Differential cortical c-Fos and Zif-268 expression after object and spatial memory processing in a standard or episodic-like object recognition task

Barbosa, Flávio Freitas; Santos, José Ronaldo; Meurer, Ywlliane S. Rodrigues; Macêdo, Priscila Tavares; Ferreira, Luane M. Stamatto; Pontes, Isabella M. Oliveira; Ribeiro, Alessandra Mussi; Silva, Regina Helena

doi:10.3389/fnbeh.2013.00112

Cited by 79Memory and Neural MechanismsMemory Processes and InfluencesNeurogenesis and neuroplasticity mechanisms

Differential cortical c-Fos and Zif-268 expression after object and spatial memory processing in a standard or episodic-like object recognition task

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Barbosa, Flávio Freitas, Santos, José Ronaldo, Meurer, Ywlliane S. Rodrigues, Macêdo, Priscila Tavares, Ferreira, Luane M. Stamatto, Pontes, Isabella M. Oliveira, Ribeiro, Alessandra Mussi, Silva, Regina Helena·2013·Frontiers in Behavioral Neuroscience

DOI 10.3389/fnbeh.2013.00112PMC PMC3749513

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Abstract

Episodic memory reflects the capacity to recollect what, where, and when a specific event happened in an integrative manner. Animal studies have suggested that the medial temporal lobe and the medial pre-frontal cortex are important for episodic-like memory (ELM) formation. The goal of present study was to evaluate whether there are different patterns of expression of the immediate early genes c-Fos and Zif-268 in these cortical areas after rats are exposed to object recognition (OR) tasks with different cognitive demands. Male rats were randomly assigned to five groups: home cage control, empty open field (CTR-OF), open field with one object (CTR-OF + Obj), novel OR task, and ELM task and were killed 1 h after the last behavioral procedure. Rats were able to discriminate the objects in the OR task. In the ELM task, rats showed spatial (but not temporal) discrimination of the objects. We found an increase in the c-Fos expression in the dorsal dentate gyrus (DG) and in the perirhinal cortex (PRh) in the OR and ELM groups. The OR group also presented an increase of c-Fos expression in the medial prefrontal cortex (mPFC). Additionally, the OR and ELM groups had increased expression of Zif-268 in the mPFC. Moreover, Zif-268 was increased in the dorsal CA1 and PRh only in the ELM group. In conclusion, the pattern of activation was different in tasks with different cognitive demands. Accordingly, correlation tests suggest the engagement of different neural networks in the tasks used. Specifically, perirhinal-DG co-activation was detected after the what-where memory retrieval, but not after the novel OR task. Both regions correlated with the respective behavioral outcome. These findings can be helpful in the understanding of the neural networks underlying memory tasks with different cognitive demands.

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The replicability of the ELM2-2 and ELM2-1 tests is verified by independent laboratories.
“The replicability of the ELM2–2 and ELM2–1 tests is verified by independent laboratories (Barbosa et al., 2013; Castilla-Ortega et al., 2012; Castilla-Ortega et al., 2014; Drieskens et al., 2017; Fernandez and Garner, 2008; Inostroza et al., 2013a; Inostroza et al., 2013b; Lanté et al., 2015; Li and Chao, 2008; Lopez-Pigozzi et al., 2016; Wang et al., 2010).”
From The medial prefrontal cortex - hippocampus circuit that integrates information of object, place and time to construct episodic memory in rodents: Behavioral, anatomical and neurochemical properties (2020) · cites this paper as Barbosa et al., 2013
Rats retain 'what-where-when' memory for up to 24 hours in the ELM2-1 test.
“Other studies have shown rats to retain “what-where-when” memory for up to 24 hours in the ELM2–1 test (Barbosa et al., 2010; Barbosa et al., 2013).”
From The medial prefrontal cortex - hippocampus circuit that integrates information of object, place and time to construct episodic memory in rodents: Behavioral, anatomical and neurochemical properties (2020) · cites this paper as Barbosa et al., 2013
Increased zif-268 expression was found in the dorsal CA1 after exposure to the ELM2-2 paradigm in which rats showed intact where but not when component.
