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      Circuits Regulating Pleasure and Happiness: The Evolution of the Amygdalar-Hippocampal-Habenular Connectivity in Vertebrates

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          Abstract

          Appetitive-searching (reward-seeking) and distress-avoiding (misery-fleeing) behavior are essential for all free moving animals to stay alive and to have offspring. Therefore, even the oldest ocean-dwelling animal creatures, living about 560 million years ago and human ancestors, must have been capable of generating these behaviors. The current article describes the evolution of the forebrain with special reference to the development of the misery-fleeing system. Although, the earliest vertebrate ancestor already possessed a dorsal pallium, which corresponds to the human neocortex, the structure and function of the neocortex was acquired quite recently within the mammalian evolutionary line. Up to, and including, amphibians, the dorsal pallium can be considered to be an extension of the medial pallium, which later develops into the hippocampus. The ventral and lateral pallium largely go up into the corticoid part of the amygdala. The striatopallidum of these early vertebrates becomes extended amygdala, consisting of centromedial amygdala (striatum) connected with the bed nucleus of the stria terminalis (pallidum). This amygdaloid system gives output to hypothalamus and brainstem, but also a connection with the cerebral cortex exists, which in part was created after the development of the more recent cerebral neocortex. Apart from bidirectional connectivity with the hippocampal complex, this route can also be considered to be an output channel as the fornix connects the hippocampus with the medial septum, which is the most important input structure of the medial habenula. The medial habenula regulates the activity of midbrain structures adjusting the intensity of the misery-fleeing response. Within the bed nucleus of the stria terminalis the human homolog of the ancient lateral habenula-projecting globus pallidus may exist; this structure is important for the evaluation of efficacy of the reward-seeking response. The described organization offers a framework for the regulation of the stress response, including the medial habenula and the subgenual cingulate cortex, in which dysfunction may explain the major symptoms of mood and anxiety disorders.

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          Parallel organization of functionally segregated circuits linking basal ganglia and cortex.

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            Ventromedial prefrontal-subcortical systems and the generation of affective meaning.

            The ventromedial prefrontal cortex (vmPFC) comprises a set of interconnected regions that integrate information from affective sensory and social cues, long-term memory, and representations of the 'self'. Alhough the vmPFC is implicated in a variety of seemingly disparate processes, these processes are organized around a common theme. The vmPFC is not necessary for affective responses per se, but is critical when affective responses are shaped by conceptual information about specific outcomes. The vmPFC thus functions as a hub that links concepts with brainstem systems capable of coordinating organism-wide emotional behavior, a process we describe in terms of the generation of affective meaning, and which could explain the common role played by the vmPFC in a range of experimental paradigms. Copyright © 2012 Elsevier Ltd. All rights reserved.
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              The structural and functional connectivity of the amygdala: from normal emotion to pathological anxiety.

              The dynamic interactions between the amygdala and the medial prefrontal cortex (mPFC) are usefully conceptualized as a circuit that both allows us to react automatically to biologically relevant predictive stimuli as well as regulate these reactions when the situation calls for it. In this review, we will begin by discussing the role of this amygdala-mPFC circuitry in the conditioning and extinction of aversive learning in animals. We will then relate these data to emotional regulation paradigms in humans. Finally, we will consider how these processes are compromised in normal and pathological anxiety. We conclude that the capacity for efficient crosstalk between the amygdala and the mPFC, which is represented as the strength of the amygdala-mPFC circuitry, is crucial to beneficial outcomes in terms of reported anxiety. Copyright © 2011 Elsevier B.V. All rights reserved.
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                Author and article information

                Contributors
                Journal
                Front Neurosci
                Front Neurosci
                Front. Neurosci.
                Frontiers in Neuroscience
                Frontiers Media S.A.
                1662-4548
                1662-453X
                22 November 2016
                2016
                : 10
                : 539
                Affiliations
                [1] 1Department of Pharmacy, University of Groningen Groningen, Netherlands
                [2] 2GGZ Westelijk Noord-Brabant (GGZ-WNB) Halsteren, Netherlands
                [3] 3Mental Health Research Institute, Tomsk National Research Medical Center of the Russian Academy of Sciences Tomsk, Russia
                [4] 4Department of Ecology and Basic Safety, National Research Tomsk Polytechnic University Tomsk, Russia
                Author notes

                Edited by: J. Michael Williams, Drexel University, USA

                Reviewed by: Lei Chang, University of Macau, Macau; Fernando Garcia-Moreno, Achucarro Basque Center for Neuroscience, Spain

                *Correspondence: Anton J. M. Loonen a.j.m.loonen@ 123456rug.nl

                This article was submitted to Evolutionary Psychology and Neuroscience, a section of the journal Frontiers in Neuroscience

                Article
                10.3389/fnins.2016.00539
                5118621
                27920666
                5969ac23-d672-48b2-b479-4d687281c754
                Copyright © 2016 Loonen and Ivanova.

                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
                : 17 September 2016
                : 04 November 2016
                Page count
                Figures: 8, Tables: 0, Equations: 0, References: 117, Pages: 17, Words: 12712
                Categories
                Neuroscience
                Hypothesis and Theory

                Neurosciences
                cerebral cortex,amygdala,hippocampus,habenula,evolution,reward,stress
                Neurosciences
                cerebral cortex, amygdala, hippocampus, habenula, evolution, reward, stress

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