Functional Properties and Projections of Neurons in the Medial Amygdala

The medial nucleus of the amygdala (MeA) plays a key role in innate emotional behaviors by relaying olfactory information to hypothalamic nuclei involved in reproduction and defense. However, little is known about the neuronal components of this region or their role in the olfactory-processing circuitry of the amygdala. Here, we have characterized neurons in the posteroventral division of the medial amygdala (MePV) using the GAD67-GFP mouse. Based on their electrophysiological properties and GABA expression, unsupervised cluster analysis divided MePV neurons into three types of GABAergic (Types 1–3) and two non-GABAergic cells (Types I and II). All cell types received olfactory synaptic input from the accessory olfactory bulb and, with the exception of Type 2 GABAergic neurons, sent projections to both reproductive and defensive hypothalamic nuclei. Type 2 GABAergic cells formed a chemically and electrically interconnected network of local circuit inhibitory interneurons that resembled neurogliaform cells of the piriform cortex and provided feedforward inhibition of the olfactory-processing circuitry of the MeA. These findings provide a description of the cellular organization and connectivity of the MePV and further our understanding of amygdala circuits involved in olfactory processing and innate emotions.

[1]  Xiling Bian Physiological and morphological characterization of GABAergic neurons in the medial amygdala , 2013, Brain Research.

[2]  Cecília Pardo-Bellver,et al.  Differential efferent projections of the anterior, posteroventral, and posterodorsal subdivisions of the medial amygdala in mice , 2012, Front. Neuroanat..

[3]  Denis Pare,et al.  Amygdala microcircuits mediating fear expression and extinction , 2012, Current Opinion in Neurobiology.

[4]  Johannes E. Schindelin,et al.  Fiji: an open-source platform for biological-image analysis , 2012, Nature Methods.

[5]  Joseph E LeDoux Rethinking the Emotional Brain , 2012, Neuron.

[6]  Norimitsu Suzuki,et al.  Microcircuits Mediating Feedforward and Feedback Synaptic Inhibition in the Piriform Cortex , 2012, The Journal of Neuroscience.

[7]  Donald A. Wilson,et al.  Cortical Processing of Odor Objects , 2011, Neuron.

[8]  M. Scanziani,et al.  How Inhibition Shapes Cortical Activity , 2011, Neuron.

[9]  L. Medina,et al.  Multiple telencephalic and extratelencephalic embryonic domains contribute neurons to the medial extended amygdala , 2011, The Journal of comparative neurology.

[10]  P. Sah,et al.  Interneurons in the basolateral amygdala , 2011, Neuropharmacology.

[11]  Norimitsu Suzuki,et al.  Two Layers of Synaptic Processing by Principal Neurons in Piriform Cortex , 2011, The Journal of Neuroscience.

[12]  N. Canteras,et al.  Amygdalar roles during exposure to a live predator and to a predator-associated context , 2011, Neuroscience.

[13]  David J. Anderson,et al.  Functional identification of an aggression locus in the mouse hypothalamus , 2010, Nature.

[14]  Y. Yanagawa,et al.  A Specific Class of Interneuron Mediates Inhibitory Plasticity in the Lateral Amygdala , 2010, The Journal of Neuroscience.

[15]  Hans-Christian Pape,et al.  GABAergic interneurons in the mouse lateral amygdala: a classification study. , 2010, Journal of neurophysiology.

[16]  J. Bekkers,et al.  Inhibitory neurons in the anterior piriform cortex of the mouse: Classification using molecular markers , 2010, The Journal of comparative neurology.

[17]  Norimitsu Suzuki,et al.  Distinctive classes of GABAergic interneurons provide layer-specific phasic inhibition in the anterior piriform cortex. , 2010, Cerebral cortex.

[18]  C. Poo,et al.  Odor representations in olfactory cortex , 2010 .

[19]  A. Young,et al.  GABAergic inhibitory interneurons in the posterior piriform cortex of the GAD67-GFP mouse. , 2009, Cerebral cortex.

[20]  J. Isaacson,et al.  Odor Representations in Olfactory Cortex: “Sparse” Coding, Global Inhibition, and Oscillations , 2009, Neuron.