“Increased zif-268 expression was found in the dorsal CA1 after exposure to the ELM2–2 paradigm in which rats showed intact where, but not when component”
From The medial prefrontal cortex - hippocampus circuit that integrates information of object, place and time to construct episodic memory in rodents: Behavioral, anatomical and neurochemical properties (2020) · cites this paper as Barbosa et al., 2013

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“In this task, we expected that rats would spend more time exploring the displaced recent object when compared to the stationary recent object, and the opposite pattern is expected to the old familiar objects (Kart-Teke et al., 2006, 2007; Li and Chao, 2008).”
Background
Neural Correlates of Object-in-Place Learning in Hippocampus and Prefrontal Cortex
Kim, J., Delcasso, S., & Lee, I. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.2859-11.2011 · Cited by 91 · see citing works
The medial and lateral entorhinal cortex both contribute to contextual and item recognition memory: A test of the binding ofitems and context model
Hunsaker, M. R., Chen, V., Tran, G. T., & Kesner, R. P. (2013) · Hippocampus · doi:10.1002/hipo.22097 · Cited by 88 · cited 2× · see citing works
“…proposes that item memory (what) is processed preferentially in the PRh cortex (and the lateral ERH) and that the contextual information is processed initially in the medial ERH, while item and contextual elements would be bound together in the HP (Eichenbaum et al., 2007; Hunsaker et al., 2013).”
Background
Engagement of the PFC in consolidation and recall of recent spatial memoryPreprint
León, W., Bruno, M. A., Allard, S., Nader, K., & Cuello, A. C. (2010) · Learning & Memory · doi:10.1101/lm.1804410 · Cited by 86 · cited 1× · see citing works
“Another possible explanation to the involvement of this region is related to the previously reported role of mPFC in the long term memory consolidation and recall processes (Frankland and Bontempi, 2005; Leon et al., 2010).”
Background
Insulin, IGF-1 and GLP-1 signaling in neurodegenerative disorders: targets for disease modification?
Bassil, F., Fernagut, P., Bézard, E., et al. (2014) · HAL (Le Centre pour la Communication Scientifique Directe) · doi:10.1016/j.pneurobio · Cited by 82 · see citing works
Contrasting brain activity patterns for item recognition memory and associative recognition memory: insights from immediate-early gene functional imaging
Aggleton, J. P., Brown, M. W., & Albasser, M. M. (2012) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2012.05.018 · Cited by 79 · cited 4× · see citing works
“Albasser and collaborators (Albasser et al., 2010; Aggleton et al., 2012) found a greater c-Fos expression in the dorsal CA3 subregion in rats exposed to novel objects when compared to rats exposed to familiar objects.”
BackgroundResultInfluential
Fos imaging reveals differential neuronal activation of areas of rat temporal cortex by novel and familiar sounds
Wan, H., Warburton, E. C., Kuśmierek, P., Aggleton, J. P., Kowalska, D. M., & Brown, M. W. (2001) · European Journal of Neuroscience · doi:10.1046/j.0953-816x.2001.01625.x · Cited by 72 · cited 3× · see citing works
“Previous studies showed a negative correlation between perirhinal c-Fos activity and exploration of familiar stimuli (Wan et al., 1999, 2001), which was not detected in the present work.”
BackgroundResult
Differential roles of the dorsal hippocampal regions in the acquisition of spatial and temporal aspects of episodic-like memory
Barbosa, F. F., de Oliveira Pontes, I. M., Ribeiro, S., Ribeiro, A. M., & Silva, R. H. (2012) · Behavioural Brain Research · doi:10.1016/j.bbr.2012.04.022 · Cited by 71 · see citing works
Object-Place Recognition Learning Triggers Rapid Induction of Plasticity-Related Immediate Early Genes and Synaptic Proteins in the Rat Dentate Gyrus
Soule, J. D., Penke, Z., Kanhema, T., Alme, M. N., Laroche, S., & Bramham, C. R. (2008) · Neural Plasticity · doi:10.1155/2008/269097 · Cited by 66 · cited 2× · see citing works
“More recently, Soulé et al. (2008) found that object-in-place task induces an increase in zif-268 in the rat DG.”
BackgroundMethod
Hippocampal c-Fos activation in normal and LPA1-null mice after two object recognition tasks with different memory demands
Castilla-Ortega, E., Pedraza, C., Chun, J., Fonseca, F. R. D., Estivill-Torrús, G., & Santín, L. J. (2012) · Behavioural Brain Research · doi:10.1016/j.bbr.2012.04.018 · Cited by 50 · cited 4× · see citing works
“In this respect, Castilla-Ortega et al. (2012) studied c-Fos activation after an ELM task in wild-type mice and LPA1-null mice.”
