Spatial memory formation differentially affects c-Fos expression in retrosplenial areas during place avoidance training in rats

Publications

Share / Export Citation / Email / Print / Text size:

Acta Neurobiologiae Experimentalis

Nencki Institute of Experimental Biology

Polish Neuroscience Society

Subject: Behavioral Sciences , Biomedical Sciences & Nutrition , Life Sciences , Medicine , Neurosciences

GET ALERTS

ISSN: 0065-1400
eISSN: 1689-0035

DESCRIPTION

0
Reader(s)
0
Visit(s)
0
Comment(s)
0
Share(s)

SEARCH WITHIN CONTENT

FIND ARTICLE

Volume / Issue / page

Related articles

VOLUME 76 , ISSUE 3 (September 2016) > List of articles

Advertisement Spatial memory formation differentially affects c-Fos expression in retrosplenial areas during place avoidance training in rats

Monika Malinowska * / Monika Niewiadomska / Malgorzata Wesierska

Keywords : granular retrosplenial areas, dysgranular retrosplenial area, c-Fos expression, spatial learning, spatial memory, place avoidance task

Citation Information : Acta Neurobiologiae Experimentalis. Volume 76, Issue 3, Pages 244-256, DOI: https://doi.org/10.21307/ane-2017-024

License : (CC BY 4.0)

Published Online: 01-August-2017

ARTICLE

ABSTRACT

The retrosplenial cortex is involved in spatial memory function, but the contribution of its individual areas is not well known. To elucidate the involvement of retrosplenial cortical areas 29c and 30 in spatial memory, we analyzed the expression of c-Fos in these areas in the experimental group of rats that were trained in a spatial place avoidance task, i.e. to avoid shocks presented in an unmarked sector of a stable arena under light conditions. Control rats were trained in the same context as the experimental rats either without (Control-noUS) or with shocks (Control-US) that were delivered in a random, noncontingent manner for three days. On the first day of place avoidance learning, the experimental group exhibited c-Fos induction in area 29c, similar to both control groups. In area 30, similarly high levels of c-Fos expression were observed in the experimental and Control-US groups. On the third day of training, when the experimental group efficiently avoided c-Fos expression in areas 29c and 30 was lower compared with the first day of training. In area 29c c-Fos level was also lower in the experimental group in comparison to the Control-US group. In area 30, c-Fos expression in the experimental group was lower than in both control groups. In conclusion, areas 29c and 30 appear to be activated during spatial memory acquisition on the first day of training, whereas area 30 seems suppressed during long-term memory functioning on the third day of training when rats effectively avoid.

