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      Asymmetric cross-hemispheric connections link the rat anterior thalamic nuclei with the cortex and hippocampal formation

      research-article
      a , * , a , b , a , a , a
      Neuroscience
      Elsevier Science
      AD, anterodorsal thalamic nucleus, AM, anteromedial thalamic nucleus, a-p, anterior-posterior, AV, anteroventral thalamic nucleus, BDA, biotinylated dextran amine, Cg, cingulate cortex, DY, diamidino yellow, FB, fast blue tracer, FG, fluorogold tracer, HPC, hippocampus, IAD, interanterodorsal thalamic nucleus, IAM, interanteromedial thalamic nucleus, LD, laterodorsal thalamic nucleus, LP, lateral posterior thalamic nucleus, M2, secondary motor cortex, MD, mediodorsal thalamic nucleus, PL, prelimbic cortex, PoS, postsubiculum, PT, parataenial thalamic nucleus, RSC, retrosplenial cortex, RSD, dysgranular retrosplenial cortex, RSG, granular retrosplenial cortex, Sm, stria medullaris of the thalamus, SUB, subiculum, V1, primary visual cortex, V2, secondary visual cortex, VA, ventral anterior thalamic nucleus, VL, ventrolateral thalamic nucleus, WGA-HRP, horseradish peroxidase-conjugated wheat germ agglutinin, Contralateral, Corticothalamic, Hippocampus, Interhemispheric, Thalamocortical, Thalamus

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          Highlights

          • Thalamocortical projections from ATN are ipsilateral with the exception of a restricted bilateral AV projection to RSC.

          • Corticothalamic projections to the ATN are bilateral with the exception of an ipsilateral Cg projection to the AV nucleus.

          • The subiculum receives ipsilateral ATN efferents and provides the ATN with bilateral afferents.

          • The LD nucleus has exclusively ipsilateral, bidirectional connections with investigated cortical and hippocampal targets.

          • The postsubiculum has exclusively ipsilateral, bidirectional connections with the ATN, as well as the LD nucleus.

          Abstract

          Dense reciprocal connections link the rat anterior thalamic nuclei with the prelimbic, anterior cingulate and retrosplenial cortices, as well as with the subiculum and postsubiculum. The present study compared the ipsilateral thalamic-cortical connections with the corresponding crossed, contralateral connections between these same sets of regions. All efferents from the anteromedial thalamic nucleus to the cortex, as well as those to the subiculum, remained ipsilateral. In contrast, all of these target sites provided reciprocal, bilateral projections to the anteromedial nucleus. While the anteroventral thalamic nucleus often shared this same asymmetric pattern of cortical connections, it received relatively fewer crossed inputs than the anteromedial nucleus. This difference was most marked for the anterior cingulate projections, as those to the anteroventral nucleus remained almost entirely ipsilateral. Unlike the anteromedial nucleus, the anteroventral nucleus also appeared to provide a restricted, crossed projection to the contralateral retrosplenial cortex. Meanwhile, the closely related laterodorsal thalamic nucleus had almost exclusively ipsilateral efferent and afferent cortical connections. Likewise, within the hippocampus, the postsubiculum seemingly had only ipsilateral efferent and afferent connections with the anterior thalamic and laterodorsal nuclei. While the bilateral cortical projections to the anterior thalamic nuclei originated predominantly from layer VI, the accompanying sparse projections from layer V largely gave rise to ipsilateral thalamic inputs. In testing a potentially unifying principle of anterior thalamic – cortical interactions, a slightly more individual pattern emerged that reinforces other evidence of functional differences within the anterior thalamic and also helps to explain the consequences of unilateral interventions involving these nuclei.

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          Most cited references82

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          The head direction signal: origins and sensory-motor integration.

          Navigation first requires accurate perception of one's spatial orientation within the environment, which consists of knowledge about location and directional heading. Cells within several limbic system areas of the mammalian brain discharge allocentrically as a function of the animal's directional heading, independent of the animal's location and ongoing behavior. These cells are referred to as head direction (HD) cells and are believed to encode the animal's perceived directional heading with respect to its environment. Although HD cells are found in several areas, the principal circuit for generating this signal originates in the dorsal tegmental nucleus and projects serially, with some reciprocal connections, to the lateral mammillary nucleus --> anterodorsal thalamus --> PoS, and terminates in the entorhinal cortex. HD cells receive multimodal information about landmarks and self-generated movements. Vestibular information appears critical for generating the directional signal, but motor/proprioceptive and landmark information are important for updating it.
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            Thalamus plays a central role in ongoing cortical functioning

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              Head-direction cells recorded from the postsubiculum in freely moving rats. I. Description and quantitative analysis.