BackgroundResultInfluential
Distinct patterns of Fos immunoreactivity in striatum and hippocampus induced by different kinds of novelty in mice
Rinaldi, A., Romeo, S., Agustín‐Pavón, C., Oliverio, A., & Mele, A. (2010) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2010.08.004 · Cited by 41 · cited 2× · see citing works
“Contrary to previous studies (Albasser et al., 2010, 2013; Rinaldi et al., 2010; Castilla-Ortega et al., 2012), we did not found any difference in the c-Fos expression in the dorsal CA1 and CA3 subregions.”
BackgroundResult
Reinstatement of episodic-like memory in rats by neurokinin-1 receptor antagonism
Kart-Teke, E., Dere, E., Brandão, M. L., Huston, J. P., & Silva, M. A. D. S. (2006) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2006.09.007 · Cited by 40 · see citing works
Lesion of the lateral entorhinal cortex amplifies odor‐induced expression of c‐fos , junB , and zif 268 mRNA in rat brain
Bernabeu, R., Thiriet, N., Zwiller, J., & Scala, G. D. (2005) · Synapse · doi:10.1002/syn.20224 · Cited by 25 · cited 1× · see citing works
“Although both IEGs are approached as plasticity markers, their coactivation in the same neural regions is not unequivocal (Herdegen and Leah, 1998; Bernabeu et al., 2006).”
Background
The neural basis of nonvisual object recognition memory in the rat.
Albasser, M. M., Olarte‐Sánchez, C. M., Amin, E., Horne, M. R., Newton, M. J., Warburton, E. C., & Aggleton, J. P. (2012) · Behavioral Neuroscience · doi:10.1037/a0031216 · Cited by 25 · cited 3× · see citing works
“Contrary to previous studies (Albasser et al., 2010, 2013; Rinaldi et al., 2010; Castilla-Ortega et al., 2012), we did not found any difference in the c-Fos expression in the dorsal CA1 and CA3 subregions.”
BackgroundResult
Extending possible applications of an episodic-like memory task in rats
Barbosa, F. F., Pontes, I. M. D. O., Ribeiro, A. M., & Silva, R. H. (2010) · Behavioural Brain Research · doi:10.1016/j.bbr.2009.11.028 · Cited by 23 · cited 3× · see citing works
“Recently, we have adapted this protocol using a 24-h retention delay (Barbosa et al., 2010), in order to study separately the acquisition, consolidation, and retrieval mnemonic Frontiers in Behavioral Neuroscience www.frontiersin.org August 2013 | Volume 7 | Article 112 | 1 processes.”
MethodResult

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The medial prefrontal cortex - hippocampus circuit that integrates information of object, place and time to construct episodic memory in rodents: Behavioral, anatomical and neurochemical properties
Chao, O. Y., de Souza Silva, M. A., Yang, Y.-M., & Huston, J. P. (2020) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2020.04.007 · Cited by 158 · see citing works
Neuronal circuitry for recognition memory of object and place in rodent models
Chao, O. Y.-H., Nikolaus, S., Yang, Y., & Huston, J. P. (2022) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2022.104855 · Cited by 157 · see citing works
Regulation of object recognition and object placement by ovarian sex steroid hormones
Tuscher, J. J., Fortress, A. M., Kim, J., & Frick, K. M. (2014) · Behavioural Brain Research · doi:10.1016/j.bbr.2014.08.001 · Cited by 134 · see citing works
“Further support for a role of the hippocampus in OR is provided by a study demonstrating significantly more c-fos expression in the dentate gyrus of rats tested in OR than in the dentate of home cage control rats [37].”
