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A Cellular Mechanism for Main and Accessory Olfactory Integration at the Medial Amygdala

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A Cellular Mechanism for Main and Accessory Olfactory Integration at the Medial Amygdala The Journal of Neuroscience, February 17, 2016 • 36(7):2083–2085 • 2083 Journal Club Editor’s Note: These short, critical reviews of recent papers in the Journal, written exclusively by graduate students or postdoctoral fellows, are intended to summarize the important findings of the paper and provide additional insight and commentary. For more information on the format and purpose of the Journal Club, please see http://www.jneurosci.org/misc/ifa_features.shtml. A Cellular Mechanism for Main and Accessory Olfactory Integration at the Medial Amygdala E. Mae Guthman1* and XJorge Vera2* 1Neuroscience Graduate Program, University of Colorado Anschutz Medical Campus, Aurora, Colorado 80045, and 2Departamento de Biología, Universidad de Chile, Santiago, Chile, 7800003 Review of Keshavarzi et al. Many vertebrates rely on their accessory (Sua´rez et al., 2012). Chemical cues reach thalamus (Keshavarzi et al., 2014), and and main olfactory systems (AOS and the AOS at a specialized sensory epithe- predator odors activate neurons in both re- MOS, respectively) to interact with their lium located in the vomeronasal organ gions (Pe´rez-Go´mez et al., 2015). Ventro- environment. Shaped by evolution to (VNO), a close-ended tubular structure medial hypothalamic neuronal activity is drive the perception of volatile and non- connected to the nostrils and positioned both necessary (Kunwar et al., 2015) and volatile molecules (for review, see Sua´rez at the base of the medial septum. The sufficient (Kunwar et al., 2015; Pe´rez- et al., 2012), these sensory systems allow VNO is sequestered from airflow; thus, Go´mez et al., 2015) to drive defensive be- animals to react and learn about the the chemical cues must solubilize with na- haviors. Thus, the MePV processes chemical distinct sets of chemical stimuli they en- sal fluids before entering the VNO via an cues detected by the AOS and transmits the counter. The AOS detects molecules with active pumping mechanism (Meredith processed signal to the hypothalamic nuclei evolutionarily stable and predictable and O’Connell, 1979). Sensory neurons to initiate the output associated with innate meaning, such as the molecules emitted located in the VNO epithelium transduce behavioral responses. by predators and conspecifics—collec- the chemical cues and project to the acces- Unlike AOB output neurons, MOB tively known as semiochemicals. The AOS sory olfactory bulb (AOB), the first pro- output neurons do not directly project to promotes innate behavioral responses cessing station of the AOS. The time the medial amygdala; instead, they project when these cues are detected (Wilson and course of activation of AOS neurons un- to a variety of higher-order processing Stevenson, 2006). Conversely, the MOS der naturalistic conditions is character- centers in the olfactory cortices (for re- detects chemical cues that have no innate ized by a slow increase in firing frequency view, see Bekkers and Suzuki, 2013). One meaning and helps to assign meaning to (in the range of seconds) and a sustained of their targets is the cortical amygdala them through associative learning pro- response, without adaptation (Luo et al., (CoA), which in turn sends projections to cesses (Wilson and Stevenson, 2006). 2003). In contrast, odorant molecules the medial amygdala (McDonald, 1998, Besides these functional differences, reach the MOS at the olfactory mucosa via their Table 3). These latter projections the AOS and MOS differ in how molecules airflow produced by an animal’s sniffing provide a means by which information reach the sensory epithelium, how the behavior. Olfactory receptor neurons lo- from the MOS can influence AOS pro- sensory information is processed, and cated in the main olfactory epithelium cessing in the medial amygdala. In fact, where the processed information is sent (MOE) transduce the odorants and trans- although traditionally viewed as function- mit their signal to the main olfactory bulb ally independent systems, recent evidence Received Nov. 30, 2015; revised Jan. 9, 2016; accepted Jan. 11, 2016. (MOB), evoking a fast response on the suggests that the MOS contributes to the We thank Ashley Bourke, Christian Cea-Del Rio, Jaclyn Essig, Molly millisecond timescale (Shusterman et al., ability of the AOS to generate innate re- Huntsman, Diego Restrepo, Jorge Mpodozis, Magdalena Sanhueza, and 2011). sponses to biologically relevant molecules Rodrigo Suarez for critical review of the manuscript, and Maritza On˜ate for assistance in figure construction. A major target of AOB output neurons is (Martínez-García et al., 2009). How these The authors declare no competing financial interests. the