Synaptic Interactions Underlying Synchronized Inhibition in the Basal Amygdala: Evidence for Existence of Two Types of Projection Cells

Center for Molecular and Behavioral Neuroscience, Rutgers, The State University of New Jersey, Newark, New Jersey 07102, USA.
Journal of Neurophysiology (Impact Factor: 3.04). 11/2010; 105(2):687-96. DOI: 10.1152/jn.00732.2010
Source: PubMed

ABSTRACT The basal amygdala (BA) plays a key role in mediating the facilitating effects of emotions on memory. Recent findings indicate that this function depends on the ability of BA neurons to generate coherent oscillatory activity, facilitating synaptic plasticity in target neurons. However, the mechanisms allowing BA neurons to synchronize their activity remain poorly understood. Here, we aimed to shed light on this question, focusing on a slow periodic inhibitory oscillation previously observed in the BA in vitro. Paired patch recordings showed that these large inhibitory postsynaptic potentials (IPSPs) occur almost synchronously in BA projection neurons, that they were typically not preceded by excitatory postsynaptic potentials (EPSPs), and that they had little or no correlate in neighboring amygdala nuclei or cortical fields. The initial phase of the IPSPs was associated with an increase in membrane potential fluctuations at 50-100 Hz. In keeping with this, the IPSPs seen in projection cells were correlated with repetitive firing at 50-100 Hz in presumed interneurons and they could be abolished by picrotoxin. However, the IPSPs were also sensitive to 6-cyano-7-nitroquinoxaline-2,3-dione, implying that they arose from the interplay between glutamatergic and GABAergic BA neurons. In support of this idea, we identified a small subset of projection cells (15%), positively identified as such by retrograde labeling from BA projection sites, that began firing shortly before the IPSP onset and presumably drove interneuronal firing. These results add to a rapidly growing body of data indicating that the BA contains at least two distinct types of projection cells that vary in their relation with interneurons and extra-amygdala targets.

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    • "Our data are consistent with this finding because presentation of a tone predicting a footshock significantly increased c-Fos expression in BA PVINs in WT mice. PVINs target the perisomatic region of PNs (Bienvenu et al, 2012), inhibiting and synchronizing their firing (Popescu and Paré, 2011; Ryan et al, 2012; Woodruff and Sah, 2007) and disinhibiting their dendrites (Wolff et al, 2014). Hence, they tightly control the BLA output to the central amygdala, orchestrating fear responses. "
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    • "The examination of neural inhibition continues, and current neurophysiology examines inhibition in relation to sensory adaptation [12], neural oscillations [13] and neuroscience of behavior [14]. Simpler networks rely on inhibition [15] and central nervous system 'gating' via inhibition is critical at every level from spinal cord (e.g., pain, [16]) to cerebellum [17] to midbrain [18] to different forebrain regions (cortex: [19]; striatum: [20] 2002; hippocampus: [21]; amygdala: [22]). A gating function is common to all inhibitory mechanisms. "
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