Background
Medial prefrontal cortex role in recognition memory in rodents
Morici, J. F., Bekinschtein, P., & Weisstaub, N. (2015) · Behavioural Brain Research · doi:10.1016/j.bbr.2015.06.030 · Cited by 119 · see citing works
Genetic and functional analyses demonstrate a role for abnormal glycinergic signaling in autism
Pilorge, M., Fassier, C., Le Corronc, H., Potey, A., Bai, J., De Gois, S., Delaby, E., Assouline, B., Guinchat, V, Devillard, F., et al. (2016) · Molecular Psychiatry · doi:10.1038/mp.2015.139 · Cited by 110 · see citing works
Object Recognition Memory: Distinct Yet Complementary Roles of the Mouse CA1 and Perirhinal Cortex
Cinalli Jr., D. A., Cohen, S. J., Guthrie, K., & Stackman Jr., R. W. (2020) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2020.527543 · Cited by 79 · see citing works
“The finding that the limited amount of exploration of, or exposure to, novel objects or stimuli dictated by the weak training protocol, elicited greater numbers of Arc-positive cells in the PRh as compared to CA1 of the hippocampus, is consistent with results of prior analyses of Fos expression (Wan et al., 1999, 2001…”
Result
Hippocampus–Prefrontal Coupling Regulates Recognition Memory for Novelty Discrimination
Wang, C., Furlong, T. M., Stratton, P. G., Lee, C. C. Y., Xu, L., Merlin, S., Nolan, C. R., Arabzadeh, E., Marek, R., & Sah, P. (2021) · Journal of Neuroscience · doi:10.1523/jneurosci.1202-21.2021 · Cited by 73 · see citing works
A critical appraisal of the what-where-when episodic-like memory test in rodents: Achievements, caveats and future directions
Binder, S., Dere, E., & Zlomuzica, A. (2015) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2015.04.002 · Cited by 53 · see citing works
In search of a recognition memory engram
Brown, M. W., & Banks, P. J. (2014) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2014.09.016 · Cited by 56 · see citing works
Young pigs exhibit differential exploratory behavior during novelty preference tasks in response to age, sex, and delay
Fleming, S. A., & Dilger, R. N. (2016) · Behavioural Brain Research · doi:10.1016/j.bbr.2016.12.027 · Cited by 53 · see citing works
Drug-activated cells: From immediate early genes to neuronal ensembles in addiction
Salery, M., Godino, A., & Nestler, E. J. (2021) · Advances in pharmacology · doi:10.1016/bs.apha.2020.09.006 · Cited by 46 · see citing works
Multi-domain cognitive assessment of male mice shows space radiation is not harmful to high-level cognition and actually improves pattern separation
Whoolery, C. W., Yun, S., Reynolds, R. P., Lucero, M. J., Soler, I., Tran, F. H., Ito, N., Redfield, R. L., Richardson, D. R., Shih, H.-Y., et al. (2020) · Scientific Reports · doi:10.1038/s41598-020-59419-z · Cited by 49 · see citing works
D2 dopamine receptor regulation of learning, sleep and plasticity
França, A. S. C., Soares, B. L., Muratori, L., Nascimento, G., Winne, J., Pereira, C. M., Jerônimo, S. M. B., & Ribeiro, S. T. G. (2015) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2015.01.011 · Cited by 43 · see citing works
Role of the anterior cingulate cortex in the retrieval of novel object recognition memory after a long delay
Pezze, M. A., Marshall, H. J., Fone, K. C., & Cassaday, H. J. (2017) · Learning & Memory · doi:10.1101/lm.044784.116 · Cited by 35 · see citing works
“They found that the number of c-Fos and Zif-268-positive neurons in the mPFC was significantly increased compared with the control condition after retrieval of a NOR task (Barbosa et al. 2013).”
Method
What does engram encode?: Heterogeneous memory engrams for different aspects of experience
Nambu, M. F., Lin, Y.-J., Reuschenbach, J., & Tanaka, K. Z. (2022) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2022.102568 · Cited by 33 · see citing works
“Experiments by Barbosa et al. (2013) showed that responses to novel relational structures differed between IEGs [59].”
