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      Postnatal development of retrosplenial projections to the parahippocampal region of the rat

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          Abstract

          The rat parahippocampal region (PHR) and retrosplenial cortex (RSC) are cortical areas important for spatial cognition. In PHR, head-direction cells are present before eye-opening, earliest detected in postnatal day (P)11 animals. Border cells have been recorded around eye-opening (P16), while grid cells do not obtain adult-like features until the fourth postnatal week. In view of these developmental time-lines, we aimed to explore when afferents originating in RSC arrive in PHR. To this end, we injected rats aged P0-P28 with anterograde tracers into RSC. First, we characterized the organization of RSC-PHR projections in postnatal rats and compared these results with data obtained in the adult. Second, we described the morphological development of axonal plexus in PHR. We conclude that the first arriving RSC-axons in PHR, present from P1 onwards, already show a topographical organization similar to that seen in adults, although the labeled plexus does not obtain adult-like densities until P12.

          DOI: http://dx.doi.org/10.7554/eLife.13925.001

          eLife digest

          Our ability to navigate critically depends on part of the brain called the parahippocampal region. Within this region, there are several different types of brain cells (or neurons) whose activity “codes” different aspects of navigation, such as position, direction and speed.

          To understand how parahippocampal neurons are able to form these activity patterns, we need to understand how they develop connections with neurons from other brain regions that are important for navigation, such as the retrosplenial cortex. If inputs from retrosplenial neurons are important for generating the activity patterns observed in the parahippocampal region, the connections between the two groups of neurons should be fully mature before the activity patterns emerge. In rats, this should occur around 11–16 days after birth.

          Sugar and Witter have now assessed how the retrosplenial inputs are organized in the parahippocampal region of rats. This revealed that, when the rats are born, there are very few retrosplenial inputs present in the parahippocampal region. However, the few inputs that are present are organized similarly to how they eventually will be organized in adults. After birth, the number of inputs gradually increases until the rats are approximately 12 days old, at which point the pattern of connections is indistinguishable from what we observe in adults. Thus it appears that retrosplenial inputs are fully mature before activity patterns emerge in the parahippocampal region.

          In the future, Sugar and Witter would like to investigate how inputs to the parahippocampal region are able to organize themselves during early development. The importance of retrosplenial inputs could also be investigated by manipulating them during development and adulthood.

          DOI: http://dx.doi.org/10.7554/eLife.13925.002

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          Most cited references 63

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          Representation of geometric borders in the entorhinal cortex.

          We report the existence of an entorhinal cell type that fires when an animal is close to the borders of the proximal environment. The orientation-specific edge-apposing activity of these "border cells" is maintained when the environment is stretched and during testing in enclosures of different size and shape in different rooms. Border cells are relatively sparse, making up less than 10% of the local cell population, but can be found in all layers of the medial entorhinal cortex as well as the adjacent parasubiculum, often intermingled with head-direction cells and grid cells. Border cells may be instrumental in planning trajectories and anchoring grid fields and place fields to a geometric reference frame.
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            Spatial representation in the entorhinal cortex.

            As the interface between hippocampus and neocortex, the entorhinal cortex is likely to play a pivotal role in memory. To determine how information is represented in this area, we measured spatial modulation of neural activity in layers of medial entorhinal cortex projecting to the hippocampus. Close to the postrhinal-entorhinal border, entorhinal neurons had stable and discrete multipeaked place fields, predicting the rat's location as accurately as place cells in the hippocampus. Precise positional modulation was not observed more ventromedially in the entorhinal cortex or upstream in the postrhinal cortex, suggesting that sensory input is transformed into durable allocentric spatial representations internally in the dorsocaudal medial entorhinal cortex.
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              Development of the spatial representation system in the rat.

              In the adult brain, space and orientation are represented by an elaborate hippocampal-parahippocampal circuit consisting of head-direction cells, place cells, and grid cells. We report that a rudimentary map of space is already present when 2 1/2-week-old rat pups explore an open environment outside the nest for the first time. Head-direction cells in the pre- and parasubiculum have adultlike properties from the beginning. Place and grid cells are also present but evolve more gradually. Grid cells show the slowest development. The gradual refinement of the spatial representation is accompanied by an increase in network synchrony among entorhinal stellate cells. The presence of adultlike directional signals at the onset of navigation raises the possibility that such signals are instrumental in setting up networks for place and grid representation.
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                Author and article information

                Contributors
                Role: Reviewing editor
                Journal
                eLife
                Elife
                eLife
                eLife
                eLife
                eLife Sciences Publications, Ltd
                2050-084X
                23 March 2016
                2016
                : 5
                Affiliations
                deptKavli Institute for Systems Neuroscience and Centre for Neural Computation , Norwegian University for Science and Technology , Trondheim, Norway
                Boston University , United States
                Boston University , United States
                Author notes
                Article
                13925
                10.7554/eLife.13925
                4859804
                27008178
                © 2016, Sugar et al

                This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited.

                Product
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/501100005416, Norges Forskningsråd;
                Award ID: 145993
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100005416, Norges Forskningsråd;
                Award ID: 181676
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100005416, Norges Forskningsråd;
                Award ID: Centre of Excellence grant
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/100001201, Kavli Foundation;
                Award Recipient :
                The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
                Categories
                Research Article
                Neuroscience
                Custom metadata
                2.5
                Retrosplenial axons arriving in the parahippocampal region around the first day after birth are topographically organized, similarly to what has been reported in the adult.

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