[21]  S. Guirado,et al.  Expression of somatostatin and neuropeptide Y in the embryonic, postnatal, and adult mouse amygdalar complex , 2009, The Journal of comparative neurology.

[22]  Demian Battaglia,et al.  Classification of NPY-Expressing Neocortical Interneurons , 2009, The Journal of Neuroscience.

[23]  A. Martínez-Marcos On the organization of olfactory and vomeronasal cortices , 2009, Progress in Neurobiology.

[24]  A. Dall’Oglio,et al.  Dendritic branching features of Golgi-impregnated neurons from the “ventral” medial amygdala subnuclei of adult male and female rats , 2008, Neuroscience Letters.

[25]  E. P. Gardner,et al.  Petilla terminology: nomenclature of features of GABAergic interneurons of the cerebral cortex , 2008, Nature Reviews Neuroscience.

[26]  Y. Yanagawa,et al.  Cortical-like functional organization of the pheromone-processing circuits in the medial amygdala. , 2008, Journal of neurophysiology.

[27]  R. Nelson,et al.  Neural mechanisms of aggression , 2007, Nature Reviews Neuroscience.

[28]  C. Woolley,et al.  Morphological sex differences and laterality in the prepubertal medial amygdala , 2007, The Journal of comparative neurology.

[29]  R. Insausti,et al.  Segregated pathways to the vomeronasal amygdala: differential projections from the anterior and posterior divisions of the accessory olfactory bulb , 2007, The European journal of neuroscience.

[30]  Pankaj Sah,et al.  Networks of Parvalbumin-Positive Interneurons in the Basolateral Amygdala , 2007, The Journal of Neuroscience.

[31]  P. Brennan,et al.  Pheromonal communication in vertebrates , 2006, Nature.

[32]  Norimitsu Suzuki,et al.  Neural Coding by Two Classes of Principal Cells in the Mouse Piriform Cortex , 2006, The Journal of Neuroscience.

[33]  H. Pape,et al.  Classification of projection neurons and interneurons in the rat lateral amygdala based upon cluster analysis , 2006, Molecular and Cellular Neuroscience.

[34]  C. Woolley,et al.  Sexually Dimorphic Synaptic Organization of the Medial Amygdala , 2005, The Journal of Neuroscience.

[35]  Joseph E LeDoux,et al.  Contributions of the Amygdala to Emotion Processing: From Animal Models to Human Behavior , 2005, Neuron.

[36]  Marco Capogna,et al.  Neurogliaform Neurons Form a Novel Inhibitory Network in the Hippocampal CA1 Area , 2005, The Journal of Neuroscience.

[37]  David J. Anderson,et al.  Lhx6 Delineates a Pathway Mediating Innate Reproductive Behaviors from the Amygdala to the Hypothalamus , 2005, Neuron.

[38]  A. Rasia-Filho,et al.  Influence of sex, estrous cycle and motherhood on dendritic spine density in the rat medial amygdala revealed by the Golgi method , 2004, Neuroscience.

[39]  H. Markram,et al.  Interneurons of the neocortical inhibitory system , 2004, Nature Reviews Neuroscience.

[40]  M. Meredith,et al.  Distinctive Responses in the Medial Amygdala to Same-Species and Different-Species Pheromones , 2004, The Journal of Neuroscience.

[41]  R. Apfelbach,et al.  Neural Correlates of Cat Odor-induced Anxiety in Rats: Region-specific Effects of the Benzodiazepine Midazolam , 2022 .

[42]  Elizabeth Hall The amygdala of the cat: A golgi study , 2004, Zeitschrift für Zellforschung und Mikroskopische Anatomie.

[43]  T. Kaneko,et al.  Green fluorescent protein expression and colocalization with calretinin, parvalbumin, and somatostatin in the GAD67‐GFP knock‐in mouse , 2003, The Journal of comparative neurology.

[44]  S. Hestrin,et al.  Synaptic Interactions of Late-Spiking Neocortical Neurons in Layer 1 , 2003, The Journal of Neuroscience.

[45]  M. Scanziani,et al.  Enforcement of Temporal Fidelity in Pyramidal Cells by Somatic Feed-Forward Inhibition , 2001, Science.

