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1.  Spike-Timing Precision and Neuronal Synchrony Are Enhanced by an Interaction between Synaptic Inhibition and Membrane Oscillations in the Amygdala 
PLoS ONE  2012;7(4):e35320.
The basolateral complex of the amygdala (BLA) is a critical component of the neural circuit regulating fear learning. During fear learning and recall, the amygdala and other brain regions, including the hippocampus and prefrontal cortex, exhibit phase-locked oscillations in the high delta/low theta frequency band (∼2–6 Hz) that have been shown to contribute to the learning process. Network oscillations are commonly generated by inhibitory synaptic input that coordinates action potentials in groups of neurons. In the rat BLA, principal neurons spontaneously receive synchronized, inhibitory input in the form of compound, rhythmic, inhibitory postsynaptic potentials (IPSPs), likely originating from burst-firing parvalbumin interneurons. Here we investigated the role of compound IPSPs in the rat and rhesus macaque BLA in regulating action potential synchrony and spike-timing precision. Furthermore, because principal neurons exhibit intrinsic oscillatory properties and resonance between 4 and 5 Hz, in the same frequency band observed during fear, we investigated whether compound IPSPs and intrinsic oscillations interact to promote rhythmic activity in the BLA at this frequency. Using whole-cell patch clamp in brain slices, we demonstrate that compound IPSPs, which occur spontaneously and are synchronized across principal neurons in both the rat and primate BLA, significantly improve spike-timing precision in BLA principal neurons for a window of ∼300 ms following each IPSP. We also show that compound IPSPs coordinate the firing of pairs of BLA principal neurons, and significantly improve spike synchrony for a window of ∼130 ms. Compound IPSPs enhance a 5 Hz calcium-dependent membrane potential oscillation (MPO) in these neurons, likely contributing to the improvement in spike-timing precision and synchronization of spiking. Activation of the cAMP-PKA signaling cascade enhanced the MPO, and inhibition of this cascade blocked the MPO. We discuss these results in the context of spike-timing dependent plasticity and modulation by neurotransmitters important for fear learning, such as dopamine.
doi:10.1371/journal.pone.0035320
PMCID: PMC3338510  PMID: 22563382
2.  A transcriptomic analysis of type I-III neurons in the bed nucleus of the stria terminalis 
The activity of neurons in the anterolateral cell group of the bed nucleus of the stria terminalis (BNSTALG) plays a critical role in anxiety- and stress-related behaviors. Histochemical studies have suggested that multiple distinct neuronal phenotypes exist in the BNSTALG. Consistent with this observation, the physiological properties of BNSTALG neurons are also heterogeneous, and three distinct cell types can be defined (Type I–III) based primarily on their expression of four key membrane currents, namely Ih, IA, IT, and IK(IR). Significantly, all four channels are multimeric proteins and can comprise of more than one pore-forming α subunit. Hence, differential expression of α subunits may further diversify the neuronal population. However, nothing is known about the relative expression of these ion channel α subunits in BNSTALG neurons.
We have addressed this lacuna by combining whole cell patch clamp recording together with single cell reverse transcriptase polymerase chain reaction (scRT-PCR) to assess the mRNA transcript expression for each of the subunits for the four key ion channels in Type I-III neurons of the BNSTALG. Here, cytosolic mRNA from single neurons was probed for the expression of transcripts for each of the α subunits of Ih (HCN1- HCN4), IT (Cav3.1- Cav3.3), IA (Kv1.4, Kv3.4, Kv4.1- Kv 4.3) and IK(IR) (Kir2.1-Kir2.4).
An unbiased hierarchical cluster analysis followed by discriminant function analysis revealed that a positive correlation exists between the physiological and genetic phenotype of BNSTALG neurons. Thus, the analysis segregated BNSTALG neurons into 3 distinct groups, based on their α subunit mRNA expression profile, which positively correlated with our existing electrophysiological classification (Type I–III). Furthermore, analysis of mRNA transcript expression in Type I –Type III neurons suggested that, whereas Type I and III neurons appear to represent genetically homologous cell populations, Type II neurons may be further subdivided into three genetically distinct subgroups. These data not only validate our original classification scheme, but further refine the classification at the molecular level, and thus identifies novel targets for potential disruption and/or pharmacotherapeutic intervention in stress-related anxiety-like behaviors.
doi:10.1016/j.mcn.2011.01.011
PMCID: PMC3066260  PMID: 21310239
Bed nucleus of the stria terminalis; ion channels; α subunits; patch clamp recording; single cell reverse transcriptase polymerase chain reaction

Results 1-2 (2)