medial amygdala (Sua´rez et al., 2012). systems interact at the cellular level was *E.M.G. and J.V. contributed equally to this work. Within the medial amygdala, neurons in the unknown until recently, however. Correspondence should be addressed to Jorge Vera, Departamento de posteroventral division (MePV) respond to In a recent study published in The Biología, Universidad de Chile, Las Palmeras #3425, Santiago, Chile, 7800003. E-mail: [email protected]. semiochemicals from predators (Bergan et Journal of Neuroscience, Keshavarzi et al. DOI:10.1523/JNEUROSCI.4304-15.2016 al., 2014; Pe´rez-Go´mez et al., 2015). MePV (2015) provided novel evidence that AOS Copyright © 2016 the authors 0270-6474/16/362083-03$15.00/0 neurons project to the ventromedial hypo- and MOS inputs converge on individual 2084 • J. Neurosci., February 17, 2016 • 36(7):2083–2085 Guthman and Vera • Journal Club MePV HYP Behavioral response MOE MOB CoA Associative Learning ? VNO AOB Figure1. Proposedcellularmechanismforassociativelearningbetweenaccessoryandmainolfactorypathways.MOS(green)inputsynapsesattheproximaldendritesofMePVneuronsandAOS (orange) synapses at distal dendritic sites. Small colored shapes on the left represent a variety of molecules. Voltage traces to the right represent the effect of associative learning on MePV neuronal responses to MOS and AOS input. medial amygdala neurons. The authors and recorded evoked responses under greater somatic depolarization (Magee, used acute coronal brain slices from whole-cell current-clamp. MePV neurons 2000). GAD67-GFP transgenic mice, which al- responded to stimulation of AOB input Interestingly, Keshavarzi et al. (2015) lowed detection of non-GABAergic (non- with increasing depolarization up to found that nearly 50% of the AOB-driven GFP expressing) projection neurons in threshold, at which point they fired a train somatic depolarization of MePV neurons the MePV, as well as selective and reliable of action potentials. In contrast, the neu- depended on NMDARs, whereas CoA- electrical stimulation of CoA and AOB in- rons responded to identical stimulation of driven somatic depolarization showed puts (via direct electrical stimulation of CoA input with subthreshold voltage re- no dependence on NMDARs despite the deep CoA layers lateral to the MePV and sponses (Keshavarzi et al., 2015, their Fig. fact that synapses associated with CoA in- the superficial molecular layer of MePV, 6A). The differential functional impact of put showed NMDAR-mediated currents respectively). Using standard electrophys- AOB and CoA inputs emerges as a re- (Keshavarzi et al., 2015, their Figs. 2A, iological techniques, Keshavarzi et al. markable characteristic of the MeA neu- 6B–D). In fact, this finding is consistent (2015) demonstrated that individual ronal circuits, displaying synaptic and with the increase in the amplitude of MePV neurons receive excitatory input electrical properties that strongly favor NMDAR-mediated currents at distal syn- from both AOS and MOS, thereby serving the distal AOB inputs. apses that occurs in hippocampal neurons as convergent hubs for both pathways. Neurons use different mechanisms to as a mechanism to increase their somatic Importantly, the authors showed that the compensate for dendritic filtering of distal impact (Magee, 2000). excitatory input from both systems was synaptic inputs (for review, see Magee, It seems plausible that the anatomical mediated by AMPA and NMDA receptors 2000). For example, in hippocampal and and functional segregation of inputs onto (AMPAR and NMDAR, respectively; cortical pyramidal neurons, active con- MePV neurons operates as a cellular mech- Keshavarzi et al., 2015, their Fig. 2A). ductances enhance dendritic propagation anism for associative learning between the In addition, the authors used a battery of distant inputs (Migliore and Shepherd, AOS and MOS. According to the available of techniques, including current-source 2002). Additionally, in these same neu- data, it can be speculated that under simul- density analysis of evoked synaptic poten- rons, synaptic current amplitude in- taneous activation of both pathways, AOB tials, selective blockade of distal synapses, creases proportionally with distance from inputs will depolarize MePV neurons to and calcium imaging paired with whole- the soma such that the somatic impact of threshold, promoting correlated firing be- cell recordings, to reveal that the inputs proximal and distal inputs is equivalent tween the MePV neurons and CoA input. from the two olfactory systems are spa- (Magee, 2000). One mechanism for this This correlated activity between the MePV tially segregated on amygdalar neurons. increase in current amplitude at distal neurons and CoA input would promote Specifically, they demonstrate that AOB synapses is an increase in AMPAR num- NMDAR-dependent long-term synaptic inputs produced synaptic depolarization
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