[46]  R. Dielenberg,et al.  ‘When a rat smells a cat’: the distribution of Fos immunoreactivity in rat brain following exposure to a predatory odor , 2001, Neuroscience.

[47]  L. Swanson Cerebral hemisphere regulation of motivated behavior 1 1 Published on the World Wide Web on 2 November 2000. , 2000, Brain Research.

[48]  A. Pitkänen,et al.  Distribution of parvalbumin, calretinin, and calbindin‐D28k immunoreactivity in the rat amygdaloid complex and colocalization with γ‐aminobutyric acid , 2000, The Journal of comparative neurology.

[49]  B. Connors,et al.  A network of electrically coupled interneurons drives synchronized inhibition in neocortex , 2000, Nature Neuroscience.

[50]  J. Rossier,et al.  Classification of fusiform neocortical interneurons based on unsupervised clustering. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[51]  K. Mori,et al.  Convergence of segregated pheromonal pathways from the accessory olfactory bulb to the cortex in the mouse , 2000, The European journal of neuroscience.

[52]  Michael Davis,et al.  The amygdala , 2000, Current Biology.

[53]  S. Hestrin,et al.  A network of fast-spiking cells in the neocortex connected by electrical synapses , 1999, Nature.

[54]  B. Connors,et al.  Two networks of electrically coupled inhibitory neurons in neocortex , 1999, Nature.

[55]  M. Cassell,et al.  The Intrinsic Organization of the Central Extended Amygdala , 1999, Annals of the New York Academy of Sciences.

[56]  S. Newman The Medial Extended Amygdala in Male Reproductive Behavior A Node in the Mammalian Social Behavior Network , 1999, Annals of the New York Academy of Sciences.

[57]  Pankaj Sah,et al.  Calcium-permeable AMPA receptors mediate long-term potentiation in interneurons in the amygdala , 1998, Nature.

[58]  L. Swanson,et al.  What is the amygdala? , 1998, Trends in Neurosciences.

[59]  George Paxinos,et al.  The Mouse Brain in Stereotaxic Coordinates , 2001 .

[60]  G. Buzsáki,et al.  Interneurons of the hippocampus , 1998, Hippocampus.

[61]  L. Swanson,et al.  Organization of projections from the basomedial nucleus of the amygdala: A PHAL study in the rat , 1996, The Journal of comparative neurology.

[62]  L. Swanson,et al.  Organization of projections from the medial nucleus of the amygdala: A PHAL study in the rat , 1995, The Journal of comparative neurology.

[63]  M. Meredith,et al.  c-fos expression in vomeronasal pathways of mated or pheromone- stimulated male golden hamsters: contributions from vomeronasal sensory input and expression related to mating performance , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[64]  E. Lauterbach The Amygdala: Neurobiological Aspects of Emotion, Memory, and Mental Dysfunction , 1993 .

[65]  M. Cassell,et al.  Intrinsic GABAergic neurons in the rat central extended amygdala , 1993, The Journal of comparative neurology.

[66]  B. Connors,et al.  Intrinsic firing patterns of diverse neocortical neurons , 1990, Trends in Neurosciences.

[67]  D. McCormick,et al.  Comparative electrophysiology of pyramidal and sparsely spiny stellate neurons of the neocortex. , 1985, Journal of neurophysiology.

[68]  L. Haberly Structure of the piriform cortex of the opossum. I. Description of neuron types with golgi methods , 1983, The Journal of comparative neurology.

[69]  M. Lehman,et al.  Medial nucleus of the amygdala mediates chemosensory control of male hamster sexual behavior. , 1980, Science.

[70]  S. S. Winans,et al.  The differential projections of the olfactory bulb and accessory olfactory bulb in mammals , 1975, The Journal of comparative neurology.

[71]  J. H. Ward Hierarchical Grouping to Optimize an Objective Function , 1963 .

[72]  R. L. Thorndike Who belongs in the family? , 1953 .

[73]  D. Sholl Dendritic organization in the neurons of the visual and motor cortices of the cat. , 1953, Journal of anatomy.

[74]  Sholl Da Dendritic organization in the neurons of the visual and motor cortices of the cat. , 1953 .