              This paper is a study of the behavioral and spatial firing correlates of neurons in the rat postsubiculum. Recordings were made from postsubicular neurons as rats moved freely throughout a cylindrical chamber, where the major cue for orientation was a white card taped to the inside wall. An automatic video/computer system monitored cell discharge while simultaneously tracking the position of 2 colored light emitting diodes (LEDs) secured to the animal's head. The animal's location was calculated from the position of one of the LEDs and head direction in the horizontal plane calculated from the relative positions of the 2 LEDs. Approximately 26% of the cells were classified as head-direction cells because they discharged as a function of the animal's head direction in the horizontal plane, independent of the animal's behavior, location, or trunk position. For each head-direction cell, vectors drawn in the direction of maximal firing were parallel throughout the recording chamber and did not converge toward a single point. Plots of firing rate versus head direction showed that each firing-rate/head-direction function was adequately described by a triangular function. Each cell's maximum firing rate occurred at only one (the preferred) head direction; firing rates at head directions on either side of the preferred direction decreased linearly with angular deviation from the preferred direction. Results from 24 head-direction cells in 7 animals showed an equal distribution of preferred firing directions over a 360 degrees angle. The peak firing rate of head-direction cells varied from 5 to 115 spikes/sec (mean: 35). The range of head-direction angles over which discharge was elevated (directional firing range) was usually about 90 degrees, with little, if any, discharge at head directions outside this range. Quantitative analysis showed the location of the animal within the cylinder had minimal effect on directional cell firing. For each head-direction cell, the preferred direction, peak firing rate, and directional firing range remained stable for days. These results identify a new cell type that signals the animal's head direction in its environment.
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                Author and article information

                Contributors
                Journal
                Neuroscience
                Neuroscience
                Neuroscience
                Elsevier Science
                0306-4522
                1873-7544
                04 May 2017
                04 May 2017
                : 349
                : 128-143
                Affiliations
                [a ]School of Psychology, Cardiff University, Tower Building, 70 Park Place, Cardiff CF10 3AT, UK
                [b ]Trinity College Institute of Neuroscience, Trinity College Dublin, Dublin, Ireland
                Author notes
                [* ]Corresponding author. MathiasenM@ 123456cardiff.ac.uk
                Article
                S0306-4522(17)30109-4
                10.1016/j.neuroscience.2017.02.026
                5387186
                28237814
                ad82c464-ca2e-4576-b871-d98a26b12cec
                © 2017 The Authors

                This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).

                History
                : 30 October 2016
                : 13 February 2017
                Categories
                Article

                Neurosciences
                ad, anterodorsal thalamic nucleus,am, anteromedial thalamic nucleus,a-p, anterior-posterior,av, anteroventral thalamic nucleus,bda, biotinylated dextran amine,cg, cingulate cortex,dy, diamidino yellow,fb, fast blue tracer,fg, fluorogold tracer,hpc, hippocampus,iad, interanterodorsal thalamic nucleus,iam, interanteromedial thalamic nucleus,ld, laterodorsal thalamic nucleus,lp, lateral posterior thalamic nucleus,m2, secondary motor cortex,md, mediodorsal thalamic nucleus,pl, prelimbic cortex,pos, postsubiculum,pt, parataenial thalamic nucleus,rsc, retrosplenial cortex,rsd, dysgranular retrosplenial cortex,rsg, granular retrosplenial cortex,sm, stria medullaris of the thalamus,sub, subiculum,v1, primary visual cortex,v2, secondary visual cortex,va, ventral anterior thalamic nucleus,vl, ventrolateral thalamic nucleus,wga-hrp, horseradish peroxidase-conjugated wheat germ agglutinin,contralateral,corticothalamic,hippocampus,interhemispheric,thalamocortical,thalamus

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