Distribution of the Olfactory Fiber Input Into the Olfactory Tubercle of the In Vitro Isolated Guinea Pig Brain

Abstract

Carriero G, Uva L, Gnatkovsky V, de Curtis M. Distribution of the olfactory fiber input into the olfactory tubercle of the in vitro isolated guinea pig brain. J Neurophysiol 101: 1613-1619, 2009. First published October 15, 2008 doi:10.1152/jn.90792.2008. The olfactory tubercle (OT) is a cortical component of the olfactory system involved in reward mechanisms of drug abuse. This region covers an extensive part of the rostral ventral cerebrum and is relatively poorly studied. The intrinsic network interactions evoked by olfactory input are analyzed in the OT of the in vitro isolated guinea pig brain by means of field potential analysis and optical imaging of voltage-sensitive signals. Stimulation of the lateral olfactory tract induces a monosynaptic response that progressively decreases in amplitude from lateral to medial. The monosynaptic input induces a disynaptic response that is proportionally larger in the medial portion of the OT. Direct stimulation of the piriform cortex and subsequent lesion of this pathway showed the existence of an associative disynaptic projection from the anterior part of the piriform cortex to the lateral part of the OT that integrates with the component mediated by the local intra-OT collaterals. Optical and electrophysiological recordings of the signals evoked by stimulation of the olfactory tract during arterial perfusion with the voltage-sensitive dye di-2-ANEPEQ confirmed the pattern of distribution of the mono and disynaptic responses in the OT. Finally, current source density analysis of laminar profiles recorded with 16-channel silicon probes confirmed that the monosynaptic and disynaptic potentials localize in the most superficial and the deep portions of the plexiform layer I, as suggested by previous reports. This study sets the standard for further analysis of the modulation of network properties in this largely unexplored brain region. I N T R O D U C T I O NThe olfactory tubercle (OT) is a tri-laminar cortical structure that occupies a large portion of the basal and rostral surface of the brain, medially to the lateral olfactory tract (LOT). It has been proposed that the meso-limbic system, OT included, is implicated with the nucleus accumbens in reward behaviors associated with psychomotor stimulants. Results obtained in self-administration and conditioned place-preference tests, and the effect of specific lesions in accumbens, suggest the OT is strongly involved in amphetamine reward behaviors (Lyness et al. 1979;Spyraki et al. 1982). No direct evidence, however, indicates OT involvement in cocaine pharmacological effects (Hoebel et al. 1983; Ikemoto and Sharpe 2001;Lyness et al. 1979;Phillips et al. 1994). Cocaine injection into the OT induces robust locomotion and rearing (Ikemoto 2002; Ikemoto and Witkin 2003). Recently, it was shown that rats self-administer more cocaine in OT than into the nucleus accumbens during cocaine reward tests. Moreover, direct injections of dopamine receptor antagonist into the OT are able to abolish this reward aspect to cocaine (Ikem...

Odor- and state-dependent olfactory tubercle local field potential dynamics in awake rats

“…Based upon the hypothesized roles for beta-band oscillations in the olfactory network (Kay et al 2009), our results confirm that the OT is involved in interregional processing of odor information in behaving animals, as suggested by previous anatomical and physiological studies (Carriero et al 2009;Chiang and Strowbridge 2007;McNamara et al 2004;Schwob and Price 1984a;Scott et al 1980). Whether LFP oscillations aid in the coupling of odor-evoked and/or behaviorally relevant spiking activity into downstream structures remains to be tested.…”

“…The OT receives dense monosynaptic input from mitral and tufted cells in the olfactory bulb (OB) (Haberly and Price 1977;Nagayama et al 2010;Schwob and Price 1984b;Scott et al 1980;White 1965), as well as bisynaptic input from piriform cortex association fibers (Carriero et al 2009;Johnson et al 2000;Luskin and Price 1983). Precisely, mitral and tufted cells project into layer I of the OT (Nagayama et al 2010;Price 1978, 1984a;Scott et al 1980), while the input to layers II and III originates from association fibers in the piriform cortex, dorsal peduncular cortex, and the ventral tenia tecta (Luskin and Price 1983;Schwob and Price 1984b).…”

Laminar and spatial localization of the islands of Calleja in mice

“…These cell layers are designated as layer i (molecular layer), layer ii (dense cell layer), and layer iii (multiform layer) due to their synaptic organization (Scott et al, 1980;Chiang and Strowbridge, 2007;Carriero et al, 2009) and cellular composition (Millhouse and Heimer, 1984). Whether or not the IC disproportionately occupy the different OT layers of the mouse is unknown.…”

The in vitro isolated whole guinea pig brain as a model to study epileptiform activity patterns

“…The most frequently explored areas in the IWB are the olfactory and limbic regions: activity have been recorded in the olfactory bulb (OB; Uva et al, 2006;Carriero et al, 2009), in the piriform cortex (PC; de Curtis, 1995, 2000;Biella et al, 1996), in the amygdala (Carriero et al, 2009), in the entorhinal and perirhinal cortex (EC and PRC;Biella et al, , 2002Gnatkovsky et al, 2004) and in the hippocampal region such as the CA1 region, the dentate gyrus (DG) and the subiculum (Boido et al, 2014;de Curtis, 2003, 2005). These regions can be easily reached in the IWB when the brain is positioned in the recording chamber with its ventral surface exposed (Fig.…”