Background
Rapid eye movement sleep deprivation disrupts consolidation but not reconsolidation of novel object recognition memory in rats
Chen, L., Tian, S., & Ke, J. (2014) · Neuroscience Letters · doi:10.1016/j.neulet.2014.01.024 · Cited by 33 · see citing works
Deltamethrin Intranasal administration induces memory, emotional and tyrosine hydroxylase immunoreactivity alterations in rats
Souza, M. F., Freire, M. A. M., Medeiros, K. A. A. L., Lins, L. C. R. F., Bispo, J. M. M., de Gois, A. M., Leal, P. C., Engelberth, R. C. G. J., Ribeiro, A. M., Silva, R. H., et al. (2018) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2018.08.007 · Cited by 33 · see citing works
Memory of occasional events in rats: individual episodic memory profiles, flexibility, and neural substrate
Veyrac, A., Allerborn, M., Gros, A., Michon, F., Raguet, L., Kenney, J., Godinot, F., Thevenet, M., Garcia, S., Messaoudi, B., et al. (2015) · The Journal of Neuroscience · doi:10.1523/jneurosci.3941-14.2015 · Cited by 31 · see citing works
CA1 inactivation impairs episodic-like memory in rats
Drieskens, D. C., Neves, L. R., Pugliane, K. C., de Souza, I. B. M. B., Lima, Á. D. C., Salvadori, M. G. D. S. S., Ribeiro, A. M., Silva, R. H., & Barbosa, F. F. (2017) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2017.08.008 · Cited by 31 · see citing works
“…last decade, studies showed, in rodents, the involvement of the medial prefrontal cortex (mPFC), perirhinal cortex (PRH) and CA3 in the WWWhen/ELM (Barbosa et al., 2013; Chao, Huston, Nikolaus, & de Souza Silva, 2016; De Souza Silva, Huston, Wang, Petri, & Chao, 2015; DeVito & Eichenbaum, 2010;…”
BackgroundResult
Maternal intake of cashew nuts accelerates reflex maturation and facilitates memory in the offspring
de Melo, M. F. F. T., Pereira, D. E., de Sousa, M., Medeiros, D., Lemos, L. T. M., Madruga, M. S., Santos, N. M., de Oliveira, M. E. G., Bertozzo, C. C. D. M. S., & Soares, J. K. B. (2017) · International Journal of Developmental Neuroscience · doi:10.1016/j.ijdevneu.2017.06.006 · Cited by 29 · see citing works
Characterizing age-related decline of recognition memory and brain activation profile in mice
Belblidia, H., Léger, M., Abdelmalek, A., Quiedeville, A., Calocer, F., Boulouard, M., Jozet‐Alves, C., Fréret, T., & Schumann‐Bard, P. (2018) · Experimental Gerontology · doi:10.1016/j.exger.2018.03.006 · Cited by 25 · see citing works
Nicotine Enhances Object Recognition Memory via Stimulating α4β2 and α7 Nicotinic Acetylcholine Receptors in the Medial Prefrontal Cortex of Mice
Esaki, H., Izumi, S., Fukao, A., Ito, S., Nishitani, N., Deyama, S., & Kaneda, K. (2021) · Biological and Pharmaceutical Bulletin · doi:10.1248/bpb.b21-00314 · Cited by 25 · see citing works
Inhibition of clathrin-mediated endocytosis prevents amyloid β-induced axonal damage
Kuboyama, T., Lee, Y., Nishiko, H., & Tohda, C. (2015) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2015.02.005 · Cited by 26 · see citing works
Memory consolidation and expression of object recognition are susceptible to retroactive interference
Villar, M. E., Martínez, M. C., da Cunha, P. L., Ballarini, F., & Viola, H. (2016) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2016.04.010 · Cited by 25 · see citing works
Galanin (1–15)-fluoxetine interaction in the novel object recognition test. Involvement of 5-HT1A receptors in the prefrontal cortex of the rats
Flores‐Burgess, A., Millón, C., Gago, B., García-Durán, L., Cantero-García, N., Coveñas, R., Narváez, J. Á., Fuxé, K., Santín, L. J., & Dı́az-Cabiale, Z. (2019) · Neuropharmacology · doi:10.1016/j.neuropharm.2019.05.023 · Cited by 23 · see citing works
Amifostine (WR-2721) Mitigates Cognitive Injury Induced by Heavy Ion Radiation in Male Mice and Alters Behavior and Brain Connectivity
Boutros, S. W., Zimmerman, B., Nagy, S. C., Lee, J. S., Perez, R., & Raber, J. (2021) · Frontiers in Physiology · doi:10.3389/fphys.2021.770502 · Cited by 23 · see citing works
Possible Involvement of Standardized Bacopa monniera Extract (CDRI-08) in Epigenetic Regulation of reelin and Brain-Derived Neurotrophic Factor to Enhance Memory
Jayakumar, P., Singh, H. K., & Rajan, K. E. (2016) · Frontiers in Pharmacology · doi:10.3389/fphar.2016.00166 · Cited by 23 · see citing works
Fatty Acid Lingual Application Activates Gustatory and Reward Brain Circuits in the Mouse
Peterschmitt, Y., Abdoul‐Azize, S., Murtaza, B., Barbier, M., Khan, A. S., Millot, J., & Khan, N. A. (2018) · Nutrients · doi:10.3390/nu10091246 · Cited by 22 · see citing works
“[35] have shown that Zif-268 was increased in the dorsal CA1 region of the hippocampus, while there was no c-Fos activation in the experiments conducted to assess episodic-like memory in rats.”
