Paraventricular Thalamus Balances Danger and Reward

被引:79
作者
Choi, Eun A. [1 ]
McNally, Gavan P. [1 ]
机构
[1] Univ New South Wales, Sch Psychol, Sydney, NSW 2052, Australia
基金
澳大利亚研究理事会;
关键词
competition; danger; paraventricular thalamus; reward; APPETITIVE-AVERSIVE INTERACTIONS; MEDIODORSAL THALAMUS; NUCLEUS-ACCUMBENS; FEAR EXTINCTION; AMYGDALA; CIRCUITS; SPECIFICITY; RECEPTORS; MIDLINE; INPUT;
D O I
10.1523/JNEUROSCI.3320-16.2017
中图分类号
Q189 [神经科学];
学科分类号
071006 ;
摘要
Foraging animals balance the need to seek food and energy against the accompanying dangers of injury and predation. To do so, they rely on learning systems encoding reward and danger. Whereas much is known about these separate learning systems, little is known about how they interact to shape and guide behavior. Here we show a key role for the rat paraventricular nucleus of the thalamus (PVT), a nucleus of the dorsal midline thalamus, in this interaction. First, we show behavioral competition between reward and danger: the opportunity to seek food reward negatively modulates expression of species-typical defensive behavior. Then, using a chemogenetic approach expressing the inhibitory hM4Di designer receptor exclusively activated by a designer drug in PVT neurons, we show that the PVTis central to this behavioral competition. Chemogenetic PVT silencing biases behavior toward either defense or reward depending on the experimental conditions, but does not consistently favor expression of one over the other. This bias could not be attributed to changes in fear memory retrieval, learned safety, or memory interference. Rather, our results demonstrate that the PVT is essential for balancing conflicting behavioral tendencies toward danger and reward, enabling adaptive responding under this basic selection pressure.
引用
收藏
页码:3018 / 3029
页数:12
相关论文
共 62 条
[31]   Lesions of the posterior paraventricular nucleus of the thalamus attenuate fear expression [J].
Li, Yonghui ;
Dong, Xinwen ;
Li, Sa ;
Kirouac, Gilbert J. .
FRONTIERS IN BEHAVIORAL NEUROSCIENCE, 2014, 8
[32]   Designer receptors show role for ventral pallidum input to ventral tegmental area in cocaine seeking [J].
Mahler, Stephen V. ;
Vazey, Elena M. ;
Beckley, Jacob T. ;
Keistler, Colby R. ;
McGlinchey, Ellen M. ;
Kaufling, Jennifer ;
Wilson, Steven P. ;
Deisseroth, Karl ;
Woodward, John J. ;
Aston-Jones, Gary .
NATURE NEUROSCIENCE, 2014, 17 (04) :577-U136
[33]   Neuronal signalling of fear memory [J].
Maren, S ;
Quirk, GJ .
NATURE REVIEWS NEUROSCIENCE, 2004, 5 (11) :844-852
[34]   Representation of negative motivational value in the primate lateral habenula [J].
Matsumoto, Masayuki ;
Hikosaka, Okihide .
NATURE NEUROSCIENCE, 2009, 12 (01) :77-84
[35]   The fear circuit of the mouse forebrain: connections between the mediodorsal thalamus, frontal cortices and basolateral amygdala [J].
Matyas, Ferenc ;
Lee, JoonHyuk ;
Shin, Hee-Sup ;
Acsady, Laszlo .
EUROPEAN JOURNAL OF NEUROSCIENCE, 2014, 39 (11) :1810-1823
[36]   The mediodorsal thalamus as a higher order thalamic relay nucleus important for learning and decision-making [J].
Mitchell, Anna S. .
NEUROSCIENCE AND BIOBEHAVIORAL REVIEWS, 2015, 54 :76-88
[37]   Advances in Understanding Mechanisms of Thalamic Relays in Cognition and Behavior [J].
Mitchell, Anna S. ;
Sherman, S. Murray ;
Sommer, Marc A. ;
Mair, Robert G. ;
Vertes, Robert P. ;
Chudasama, Yogita .
JOURNAL OF NEUROSCIENCE, 2014, 34 (46) :15340-15346
[38]   Extinction-Reconsolidation Boundaries: Key to Persistent Attenuation of Fear Memories [J].
Monfils, Marie-H. ;
Cowansage, Kiriana K. ;
Klann, Eric ;
LeDoux, Joseph E. .
SCIENCE, 2009, 324 (5929) :951-955
[39]   A circuit mechanism for differentiating positive and negative associations [J].
Namburi, Praneeth ;
Beyeler, Anna ;
Yorozu, Suzuko ;
Calhoon, Gwendolyn G. ;
Halbert, Sarah A. ;
Wichmann, Romy ;
Holden, Stephanie S. ;
Mertens, Kim L. ;
Anahtar, Melodi ;
Felix-Ortiz, Ada C. ;
Wickersham, Ian R. ;
Gray, Jesse M. ;
Tye, Kay M. .
NATURE, 2015, 520 (7549) :675-U208
[40]   Neural correlates of appetitive-aversive interactions in Pavlovian fear conditioning [J].
Nasser, Helen M. ;
McNally, Gavan P. .
LEARNING & MEMORY, 2013, 20 (04) :220-228