Identification of Functional Circuitry between Retrosplenial and Postrhinal Cortices during Fear Conditioning

Robinson, Siobhan; Poorman, Caroline E.; Marder, Thomas J.; Bucci, David J.

doi:10.1523/jneurosci.2814-12.2012

Cited by 50 publications

(40 citation statements)

References 65 publications

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“…Therefore, this structure seems to be an important component of spatial circuits in both humans and rodents. Based on this evidence, it has been proposed that the RSC role in spatial navigation is due to either its ability to process the sequence of heading vectors required for navigating in space or its ability to support the transition between allocentric (world-centered) references, encoded by the hippocampus, and egocentric (selfcentered) references, supported by the parietal cortex (21).Recent studies suggested that, in addition to the hippocampus, other connected cortical regions can support encoding and storage of spatial memory (22)(23)(24)(25). Elevated expression of immediate early genes (IEGs) is thought to reflect this involvement (22,25,26).…”

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confidence: 99%

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Encoding and storage of spatial information in the retrosplenial cortex

Czajkowski

Balaji

Wiltgen

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

212

150

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The retrosplenial cortex (RSC) is part of a network of interconnected cortical, hippocampal, and thalamic structures harboring spatially modulated neurons. The RSC contains head direction cells and connects to the parahippocampal region and anterior thalamus. Manipulations of the RSC can affect spatial and contextual tasks. A considerable amount of evidence implicates the role of the RSC in spatial navigation, but it is unclear whether this structure actually encodes or stores spatial information. We used a transgenic mouse in which the expression of green fluorescent protein was under the control of the immediate early gene c-fos promoter as well as timelapse two-photon in vivo imaging to monitor neuronal activation triggered by spatial learning in the Morris water maze. We uncovered a repetitive pattern of cell activation in the RSC consistent with the hypothesis that during spatial learning an experience-dependent memory trace is formed in this structure. In support of this hypothesis, we also report three other observations. First, temporary RSC inactivation disrupts performance in a spatial learning task. Second, we show that overexpressing the transcription factor CREB in the RSC with a viral vector, a manipulation known to enhance memory consolidation in other circuits, results in spatial memory enhancements. Third, silencing the viral CREB-expressing neurons with the allatostatin system occludes the spatial memory enhancement. Taken together, these results indicate that the retrosplenial cortex engages in the formation and storage of memory traces for spatial information. S patial navigation, learning, and memory depend on several interconnected brain regions. The hippocampus is known to have a central role in spatial learning and memory. Place cells in this structure form a spatial map of an animal's environment (1). The main input to the hippocampus comes from the entorhinal cortex, an area that integrates cortical inputs before forwarding them into the hippocampal formation. The dorsal medial entorhinal cortex (MEC) contains spatially modulated cells (grid cells) that fire at the nodes of a hexagonal lattice as the animal traverses its environment (2). Beyond hippocampal place cells and MEC grid cells, there is also extensive evidence for another type of spatially modulated neurons that increase firing when the animal's head points in a specific direction [head direction (HD) cells] (3). These cells reside in several subcortical and cortical regions, including the retrosplenial cortex (RSC). The RSC is one of the most important cortical afferents to MEC (4, 5). It is the most caudal part of the cingulate cortex, positioned between anterior cingulate, parietal/visual, and parahippocampal cortices. It is further subdivided into areas A29a-c (granular cortex) and area A30 (dysgranular cortex) (6). The RSC has been implicated in a number of cognitive tasks, including navigation based on external spatial (allothetic) information (7). Human functional MRI (fMRI) studies showed that the RSC is activated duri...

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confidence: 99%

“…Recent studies suggested that, in addition to the hippocampus, other connected cortical regions can support encoding and storage of spatial memory (22)(23)(24)(25). Elevated expression of immediate early genes (IEGs) is thought to reflect this involvement (22,25,26).…”

mentioning

confidence: 99%

Encoding and storage of spatial information in the retrosplenial cortex

Czajkowski

Balaji

Wiltgen

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

212

150

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“…Several lesion studies have involved RSC in memory (Sutherland et al 1988;Aggleton 2002, 2004;Harker and Whishaw 2004;Keene and Bucci 2008a,b,c;Dumont et al 2010;Haijima and Ichitani 2012;Robinson et al 2012). However, this kind of intervention has several drawbacks (Izquierdo and Medina 1998), including a lack of discrimination between memory acquisition, memory formation, or memory expression.…”

Section: [Supplemental Materials Is Available For This Article]mentioning

confidence: 99%

Functional integrity of the retrosplenial cortex is essential for rapid consolidation and recall of fear memory

Katche¹,

Dorman²,

Slipczuk

et al. 2013

Learn. Mem.

