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      The anterior thalamus provides a subcortical circuit supporting memory and spatial navigation

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          Abstract

          The anterior thalamic nuclei (ATN), a central component of Papez' circuit, are generally assumed to be key constituents of the neural circuits responsible for certain categories of learning and memory. Supporting evidence for this contention is that damage to either of two brain regions, the medial temporal lobe and the medial diencephalon, is most consistently associated with anterograde amnesia. Within these respective regions, the hippocampal formation and the ATN (anteromedial, anteroventral, and anterodorsal) are the particular structures of interest. The extensive direct and indirect hippocampal-anterior thalamic interconnections and the presence of theta-modulated cells in both sites further support the hypothesis that these structures constitute a neuronal network crucial for memory and cognition. The major tool in understanding how the brain processes information is the analysis of neuronal output at each hierarchical level along the pathway of signal propagation coupled with neuroanatomical studies. Here, we discuss the electrophysiological properties of cells in the ATN with an emphasis on their role in spatial navigation. In addition, we describe neuroanatomical and functional relationships between the ATN and hippocampal formation.

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          Most cited references101

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          Microstructure of a spatial map in the entorhinal cortex.

          The ability to find one's way depends on neural algorithms that integrate information about place, distance and direction, but the implementation of these operations in cortical microcircuits is poorly understood. Here we show that the dorsocaudal medial entorhinal cortex (dMEC) contains a directionally oriented, topographically organized neural map of the spatial environment. Its key unit is the 'grid cell', which is activated whenever the animal's position coincides with any vertex of a regular grid of equilateral triangles spanning the surface of the environment. Grids of neighbouring cells share a common orientation and spacing, but their vertex locations (their phases) differ. The spacing and size of individual fields increase from dorsal to ventral dMEC. The map is anchored to external landmarks, but persists in their absence, suggesting that grid cells may be part of a generalized, path-integration-based map of the spatial environment.
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            Theta oscillations in the hippocampus.

            Theta oscillations represent the "on-line" state of the hippocampus. The extracellular currents underlying theta waves are generated mainly by the entorhinal input, CA3 (Schaffer) collaterals, and voltage-dependent Ca(2+) currents in pyramidal cell dendrites. The rhythm is believed to be critical for temporal coding/decoding of active neuronal ensembles and the modification of synaptic weights. Nevertheless, numerous critical issues regarding both the generation of theta oscillations and their functional significance remain challenges for future research.
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              Memory, navigation and theta rhythm in the hippocampal-entorhinal system.

              Theories on the functions of the hippocampal system are based largely on two fundamental discoveries: the amnestic consequences of removing the hippocampus and associated structures in the famous patient H.M. and the observation that spiking activity of hippocampal neurons is associated with the spatial position of the rat. In the footsteps of these discoveries, many attempts were made to reconcile these seemingly disparate functions. Here we propose that mechanisms of memory and planning have evolved from mechanisms of navigation in the physical world and hypothesize that the neuronal algorithms underlying navigation in real and mental space are fundamentally the same. We review experimental data in support of this hypothesis and discuss how specific firing patterns and oscillatory dynamics in the entorhinal cortex and hippocampus can support both navigation and memory.
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                Author and article information

                Journal
                Front Syst Neurosci
                Front Syst Neurosci
                Front. Syst. Neurosci.
                Frontiers in Systems Neuroscience
                Frontiers Media S.A.
                1662-5137
                30 August 2013
                2013
                : 7
                : 45
                Affiliations
                [1] 1Trinity College Institute of Neuroscience, Trinity College Dublin Dublin 2, Ireland
                [2] 2School of Psychology, Cardiff University Cardiff, UK
                [3] 3School of Optometry and Vision Sciences, Cardiff University Cardiff, UK
                Author notes

                Edited by: Yuri B. Saalmann, Princeton University, USA

                Reviewed by: Natasha Sigala, University of Sussex, UK; Jorge Medina, Universidad de Buenos Aires, Argentina

                *Correspondence: Shane M. O'Mara, Trinity College Institute of Neuroscience, Trinity College Dublin, College Green, Dublin 2, Ireland e-mail: smomara@ 123456tcd.ie

                This article was submitted to the journal Frontiers in Systems Neuroscience.

                Article
                10.3389/fnsys.2013.00045
                3757326
                24009563
                c817b6f3-eba9-4905-b026-e1378f6da2c3
                Copyright © 2013 Jankowski, Ronnqvist, Tsanov, Vann, Wright, Erichsen, Aggleton, and O'Mara.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 19 April 2013
                : 08 August 2013
                Page count
                Figures: 5, Tables: 0, Equations: 0, References: 114, Pages: 12, Words: 9527
                Categories
                Neuroscience
                Review Article

                Neurosciences
                anterior thalamus,memory,spatial navigation,theta rhythm,head direction cells
                Neurosciences
                anterior thalamus, memory, spatial navigation, theta rhythm, head direction cells

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