Content not available PDF Share

FIGURES & TABLES

REFERENCES

  1. Aggleton JP (2010) Understanding retrosplenial amnesia: Insights from animal studies. Neuropsychologia 48: 2328–2338.
  2. Albasser MM, Poirier GL, Warburton EC, Aggleton JP (2007) Hippocampal lesions halve immediate-early gene protein counts in retrosplenial cortex: distal dysfunctions in a spatial memory system. Eur J Neurosci 26: 1254–1266.
  3. Amin E, Wright N, Poirier GL, Thomas KL, Erichsen JT, Aggleton JP (2010) Selective lamina dysregulation in granular retrosplenial cortex (area 29) after anterior thalamic lesions: An in situ hybridization and trans-neuronal tracing study in rats. Neuroscience 169(3): 1255–1267.
  4. Bergado JA, Lucas M, Richter-Levin G (2011) Emotional tagging-a simple hypothesis in a complex reality. Prog Neurobiol 94(1): 64–76.
  5. Bertaina-Anglade V, Tramu G, Destrade C (2000) Differential learning-stage dependent patterns of c-Fos protein expression in brain regions during the acquisition and memory consolidation of an operant task in mice. Eur J Neurosci 12: 3803–3812.
  6. Brodmann K (1909) Vergleichende Lokalisationslehre der Grosshirnrinde in ihren Prinzipien dargestellt auf Grund des Zellenbauers. (Ed. Brodmann K). Johann Ambrosius Barth, Leipzig, Germany.
  7. Bures J, Fenton AA, 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(1360): 1515–1524.
  8. Chen L, Lin L-H, Barnes C, McNaughton B (1994a) Head-direction cells in the rat posterior cortex. II. Contributions of visual and ideothetic information to the directional firing. Exp Brain Res 101: 24–34.
  9. Chen L, Lin L-H, Green E, Barnes C, McNaughton B (1994b) Head-direction cells in the rat posterior cortex. I. Anatomical distribution and behavioral modulation. Exp Brain Res 101: 8–23.
  10. Cimadevilla JM, Kaminsky Y, Fenton A, Bures J (2000) Passive and active place avoidance as a tool of spatial memory research in rats. J Neurosci Methods 102(2): 155–164.
  11. Czajkowski R, Jayaprakash B, Wiltgen B, Rogerson T, Guzman-Karlsson MC, Barth AL, Trachtenberg JT, Silva AJ (2014) Encoding and storage of spatial information in the retrosplenial cortex. Proc Natl Acad Sci USA 111: 8661–8666.
  12. Dupire A, Kant P, Mons N, Marchand AR, Coutureau E, Dalrymple-Alford J, Wolff M (2013) A role for anterior thalamic nuclei in affective cognition: interaction with environmental conditions. Hippocampus 23: 392–404.
  13. Fenton AA, 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.
  14. Finch DM, Derian EL, Babb TL (1984) Excitatory projection of the rat subicular complex to the cingulate cortex and synaptic integration with thalamic afferents. Brain Res 301: 25–37.
  15. Gabriel M (1980) Interaction of laminae of the cingulate cortex with the anteroventral thalamus during behavioral learning. Science 208(4447): 1050–1052.
  16. Gabriel M (1990) Functions of anterior and posterior cingulate cortex during avoidance learning in rabbits. Prog Brain Res 85: 467–483.
  17. Gabriel M (1993) Discriminative avoidance learning: a model system. In: Neurobiology of Cingulate Cortex and Limbic Thalamus, A Comprehensive Handbook (Vogt BA, Gabriel M, Eds), Birkhauser, Boston, USA, p. 478–523.
  18. Gabriel M, Vogt BA, Kubota Y, Poremba A, Kang E (1991) Training-stage related neuronal plasticity in limbic thalamus and cingulate cortex during learning: a possible key to mnemonic retrieval. Behav Brain Res 46: 175–185.
  19. Garden DLF, Massey PV, Caruana DA, Johnson B, Warburton EC, Aggleton JP, Bashir ZI (2009) Anterior thalamic lesions stop synaptic plasticity in retrosplenial cortex slices: expanding the pathology of diencephalic amnesia. Brain 132: 1847–1857.
  20. Grimm R, Tischmeyer W (1997) Complex patterns of immediate early gene induction in rat brain following brightness discrimination training and pseudotraining. Behav Brain Res 84(1–2): 109–116.
  21. Jenkins TA, Vann SD, Amin E, Aggleton JP (2004) Anterior thalamic lesions stop immediate early gene activation in selective laminae of the retrosplenial cortex: evidence of covert pathology in rats?. Eur J Neurosci 19: 3291–3304.
  22. Jinno S (2009) Structural organization of long-range GABAergic projection system of the hippocampus. Front Neuroanat 3: 13.
  23. Jones BF, Witter MP (2007) Cingulate cortex projections to the parahippocampal region and hippocampal formation in the rat. Hippocampus 17: 957–976.
  24. Kaczmarek L (2000) Gene expression in learning processes. Acta Neurobiol Exp (Wars) 60(3): 419–424.