Background
CRF2 receptor-deficiency reduces recognition memory deficits and vulnerability to stress induced by cocaine withdrawal
Morisot, N., Moine, C. L., Millan, M. J., & Contarino, A. (2014) · The International Journal of Neuropsychopharmacology · doi:10.1017/s1461145714000625 · Cited by 21 · see citing works
Contrasting roles for DNA methyltransferases and histone deacetylases in single-item and associative recognition memory
Scott, H., Smith, A. E., Barker, G. R., Uney, J. B., & Warburton, E. C. (2017) · Neuroepigenetics · doi:10.1016/j.nepig.2017.02.001 · Cited by 18 · see citing works
“…expression of immediate early genes and a number of transcription factors (Zhu et al., 1995; Bozon et al., 2003; Warburton et al., 2005; Soulé et al., 2008; McNulty et al., 2012; Seoane et al., 2012; Barbosa et al., 2013; Beer et al., 2013), little is known about how these genes are regulated.”
Rescue of synaptic and cognitive functions in polysialic acid-deficient mice and dementia models by short polysialic acid fragments
Varbanov, H., Jia, S., Kochlamazashvili, G., Bhattacharya, S., Buabeid, M. A., El‐Tabbal, M., Hayani, H., Stoyanov, S., Sun, W., Thiesler, H., et al. (2023) · Neurobiology of Disease · doi:10.1016/j.nbd.2023.106079 · Cited by 20 · see citing works
“The prefrontal cortex is known to be involved in object recognition memory in rodents (Barbosa et al., 2013).”
Background
Episodic-like memory impairment induced by sub-anaesthetic doses of ketamine
de Souza, I. B. M. B., Meurer, Y. D. S. R., Tavares, P. M., Pugliane, K. C., Lima, R. H., Silva, R. H., & Barbosa, F. F. (2019) · Behavioural Brain Research · doi:10.1016/j.bbr.2018.10.031 · Cited by 19 · see citing works
“This task was based on the natural exploratory behaviour to detect novelty in the environment [14,17].”
The Involvement of Canonical Wnt Signaling in Memory Impairment Induced by Chronic Cerebral Hypoperfusion in Mice
Kim, M., Bang, J., & Jeon, W. K. (2020) · Translational Stroke Research · doi:10.1007/s12975-019-00748-1 · Cited by 19 · see citing works
The Rap1 small GTPase is a critical mediator of the effects of stress on prefrontal cortical dysfunction
Kermath, B. A., Vanderplow, A. M., Bjornson, K. J., Seablom, E. N., Novak, A., Bernhardt, C. R., & Cahill, M. E. (2020) · Molecular Psychiatry · doi:10.1038/s41380-020-0835-0 · Cited by 17 · see citing works
“familiar objects in a recognition test and in response to investigating objects that are mismatched relative to their previously explored locations in an episodic memory test [73, 74].”
Background
Epigenomically Bistable Regions across Neuron-Specific Genes Govern Neuron Eligibility to a Coding Ensemble in the Hippocampus
Odell, S. C., Taki, F., Klein, S. L., Chen, R. J., Levine, O. B., Skelly, M. J., Nabila, A., Brindley, E., Toth, J. G., Dündar, F., et al. (2020) · Cell Reports · doi:10.1016/j.celrep.2020.107789 · Cited by 18 · see citing works
“Novelty is known to enhance extracellular glutamate levels in the hippocampus (Cohen et al., 2013) and to increase firing rates and frequencies of Ca 2+ events of DGCs (Barbosa et al., 2013; Cohen et al., 2013).”
Early memory deficits and extensive brain network disorganization in the App/MAPT double knock-in mouse model of familial Alzheimer’s disease
Borcuk, C., Héraud, C., Herbeaux, K., Diringer, M., Panzer, É., Scuto, J., Hashimoto, S., Saido, T. C., Saito, T., Goutagny, R., et al. (2022) · Aging Brain · doi:10.1016/j.nbas.2022.100042 · Cited by 16 · see citing works
“Post-mortem mapping of activity-regulated expression of immediate early gene c-fos has been widely accepted to identify populations of neurons activated during encoding and retrieval phases of different aspects of recognition memory in rodents (e.g., [1,5,79].”
