Target-Specific Suppression of GABA Release from Parvalbumin Interneurons in the Basolateral Amygdala by Dopamine

Dopamine (DA) in the basolateral amygdala (BLA) promotes fear learning by disinhibiting principal neurons (PNs) and enabling synaptic plasticity in their sensory inputs. While BLA interneurons (INs) are heterogeneous, it is unclear which interneuron subtypes decrease GABAergic input to PNs in the presence of DA. Here, using cell type-selective photostimulation by channelrhodopsin 2 in BLA slices from mouse brain, we examined the role of parvalbumin-positive INs (PV-INs), the major interneuronal subpopulation in BLA, in the disinhibitory effect of DA. We found that DA selectively suppressed GABAergic transmission from PV-INs to PNs by acting on presynaptic D2 receptors, and this effect was mimicked by Rp-cAMP, an inhibitor of cAMP-dependent signaling. In contrast, DA did not alter GABA release from PV-INs to INs. Furthermore, neither suppressing cAMP-dependent signaling by Rp-cAMP nor enhancing it by forskolin altered GABA release from PV-INs to BLA INs. Overall, DA disinhibits BLA, at least in part, by suppressing GABA release from PV-INs in the target cell-specific manner that results from differential control of this release by cAMP-dependent signaling.

[1]  B. Moghaddam,et al.  Dopaminergic Innervation of the Amygdala Is Highly Responsive to Stress , 1999, Journal of neurochemistry.

[2]  Raag D. Airan,et al.  Optogenetic interrogation of neural circuits: technology for probing mammalian brain structures , 2010, Nature Protocols.

[3]  H. Markram,et al.  Differential signaling via the same axon of neocortical pyramidal neurons. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[4]  Y. Yanagawa,et al.  A Specialized Subclass of Interneurons Mediates Dopaminergic Facilitation of Amygdala Function , 2005, Neuron.

[5]  T. Südhof,et al.  Endocannabinoid-Mediated Long-Term Plasticity Requires cAMP/PKA Signaling and RIM1α , 2007, Neuron.

[6]  S. Sternson,et al.  AGRP neurons are sufficient to orchestrate feeding behavior rapidly and without training , 2010, Nature Neuroscience.

[7]  R. Gainetdinov,et al.  The Physiology, Signaling, and Pharmacology of Dopamine Receptors , 2011, Pharmacological Reviews.

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

[9]  F. Mascagni,et al.  Dopaminergic innervation of pyramidal cells in the rat basolateral amygdala , 2009, Brain Structure and Function.

[10]  B. Rudy,et al.  Perisomatic GABA Release and Thalamocortical Integration onto Neocortical Excitatory Cells Are Regulated by Neuromodulators , 2008, Neuron.

[11]  Marco Capogna,et al.  Cell-Type-Specific Recruitment of Amygdala Interneurons to Hippocampal Theta Rhythm and Noxious Stimuli In Vivo , 2012, Neuron.

[12]  R. Palmiter,et al.  Dopamine Is Necessary for Cue-Dependent Fear Conditioning , 2009, The Journal of Neuroscience.

[13]  G. Phillips,et al.  Enhanced dopamine efflux in the amygdala by a predictive, but not a non-predictive, stimulus: facilitation by prior repeated d-amphetamine , 1999, Neuroscience.

[14]  Shigeru Watanabe,et al.  Enhancement of delayed release of dopamine in the amygdala induced by conditioned fear stress in methamphetamine-sensitized rats. , 2002, European journal of pharmacology.

[15]  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.

[16]  B. Gähwiler,et al.  Target cell-specific modulation of transmitter release at terminals from a single axon. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[17]  F. Mascagni,et al.  Coupled Networks of Parvalbumin-Immunoreactive Interneurons in the Rat Basolateral Amygdala , 2005, The Journal of Neuroscience.

[18]  S. Nelson,et al.  A Resource of Cre Driver Lines for Genetic Targeting of GABAergic Neurons in Cerebral Cortex , 2011, Neuron.

[19]  A. McDonald,et al.  Parvalbumin-containing neurons in the rat basolateral amygdala: morphology and co-localization of Calbindin-D 28k , 2001, Neuroscience.

[20]  D. Paré,et al.  Plastic synaptic networks of the amygdala for the acquisition, expression, and extinction of conditioned fear. , 2010, Physiological reviews.

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

[22]  F. Mascagni,et al.  Colocalization of calcium-binding proteins and GABA in neurons of the rat basolateral amygdala , 2001, Neuroscience.

[23]  Pedro Grandes,et al.  Dopaminergic Modulation of Endocannabinoid-Mediated Plasticity at GABAergic Synapses in the Prefrontal Cortex , 2010, The Journal of Neuroscience.

[24]  A. Grace,et al.  Dopamine Attenuates Prefrontal Cortical Suppression of Sensory Inputs to the Basolateral Amygdala of Rats , 2001, The Journal of Neuroscience.

[25]  Joseph E LeDoux.  Emotion circuits in the brain. , 2009, Annual review of neuroscience.

[26]  S. Arber,et al.  A Developmental Switch in the Response of DRG Neurons to ETS Transcription Factor Signaling , 2005, PLoS biology.

[27]  S. Sesack,et al.  Ultrastructural analysis of prefrontal cortical inputs to the rat amygdala: spatial relationships to presumed dopamine axons and D1 and D2 receptors , 2008, Brain Structure and Function.

[28]  Stefan Hefft,et al.  Asynchronous GABA release generates long-lasting inhibition at a hippocampal interneuron–principal neuron synapse , 2005, Nature Neuroscience.

[29]  George Kunos,et al.  Presynaptic Specificity of Endocannabinoid Signaling in the Hippocampus , 2001, Neuron.

[30]  E. Asan.  Ultrastructural features of tyrosine-hydroxylase-immunoreactive afferents and their targets in the rat amygdala , 1997, Cell and Tissue Research.

[31]  C. Pinard,et al.  Dopaminergic innervation of interneurons in the rat basolateral amygdala , 2008, Neuroscience.

[32]  T. Freund,et al.  Perisomatic Inhibition , 2007, Neuron.

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

[34]  Y. Humeau,et al.  Dopamine gates LTP induction in lateral amygdala by suppressing feedforward inhibition , 2003, Nature Neuroscience.