Transient Inactivation of the Medial Prefrontal Cortex and Ventral Hippocampus Impairs Active Place Avoidance Retrieval on a Rotating Arena

. 2021 ; 15 () : 634533. [epub] 20210428

Jazyk angličtina Země Švýcarsko Médium electronic-ecollection

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid33994956

It is well known that communication between the medial prefrontal cortex (mPFC) and the ventral hippocampus (vHPC) is critical for various cognitive and behavioral functions. However, the exact role of these structures in spatial coordination remains to be clarified. Here we sought to determine the involvement of the mPFC and the vHPC in the spatial retrieval of a previously learned active place avoidance task in adult male Long-Evans rats, using a combination of unilateral and bilateral local muscimol inactivations. Moreover, we tested the role of the vHPC-mPFC pathway by performing combined ipsilateral and contralateral inactivations. Our results showed not only bilateral inactivations of either structure, but also the combined inactivations impaired the retrieval of spatial memory, whereas unilateral one-structure inactivations did not yield any effect. Remarkably, muscimol injections in combined groups exerted similar deficits, regardless of whether the inactivations were contralateral or ipsilateral. These findings confirm the importance of these structures in spatial cognition and emphasize the importance of the intact functioning of the vHPC-mPFC pathway.

Zobrazit více v PubMed

Adams R. A., Bush D., Zheng F., Meyer S. S., Kaplan R., Orfanos S., et al. (2020). Impaired theta phase coupling underlies frontotemporal dysconnectivity in schizophrenia. Brain 143 1261–1277. 10.1093/brain/awaa035 PubMed DOI PMC

Bahník Š. (2014). Carousel Maze Manager (Version 0.4.0) Software. Available online at: https://github.com/bahniks/CM_Manager_0_4_0 (accessed November 28, 2020).

Bannerman D. M., Grubb M., Deacon R. M. J., Yee B. K., Feldon J., Rawlins J. N. P. (2003). Ventral hippocampal lesions affect anxiety but not spatial learning. Behav. Brain Res. 139 197–213. 10.1016/s0166-4328(02)00268-1 PubMed DOI

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. 10.1016/j.neubiorev.2004.03.004 PubMed DOI

Bast T., Zhang W. N., Feldon J. (2001). Hyperactivity, decreased startle reactivity, and disrupted prepulse inhibition following disinhibition of the rat ventral hippocampus by the GABA(A) receptor antagonist picrotoxin. Psychopharmacology (Berl) 156 225–233. 10.1007/s002130100775 PubMed DOI

Birrell J. M., Brown V. J. (2000). Medial frontal cortex mediates perceptual attentional set shifting in the rat. J. Neurosci. 20 4320–4324. 10.1523/jneurosci.20-11-04320.2000 PubMed DOI PMC

Boulougouris V., Dalley J. W., Robbins T. W. (2007). Effects of orbitofrontal, infralimbic and prelimbic cortical lesions on serial spatial reversal learning in the rat. Behav. Brain Res. 179 219–228. 10.1016/j.bbr.2007.02.005 PubMed DOI

Broadbent N. J., Squire L. R., Clark R. E. (2004). Spatial memory, recognition memory, and the hippocampus. Proc. Natl. Acad. Sci. U.S.A. 101 14515–14520. 10.1073/pnas.0406344101 PubMed DOI PMC

Bures J., Fenton A. A., Kaminsky Y., Rossier J., Sacchetti B., Zinyuk L. (1997). Dissociation of exteroceptive and idiothetic orientation cues: effect on hippocampal place cells and place navigation. Philos. Trans. R. Soc. Lond. B Biol. Sci. 352 1515–1524. 10.1098/rstb.1997.0138 PubMed DOI PMC

Cholvin T., Loureiro M., Cassel R., Cosquer B., Herbeaux K., de Vasconcelos A. P., et al. (2016). Dorsal hippocampus and medial prefrontal cortex each contribute to the retrieval of a recent spatial memory in rats. Brain Struct. Funct. 221 91–102. 10.1007/s00429-014-0894-6 PubMed DOI

Churchwell J. C., Morris A. M., Musso N. D., Kesner R. P. (2010). Prefrontal and hippocampal contributions to encoding and retrieval of spatial memory. Neurobiol. Learn. Mem. 93 415–421. 10.1016/j.nlm.2009.12.008 PubMed DOI

Cimadevilla J. M., Wesierska M., Fenton A. A., Bures J. (2001). Inactivating one hippocampus impairs avoidance of a stable room-defined place during dissociation of arena cues from room cues by rotation of the arena. Proc. Natl. Acad. Sci. U.S.A. 98 3531–3536. 10.1073/pnas.051628398 PubMed DOI PMC

de Hoz L., Knox J., Morris R. G. M. (2003). Longitudinal axis of the hippocampus: both septal and temporal poles of the hippocampus support water maze spatial learning depending on the training protocol. Hippocampus 13 587–603. 10.1002/hipo.10079 PubMed DOI

