Membrane and synaptic properties of pyramidal neurons in the anterior olfactory nucleus

Abstract

McGinley MJ, Westbrook GL. Membrane and synaptic properties of pyramidal neurons in the anterior olfactory nucleus. J Neurophysiol 105: 1444Neurophysiol 105: -1453Neurophysiol 105: , 2011. First published December 1, 2010; doi:10.1152/jn.00715.2010.-The anterior olfactory nucleus (AON) is positioned to coordinate activity between the piriform cortex and olfactory bulbs, yet the physiology of AON principal neurons has been little explored. Here, we examined the membrane properties and excitatory synapses of AON principal neurons in brain slices of PND22-28 mice and compared their properties to principal cells in other olfactory cortical areas. AON principal neurons had firing rates, spike rate adaptation, spike widths, and I-V relationships that were generally similar to pyramidal neurons in piriform cortex, and typical of cerebral cortex, consistent with a role for AON in cortical processing. Principal neurons in AON had more hyperpolarized action potential thresholds, smaller afterhyperpolarizations, and tended to fire doublets of action potentials on depolarization compared with ventral anterior piriform cortex and the adjacent epileptogenic region preendopiriform nucleus (pEN). Thus, AON pyramidal neurons have enhanced membrane excitability compared with surrounding subregions. Interestingly, principal neurons in pEN were the least excitable, as measured by a larger input conductance, lower firing rates, and more inward rectification. Afferent and recurrent excitatory synapses onto AON pyramidal neurons had small amplitudes, paired pulse facilitation at afferent synapses, and GABA B modulation at recurrent synapses, a pattern similar to piriform cortex. The enhanced membrane excitability and recurrent synaptic excitation within the AON, together with its widespread outputs, suggest that the AON can boost and distribute activity in feedforward and feedback circuits throughout the olfactory system. piriform cortex; preendopiriform nucleus; area tempestas; afterhyperpolarization; inward rectifying potassium channels; cable properties; pyramidal neuron WITH ITS FEEDBACK CONNECTIONS to the ipsilateral and contralateral olfactory bulbs, and feedforward connections to the piriform cortex, the anterior olfactory nucleus (AON) is poised to coordinate the flow of activity between olfactory areas (Alheid et al. 1984;Reyher et al. 1988; Haberly and Price 1978;Yan et al. 2008). The entire AON receives input from the ipsilateral olfactory bulb, but it is divided into subregions by the topography of output projections and cytoarchitecture ( Principal neurons in pars principalis of AON are particularly well positioned to influence activity in piriform cortex for several reasons. Tufted cells in the olfactory bulb project selectively to the AON as well as the neighboring ventrorostral anterior piriform cortex (APC V-R ) (Matsutani et al. 1989). Tufted cells show enhanced excitation relative to mitral cells, which project to the entire olfactory cortex (Schneider and Scott 1983;Orona et al. 1984;Scott et al. 1985; Christie...

Hierarchical excitatory synaptic connectivity in mouse olfactory cortex

“…Furthermore, when AOC was separated with a knife cut from the pEN and piriform cortex stimulation of AOC no longer generated bursts (Fig. S5), even though the AOC exhibits recurrent connectivity (22). Thus, the pairwise variance patterns seen in our recordings are most consistent with hierarchical connectivity critically involving the pEN.…”

“…In addition, the strength of individual connections and background firing rates must be low (25,26). These conditions match the properties of excitatory synapses and neuronal excitability in brain slices of olfactory cortex (22). However, isolated AOC did not generate network bursts in our experiments, so not all subregions of olfactory cortex are equivalent in this regard.…”

“…Blockade of NMDA receptors revealed a slow outward current that could be blocked by the GABA B antagonist CGP55845 (10 μM; ref. 22). Thus, picrotoxin and CPP were included in subsequent experiments to examine bursts generated by fast excitatory synaptic activity.…”

The Olfactory System

“…Other outputs and neurochemical features of AON neurons are discussed elsewhere (Shipley et al, 2004;Meyer et al, 2006). AON pyramidal cells are glutamatergic and exhibit many electrophysiological properties in common with Pir pyramidal cells, including responses to MTC input (McGinley and Westbrook, 2011;Markopoulos et al, 2012). In addition to the MOB, AOB receives input from other POC structures and modulatory inputs from the raphe nuclei, LC and DB (Shipley et al, 2004).…”

A direct anterior cingulate pathway to the primate primary olfactory cortex may control attention to olfaction

“…Activation of as few as 1% of piriform neurons can recruit an ensemble of odor responsive neurons (Franks et al 2011) and AON neurons show even more enhanced excitability (McGinley and Westbrook 2011). Consequently, excitation of a small number of AON excitatory neurons by the efficient ACC pathway may have widespread and significant effects throughout the primary olfactory cortex, as summarized in Figure 7.…”