Probing the nature of episodic memory in rodents
Huston, J. P., & Chao, O. Y.-H. (2022) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2022.104930 · Cited by 16 · see citing works
Comparable reduction in Zif268 levels and cytochrome oxidase activity in the retrosplenial cortex following mammillothalamic tract lesions
Frizzati, A., Milczarek, M. M., Sengpiel, F., Thomas, K. L., Dillingham, C. M., & Vann, S. D. (2016) · Neuroscience · doi:10.1016/j.neuroscience.2016.05.030 · Cited by 15 · see citing works
“Furthermore, increased levels of c-Fos, Zif268 and cytochrome oxidase have been found in both the retrosplenial cortex and hippocampus of rats performing spatial memory tasks (Vann et al., 2000a,b; Soule et al., 2008; Pothuizen et al., 2009; Barbosa et al., 2013).”
Background
Nicotine enhances object recognition memory through inhibition of voltage-dependent potassium 7 channels in the medial prefrontal cortex of mice
Esaki, H., Izumi, S., Fukao, A., Nishitani, N., Deyama, S., & Kaneda, K. (2021) · Journal of Pharmacological Sciences · doi:10.1016/j.jphs.2021.05.009 · Cited by 15 · see citing works
Viral-mediated Zif268 expression in the prefrontal cortex protects against gonadectomy-induced working memory, long-term memory, and social interaction deficits in male rats
Dossat, A. M., Jourdi, H., Wright, K. N., Strong, C. E., Sarkar, A., & Kabbaj, M. (2016) · Neuroscience · doi:10.1016/j.neuroscience.2016.10.062 · Cited by 15 · see citing works
“, 2014), and the mPFC contributes to memory tasks without a spatial component (Barker et al., 2007; Barbosa et al., 2013), another aim of this work was to examine the role of mPFC Zif268 in long-term memory, investigated using the spontaneous object recognition (SOR; also known as: novel object recognition) test (Wint…”
Background
Timing of presentation and nature of stimuli determine retroactive interference with social recognition memory in mice
Camats‐Perna, J., Wotjak, C. T., Stork, O., & Engelmann, M. (2015) · Physiology & Behavior · doi:10.1016/j.physbeh.2015.02.029 · Cited by 15 · see citing works
“The object was chosen to primarily stimulate vision [22] and taction.”
Perturbation of GABAergic Synapses at the Axon Initial Segment of Basolateral Amygdala Induces Trans-regional Metaplasticity at the Medial Prefrontal Cortex
Saha, R., Shrivastava, K., Jing, L., Schayek, R., Maroun, M., Kriebel, M., Volkmer, H., & Richter‐Levin, G. (2017) · Cerebral Cortex · doi:10.1093/cercor/bhx300 · Cited by 13 · see citing works
“To evaluate the object place recognition memory, we have used a modified SOR task based on the protocol of (Barbosa et al. 2012, 2013).”
Method
Biological Sex and Sex Hormone Impacts on Deficits in Episodic-Like Memory in a Rat Model of Early, Pre-motor Stages of Parkinson's Disease
Conner, M. R., Jang, D., Anderson, B. J., & Kritzer, M. F. (2020) · Frontiers in Neurology · doi:10.3389/fneur.2020.00942 · Cited by 13 · see citing works
Immediate-Early Gene Expression in Neural Circuits Related to Object Recognition Memory
Barbosa, F. F., & Silva, R. H. (2018) · Handbook of behavioral neuroscience · doi:10.1016/b978-0-12-812012-5.00018-5 · Cited by 11 · see citing works
Serotonin Type 2a Receptor in the Prefrontal Cortex Controls Perirhinal Cortex Excitability During Object Recognition Memory Recall
Morici, J. F., Cicuttin, G., Silva, A., Gallo, F. T., Miranda, M., Belluscio, M., Zold, C. L., Bekinschtein, P., & Weisstaub, N. (2022) · Neuroscience · doi:10.1016/j.neuroscience.2022.05.015 · Cited by 10 · see citing works
Recognition memory-induced gene expression in the perirhinal cortex: A transcriptomic analysis
Scott, H., Rogers, M. F., Scott, H. L., Campbell, C., Warburton, E. C., & Uney, J. B. (2017) · Behavioural Brain Research · doi:10.1016/j.bbr.2017.04.007 · Cited by 9 · see citing works
“In group Novel, genes that were highly significantly upregulated compared to Control included transcription factors and immediate early genes such as Arc (p = 5.29E10), Egr1 (p = 1.11E-08) and Trps1 (p = 5.65E-09) as well as heat shock proteins Hspa1b (p = 5.60E-12) and Hspa5 (p= 3.44E-10).”