Fenton A. A., Wesierska M., Kaminsky Y., Bures J. (1998). Both here and there: simultaneous expression of autonomous spatial memories in rats. Proc. Natl. Acad. Sci. U.S.A. 95 11493–11498.10.1073/pnas.95.19.11493 PubMed DOI PMC

Ferbinteanu J., Ray C., McDonald R. J. (2003). Both dorsal and ventral hippocampus contribute to spatial learning in Long-Evans rats. Neurosci. Lett. 345 131–135. 10.1016/s0304-3940(03)00473-7 PubMed DOI

Floresco S. B., Block A. E., Tse M. T. L. (2008). Inactivation of the medial prefrontal cortex of the rat impairs strategy set-shifting, but not reversal learning, using a novel, automated procedure. Behav. Brain Res. 190 85–96. 10.1016/j.bbr.2008.02.008 PubMed DOI

Floresco S. B., Seamans J. K., Phillips A. G. (1997). Selective roles for hippocampal, prefrontal cortical, and ventral striatal circuits in radial-arm maze tasks with or without a delay. J. Neurosci. 17 1880–1890. 10.1523/jneurosci.17-05-01880.1997 PubMed DOI PMC

Hamilton D. A., Brigman J. L. (2015). Behavioral flexibility in rats and mice: contributions of distinct frontocortical regions. Genes Brain Behav. 14 4–21. 10.1111/gbb.12191 PubMed DOI PMC

Herman J. P., Cullinan W. E., Young E. A., Akil H., Watson S. J. (1992). Selective forebrain fiber tract lesions implicate ventral hippocampal structures in tonic regulation of paraventricular nucleus corticotropin-releasing hormone (CRH) and arginine vasopressin (AVP) mRNA expression. Brain Res. 592 228–238. 10.1016/0006-8993(92)91680-D PubMed DOI

Hoover W. B., Vertes R. P. (2007). Anatomical analysis of afferent projections to the medial prefrontal cortex in the rat. Brain Struct. Funct. 212 149–179. 10.1007/s00429-007-0150-4 PubMed DOI

Jay T. M., Glowinski J., Thierry A. M. (1989). Selectivity of the hippocampal projection to the prelimbic area of the prefrontal cortex in the rat. Brain Res. 505 337–340. 10.1016/0006-8993(89)91464-9 PubMed DOI

Jo Y. S., Park E. H., Kim I. H., Park S. K., Kim H., Kim H. T., et al. (2007). The medial prefrontal cortex is involved in spatial memory retrieval under partial-cue conditions. J. Neurosci. 27 13567–13578. 10.1523/JNEUROSCI.3589-07.2007 PubMed DOI PMC

Jones M. W., Wilson M. A. (2005). Theta rhythms coordinate hippocampal-prefrontal interactions in a spatial memory task. PLoS Biol. 3:e402. 10.1371/journal.pbio.0030402 PubMed DOI PMC

Kelemen E., Fenton A. A. (2010). Dynamic grouping of hippocampal neural activity during cognitive control of two spatial frames. PLoS Biol. 8:e1000403. 10.1371/journal.pbio.1000403 PubMed DOI PMC

Kubík S., Fenton A. A. (2005). Behavioral evidence that segregation and representation are dissociable hippocampal functions. J. Neurosci. 25 9205–9212. 10.1523/JNEUROSCI.1707-05.2005 PubMed DOI PMC

Kubík S., Stuchlík A., Fenton A. A. (2006). Evidence for hippocampal role in place avoidance other than merely memory storage. Physiol. Res. 55 445–452. PubMed

Lee S. L. T., Lew D., Wickenheisser V., Markus E. J. (2019). Interdependence between dorsal and ventral hippocampus during spatial navigation. Brain Behav. 9:e01410. 10.1002/brb3.1410 PubMed DOI PMC

Leon W. C., Bruno M. A., Allard S., Nader K., Cuello A. C. (2010). Engagement of the PFC in consolidation and recall of recent spatial memory. Learn. Mem. 17 297–305. 10.1101/lm.1804410 PubMed DOI

Loureiro M., Lecourtier L., Engeln M., Lopez J., Cosquer B., Geiger K., et al. (2012). The ventral hippocampus is necessary for expressing a spatial memory. Brain Struct. Funct. 217 93–106. 10.1007/s00429-011-0332-y PubMed DOI

Malá H., Andersen L. G., Christensen R. F., Felbinger A., Hagstrøm J., Meder D., et al. (2015). Prefrontal cortex and hippocampus in behavioural flexibility and posttraumatic functional recovery: reversal learning and set-shifting in rats. Brain Res. Bull. 116 34–44. 10.1016/j.brainresbull.2015.05.006 PubMed DOI

