.-Y., Casali G., Spieser L. et al. An independent, landmark-dominated head-direction signal in dysgranular retrosplenial cortex. Nat Neurosci 2017; 20: 173–175. DOI: 10.1038/nn.4465. PMID: 27991898.

Alexander A.S., Nitz D.A. Spatially periodic activation patterns of retrosplenial cortex encode route sub-spaces and distance traveled. Curr Biol 2017; 27: 1551–1560.e4. DOI: 10.1016/j.cub.2017.04.036. PMID: 28528904.

Smith D.M., Barredo J., Mizumori S.J.Y. Complimentary roles of the hippocampus and retrosplenial cortex in behavioral context discrimination. Hippocampus 2012; 22: 1121–1133. DOI: 10.1002/hipo.20958. PMID: 21630374.

Navratilova Z., Hoang L.T., Schwindel C.D. et al. Experience-dependent firing rate remapping generates directional selectivity in hippocampal place cells. Front Neural Circuits 2012; 6: 6. DOI: 10.3389/fncir.2012.00006. PMID: 22363267




DOI: http://dx.doi.org/10.25692/ACEN.2019.1.6