Influential
Activity-regulated E3 ubiquitin ligase TRIM47 modulates excitatory synapse development
Sharma, G., & Banerjee, S. (2022) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2022.943980 · Cited by 8 · see citing works
Domain‐specific contributions of biological sex and sex hormones to what, where and when components of episodic‐like memory in adult rats
Conner, M. R., Adeyemi, O. M., Anderson, B. J., & Kritzer, M. F. (2020) · European Journal of Neuroscience · doi:10.1111/ejn.14676 · Cited by 8 · see citing works
“The brain areas involved include medial temporal and frontal cortical structures that are homologous to those identified as essential for episodic memory in lesion (Chao, Nikolaus, Lira Brandao, Huston, & Souza Silva, 2017; DeVito & Eichenbaum, 2010; Eichenbaum, Sauvage, Fortin, Komorowski, & Lipton, 2012; Li & Chao,…”
Background
Trauma-like exposure alters neuronal apoptosis, Bin1, Fkbp5 and NR2B expression in an amyloid-beta (1–42) rat model of Alzheimer's disease
Faborode, O. S., Dallé, E., & Mabandla, M. V. (2022) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2022.107611 · Cited by 7 · see citing works
Working memory training triggers delayed chromatin remodeling in the mouse corticostriatothalamic circuit
Cassanelli, P. M., Cladouchos, M. L., Macedo, G. V. F., Sifonios, L. L., Giaccardi, L. I., Gutiérrez, M. L., Gravielle, M. C., & Wikinski, S. (2015) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2015.02.011 · Cited by 7 · see citing works
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Authors: Barbosa, F. F., Santos, J. R., Meurer, Y. S. R., Macêdo, P. T., Ferreira, L. M. S., Pontes, I. M. O., Ribeiro, A. M., & Silva, R. H.
Affiliations: Universidade Federal da Paraíba (BR)
Universidade Federal de Sergipe (BR)
Universidade Federal do Rio Grande do Norte (BR)
Corresponding author: Silva, Regina Helena
ORCID: Barbosa, Flávio Freitas
Santos, José Ronaldo
Ribeiro, Alessandra Mussi
Silva, Regina Helena
Venue: Frontiers in Behavioral Neuroscience
Publisher: Frontiers Media SA
Published: 2013
Volume: 7
Pages: 112-112
ISSN: 1662-5153 (ISSN-L)
DOI: 10.3389/fnbeh.2013.00112
PMC: PMC3749513
OpenAlex: W2155145921
Cited by: 79
References: 67
Citations by year: 2026: 1 · 2025: 3 · 2024: 2 · 2023: 3 · 2022: 13 · 2021: 8 · 2020: 11 · 2019: 4 · 2018: 6 · 2017: 7 · 2016: 7 · 2015: 10 · 2014: 4
FWCI: 3.84
Type: journal article
Language: en
Open access: gold
doi.org
Licence: cc-by
Locations: Frontiers in Behavioral Neuroscience (publishedVersion, cc-by)
Europe PMC (PubMed Central) (publishedVersion, cc-by)
PubMed Central (publishedVersion, cc-by)
PubMed (publishedVersion)
LA Referencia (Red Federada de Repositorios Institucionales de Publicaciones Científicas) (publishedVersion, other-oa)
DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
Funders: Coordenação de Aperfeiçoamento de Pessoal de Nível Superior
Conselho Nacional de Desenvolvimento Científico e Tecnológico
Fundação de Apoio à Pesquisa do Rio Grande do Norte
Topics: Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
Life Sciences › Neuroscience › Cognitive Neuroscience › Memory Processes and Influences
Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
Keywords: episodic-like memory, object recognition, c-fos, Zif268, immediate early genes, medial prefrontal cortex, perirhinal cortex, dorsal dentate gyrus, dorsal CA1, spatial memory, neural network activation, rats

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Differential cortical c-Fos and Zif-268 expression after object and spatial memory processing in a standard or episodic-like object recognition task

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