Martin J. H. (1991). Autoradiographic estimation of the extent of reversible inactivation produced by microinjection of lidocaine and muscimol in the rat. Neurosci. Lett. 127 160–164. 10.1016/0304-3940(91)90784-q PubMed DOI

Moser E., Moser M. B., Andersen P. (1993). Spatial learning impairment parallels the magnitude of dorsal hippocampal lesions, but is hardly present following ventral lesions. J. Neurosci. 13 3916–3925. 10.1523/jneurosci.13-09-03916.1993 PubMed DOI PMC

Moser M. B., Moser E. I., Forrest E., Andersen P., Morris R. G. (1995). Spatial learning with a minislab in the dorsal hippocampus. Proc. Natl. Acad. Sci. U.S.A. 92 9697–9701. 10.1073/pnas.92.21.9697 PubMed DOI PMC

Olypher A. V., Klement D., Fenton A. A. (2006). Cognitive disorganization in hippocampus: a physiological model of the disorganization in psychosis. J. Neurosci. 26 158–168. 10.1523/JNEUROSCI.2064-05.2006 PubMed DOI PMC

Park E. H., O’Reilly K. C., Taborga D., Nicholas K., Ahmed A. S., Ruiz N., et al. (2019). Is the rat prefrontal cortex crucial for cognitive control during spatial cognition? Neuroscience. (preprint). 10.1101/2019.12.20.884262 DOI

Paxinos G., Watson C. (2007). The Rat Brain in Stereotaxic Coordinates. Amsterdam: Elsevier. PubMed

Pothuizen H. H. J., Zhang W.-N., Jongen-Rêlo A. L., Feldon J., Yee B. K. (2004). Dissociation of function between the dorsal and the ventral hippocampus in spatial learning abilities of the rat: a within-subject, within-task comparison of reference and working spatial memory. Eur. J. Neurosci. 19 705–712. 10.1111/j.0953-816x.2004.03170.x PubMed DOI

Potvin O., Allen K., Thibaudeau G., Doré F. Y., Goulet S. (2006). Performance on spatial working memory tasks after dorsal or ventral hippocampal lesions and adjacent damage to the subiculum. Behav. Neurosci. 120 413–422. 10.1037/0735-7044.120.2.413 PubMed DOI

Ragozzino M. E., Detrick S., Kesner R. P. (1999). Involvement of the prelimbic-infralimbic areas of the rodent prefrontal cortex in behavioral flexibility for place and response learning. J. Neurosci. 19 4585–4594. 10.1523/jneurosci.19-11-04585.1999 PubMed DOI PMC

Seamans J. K., Floresco S. B., Phillips A. G. (1998). D1 receptor modulation of hippocampal-prefrontal cortical circuits integrating spatial memory with executive functions in the rat. J. Neurosci. 18 1613–1621. 10.1523/jneurosci.18-04-01613.1998 PubMed DOI PMC

Stuchlík A., Petrásek T., Prokopová I., Holubová K., Hatalová H., Valeš K., et al. (2013). Place avoidance tasks as tools in the behavioral neuroscience of learning and memory. Physiol. Res. 62(Suppl. 1) S1–S19. 10.1111/j.1460-9568.2012.08066.x PubMed DOI

Svoboda J., Stankova A., Entlerova M., Stuchlik A. (2015a). Acute administration of MK-801 in an animal model of psychosis in rats interferes with cognitively demanding forms of behavioral flexibility on a rotating arena. Front. Behav. Neurosci. 9:75. 10.3389/fnbeh.2015.00075 PubMed DOI PMC

Svoboda J., Telensky P., Blahna K., Vodicka M., Stuchlik A. (2015b). The role of rat posterior parietal cortex in coordinating spatial representations during place avoidance in dissociated reference frames on a continuously rotating arena (Carousel). Behav. Brain Res. 292 1–9. 10.1016/j.bbr.2015.05.008 PubMed DOI

Wang G.-W., Cai J.-X. (2006). Disconnection of the hippocampal-prefrontal cortical circuits impairs spatial working memory performance in rats. Behav. Brain Res. 175 329–336. 10.1016/j.bbr.2006.09.002 PubMed DOI

Wang J., Bast T., Wang Y.-C., Zhang W.-N. (2015). Hippocampus and two-way active avoidance conditioning: contrasting effects of cytotoxic lesion and temporary inactivation. Hippocampus 25 1517–1531. 10.1002/hipo.22471 PubMed DOI

Wesierska M., Dockery C., Fenton A. A. (2005). Beyond memory, navigation, and inhibition: behavioral evidence for hippocampus-dependent cognitive coordination in the rat. J. Neurosci. 25 2413–2419. 10.1523/JNEUROSCI.3962-04.2005 PubMed DOI PMC

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...