  25. Kaczmarek L (2002) Immediate early genes and inducible transcription factors in mapping of the central nervous system function and disfunction. In: Handbook of Chemical Neuroanatomy. Vol. 19 (Kaczmarek L, Robertson HA, Eds). Elsevier Science, Amsterdam, Netherlands.
  26. Kubik S, Miyashita T, Kubik-Zahorodna A, Guzowski JF (2012) Loss of activity-dependent Arc gene expression in the retrosplenial cortex after hippocampal inactivation: Interaction in a higher-order memory circuit. Neurobiol Learn Mem 97: 124–131.
  27. Meibach RC, Siegel A (1977) Subicular projections to the posterior cingulate cortex in rats. Exp Neurol 57: 264–274.
  28. Mendez-Lopez M, Arias JL, Bontempi B, Wolff M (2013) Reduced cytochrome oxidase activity in retrosplenial cortex after lesions to the anterior thalamic nuclei. Behav Brain Res 250: 264–273.
  29. Milanovic S, Radulovic J, Laban O, Stiedl O, Henn F, Spiess J (1998) Production of the Fos protein after contextual fear conditioning of C57BL/6N mice. Brain Res 784(1–2): 37–47.
  30. Miyashita T, Rockland KS (2007) GABAergic projections from the hippocampus to the retrosplenial cortex in the rat. Eur J Neurosci 26: 1193–1204.
  31. Nikolaev E, Werka T, Kaczmarek L (1992) C-fos protooncogene expression in rat brain after long-term training of two-way active avoidance reaction. Behav Brain Res 48(1): 91–94.
  32. Pothuizen HHJ, Davies M, Aggleton JP, Vann SD (2010) Effects of selective granular retrosplenial cortex lesions on spatial working memory in rats. Behav Brain Res 208(2): 566–575.
  33. Pothuizen HHJ, Davies M, Albasser MM, Aggleton JP, Vann SD (2009) Granular and dysgranular retrosplenial cortices provide qualitatively different contributions to spatial working memory: evidence from immediate-early gene imaging in rats. Eur J Neurosci 30: 877–888.
  34. Rosen JB, Fanselow MS, Young SL, Sitcoske M, Maren S (1998) Immediate-early gene expression in the amygdala following footshock stress and contextual fear-conditioning. Brain Res 796(1–2): 132–142.
  35. Shibata H (1993) Efferent projections from the anterior thalamic nuclei to the cingulate cortex in the rat. J Comp Neurol 330: 533–542.
  36. Shibata H (1998) Organization of projections of rat retrosplenial cortex to the anterior thalamic nuclei. Eur J Neurosci 10: 3210–3219.
  37. Shibata H, Kondo S, Naito J (2004) Organization of retrosplenial cortical projections to the anterior cingulate, motor, and prefrontal cortices in the rat. Neurosci Res 49(1): 1–11.
  38. Shibata H, Naito J (2008) Organization of anterior cingulate and frontal cortical projections to the retrosplenial cortex in the rat. J Comp Neurol 506(1): 30–45.
  39. Sugar J, Witter MP, Van Strien N, Cappaert N (2011) The retrosplenial cortex: intrinsic connectivity and connections with the (para)hippocampal region in the rat. An interactive connectome. Front Neuroinform 5: 7.
  40. Tischmeyer W, Grimm R (1999) Activation of immediate early genes and memory formation (review). Cell Mol Life Sci 55(4): 564–574.
  41. van Groen T, Kadish I, Wyss JM (2004) Retrosplenial cortex lesions of area Rgb (but not of area Rga) impair spatial learning and memory in the rat. Behav Brain Res 154: 483–491.
  42. van Groen T, Wyss JM (1992) Connections of the retrosplenial dysgranular cortex in the rat. J Comp Neurol 315: 200–216.
  43. van Groen T, Wyss JM (2003) Connections of the retrosplenial granular b cortex in the rat. J Comp Neurol 463: 249–263.
  44. Vann SD, Aggleton JP (2005) Selective dysgranular retrosplenial cortex lesions in rats disrupt allocentric performance of the radial-arm maze task. Behav Neurosci 119: 1682–1686.
  45. Vann SD, Aggleton JP, Maguire EA (2009) What does the retrosplenial cortex do? Nature Rev Neurosci 10(11): 792–802.
  46. Vogt BA (ed.) (1985) Cingulate Cortex. Plenum Press, New York–London.
  47. Vogt BA, Miller MW (1983) Cortical connections between rat cingulate cortex and visual, motor, and postsubicular cortices. J Comp Neurol 216(2): 192–210.
  48. Vogt BA, Paxinos G (2014) Cytoarchitecture of mouse and rat cingulate cortex with human homologies. Brain Struct Funct 29(1): 185–192.
  49. Vogt BA, Peters A (1981) Form and distribution of neurons in rat cingulate cortex: Areas 32, 24, and 29. J Comp Neurol 195: 603–625.
  50. Wesierska M, Adamska I, Malinowska M (2009) Retrosplenial cortex lesion affected segregation of spatial information in place avoidance task in the rat. Neurobiol Learn Mem 91(1): 41–49.
  51. Wesierska M, Dockery C, Fenton AA (2005) Beyond memory, navigation, and inhibition: behavioral evidence for hippocampus-dependent cognitive coordination in the rat. J Neurosci 25(9): 2413–2419.

EXTRA FILES

COMMENTS