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Memory storage is a temporally graded process involving different phases and different structures in the mammalian brain. Cortical plasticity is essential to store stable memories, but little is known regarding its involvement in memory processing. Here we show that fear memory consolidation requires early post-training macromolecular synthesis in the anterior part of the retrosplenial cortex (aRSC), and that reversible pharmacological inactivation of this cortical region impairs recall of recent as well as of remote memories. These results challenge the generally accepted idea that neocortical areas are slow encoding systems that participate in the retrieval of remote memories only. [Supplemental material is available for this article.]A dominant idea that emerged in the last two decades is that memory consolidation comprises two phases. The initial one, called cellular or synaptic consolidation, is fast, lasting from several hours to a couple of days, and depends on de novo protein and mRNA synthesis required for functional and structural changes in brain regions engaged in the acquisition and early processing of new information, such as the hippocampus and related noncortical structures (Dudai 2002;Dudai and Eisenberg 2004;Morris 2006). The second phase is slower, and would entail the participation of neocortical regions and their interactions with medial temporal lobe structures reorganizing the recently learned material (Squire 1992). It is called systems-level consolidation and seems to begin late after acquisition and last from several days to weeks to months in most learning tasks studied so far (Frankland and Bontempi 2005). However, when recently encoded information interacts with an already stored associative schema, systems-level consolidation may well be very rapid (Tse et al. 2007(Tse et al. , 2011. Consistent with the standard model of memory consolidation, it has been shown that, while the hippocampus is mainly involved in consolidating and recalling recent episodic-like memories, some cortical regions, including prelimbic, orbitofrontal, and anterior cingulate areas, are involved preferentially with remote, well-consolidated memory traces (Frankland et al. 2004;Maviel et al. 2004;Shan et al. 2008;Lesburgueres et al. 2011;Tse et al. 2011).The retrosplenial cortex (RSC) comprises the entire posterior cingulate cortex in rodents (Vogt and Peters 1981) and is one of the largest cortical areas in the rat. Situated at the crossroads between the hippocampal formation and many neocortical areas, it has attracted much attention especially for its involvement in cognition (Vann et al. 2009). Although RSC inactivation produces memory impairments similar to those caused by hippocampal lesions (Cooper and Mizumori 2001;Vann and Aggleton 2004), and it has been shown that RSC is activated during retrieval of contextual information and autobiographical memory (Valenstein et al. 1987, Daselaar et al. 2006), the precise function of this area is poorly understood (Ranganath and Ritchey 2012).To study the precise r...

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“…However, the hippocampus does not exist nor act in isolation; cortical regions both within and outside of the medial temporal lobe provide critical sensory information to the hippocampal formation [5][6][7] . Traditional permanent lesion studies provide compelling evidence for the involvement of a number of cortical regions (e.g., the retrosplenial, postrhinal and entorhinal cortices) in hippocampal-dependent learning but are limited in their ability to discern the role of a particular region during discrete phases of learning [8][9][10] .…”

Section: Introductionmentioning

confidence: 99%

A Method for Remotely Silencing Neural Activity in Rodents During Discrete Phases of Learning

Robinson

Adelman

2015

JoVE

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This protocol describes how to temporarily and remotely silence neuronal activity in discrete brain regions while animals are engaged in learning and memory tasks. The approach combines pharmacogenetics (Designer-Receptors-Exclusively-Activated-by-Designer-Drugs) with a behavioral paradigm (sensory preconditioning) that is designed to distinguish between different forms of learning. Specifically, viral-mediated delivery is used to express a genetically modified inhibitory G-protein coupled receptor (the Designer Receptor) into a discrete brain region in the rodent. Three weeks later, when designer receptor expression levels are high, a pharmacological agent (the Designer Drug) is administered systemically 30 min prior to a specific behavioral session. The drug has affinity for the designer receptor and thus results in inhibition of neurons that express the designer receptor, but is otherwise biologically inert. The brain region remains silenced for 2-5 hr (depending on the dose and route of administration). Upon completion of the behavioral paradigm, brain tissue is assessed for correct placement and receptor expression. This approach is particularly useful for determining the contribution of individual brain regions to specific components of behavior and can be used across any number of behavioral paradigms. Video LinkThe video component of this article can be found at

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Identification of Functional Circuitry between Retrosplenial and Postrhinal Cortices during Fear Conditioning

Cited by 50 publications

References 65 publications

Encoding and storage of spatial information in the retrosplenial cortex

Encoding and storage of spatial information in the retrosplenial cortex

Functional integrity of the retrosplenial cortex is essential for rapid consolidation and recall of fear memory

A Method for Remotely Silencing Neural Activity in Rodents During Discrete Phases of Learning

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