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• W2024939917 abstract "The olfactory system has generated considerable interest in recent years, mainly focused on receptor genes and early olfactory processing. In this issue of Neuron, Mori et al. focus centrally, providing evidence for slow- and fast-wave states in olfactory cortex that appear to gate the inflow of information underlying conscious smell perception. The olfactory system has generated considerable interest in recent years, mainly focused on receptor genes and early olfactory processing. In this issue of Neuron, Mori et al. focus centrally, providing evidence for slow- and fast-wave states in olfactory cortex that appear to gate the inflow of information underlying conscious smell perception. A consensus has been emerging in recent years on the steps involved in what may be called early olfaction (Wilson and Stevenson, 2003Wilson D.A. Stevenson R.J. Neurosci. Biobehav. Rev. 2003; 27: 307-328Crossref PubMed Scopus (145) Google Scholar, Shepherd, 2005Shepherd G.M. Chem. Senses. 2005; 30: i3-i5Crossref PubMed Scopus (27) Google Scholar). These begin with the combinatorial transduction of odor molecules by a large family of olfactory receptors (Buck and Axel, 1991Buck L.B. Axel R. Cell. 1991; 65: 175-189Abstract Full Text PDF PubMed Scopus (3446) Google Scholar, Malnic et al., 1999Malnic B. Hrono J. Sato T. Buck L.B. Cell. 1999; 96: 713-723Abstract Full Text Full Text PDF PubMed Scopus (1590) Google Scholar); conversion of those responses into odor maps (“odor images”) in the glomerular layer of the olfactory bulb (summarized in Xu et al., 2000Xu F. Greer C.A. Shepherd G.M. J. Comp. Neurol. 2000; 422: 489-495Crossref PubMed Scopus (136) Google Scholar); extraction of features of the odor maps by synaptic microcircuits in the bulb (Mori and Yoshihara, 1995Mori K. Yoshihara Y. Prog. Neurobiol. 1995; 45: 585-619Crossref PubMed Scopus (207) Google Scholar); and processing of the maps into a content-addressable memory representation in the olfactory cortex (Haberly, 2001Haberly L.B. Chem. Senses. 2001; 26: 551-576Crossref PubMed Scopus (481) Google Scholar, Wilson and Stevenson, 2003Wilson D.A. Stevenson R.J. Neurosci. Biobehav. Rev. 2003; 27: 307-328Crossref PubMed Scopus (145) Google Scholar). This combination of evidence represents a tremendous advance for the field, putting our understanding of early olfaction on par with early vision (Tsodyks and Gilbert, 2004Tsodyks M. Gilbert C. Nature. 2004; 431: 775-781Crossref PubMed Scopus (110) Google Scholar) and initial processing in other sensory systems. At the olfactory cortex, however, we reach an impasse. There is a common assumption, explicit or implicit, that conscious perception of smell may arise in this three-layered cortex. However, in other sensory systems, conscious perception depends on a pathway to the level of the neocortex, and in those systems this requires going through thalamus (see, for example, Pinault, 2004Pinault D. Brain Res. Brain Res. Rev. 2004; 46: 1-31Crossref PubMed Scopus (393) Google Scholar). For many years it was thought that the olfactory pathway also passes through the thalamus, from olfactory cortex through the mediodorsal thalamic nucleus to prefrontal cortex. However, recent careful anatomical studies have shown that the pathway between olfactory cortex and prefrontal cortex is mostly direct, with only a small contingent of fibers going to mediodorsal thalamus (Ongur and Price, 2000Ongur D. Price J.L. Cereb. Cortex. 2000; 10: 206-219Crossref PubMed Scopus (1916) Google Scholar). Within prefrontal cortex, the primary olfactory area consists of the medial and lateral orbitofrontal cortex. This mainly direct pathway to the neocortex, for the most part bypassing the thalamus, raises a host of questions regarding the neural substrate for conscious smell perception. Where does conscious perception arise? At the level of the olfactory cortex or orbitofrontal cortex? How does activity in the olfactory pathway relate to the alternating levels of activity between waking and deep sleep that are found in all other systems? How does synchronization of activity between olfactory and nonolfactory systems occur? How can conscious perception of odors arise without the participation of the thalamus? If olfaction does not require a thalamic relay, what does this tell us about the presumably critical role that the thalamus plays for the conscious state in other sensory systems? In this issue of Neuron, Murakami et al., 2005Murakami M. Kashiwadani H. Kirino Y. Mori K. Neuron. 2005; 46 (this issue): 285-296Abstract Full Text Full Text PDF PubMed Scopus (150) Google Scholar have taken the first step toward answering these questions by asking: is there evidence for waking and deep sleep states in the cellular activity of the olfactory cortex? They carried out experiments in the urethane-anesthetized rat, in which the cortical EEG showed the well-known spontaneous alternations between a fast-wave state (FWS) and slow-wave state (SWS). Single-cell recordings from the olfactory cortex showed vigorous spike discharge responses to odors during FWS but not SWS. This indicated that the flow of activity through the olfactory pathway was gated in relation to behavioral state in a manner similar to other sensory systems (Steriade and Llinas, 1988Steriade M. Llinas R.R. Physiol. Rev. 1988; 68: 649-742PubMed Google Scholar). The authors carried out further experiments to document this finding. The gating applied across the odors tested, and thus was not odor specific. It was found with both natural and artifical respiration. It was particularly prominent in the olfactory cortex, including the anterior pyriform area and the olfactory tubercle, but was largely absent from the olfactory bulb; the small degree of gating found there may reflect the action of the long association fibers in the cortex recurring to the olfactory bulb. Membrane mechanisms were analyzed with intracellular recordings, which showed that during SWS the membrane potential oscillated between up (depolarized) and down (hyperpolarized) states, changing to an up, depolarized state during FWS. The olfactory SWS oscillations were synchronized with the generalized SWS oscillations of the cortical EEG. Electrical stimulation of the olfactory bulb evoked excitatory postsynaptic potentials (EPSPs) in olfactory cortical neurons. An intriguing finding was that this EPSP is larger during the hyperpolarizing phase, but does not reach spike threshold because of the hyperpolarizing shift. This suggests that gating does not block the input from the olfactory bulb or the EPSP response, but acts through a mechanism of disfacilitation similar to that shown in neocortical neurons during SWS. Further experiments will be needed to test for this mechanism. How is gating in the olfactory pathway coordinated with gating in other sensory systems? To test for this, the authors carried out electrical stimulation of the brainstem interpeduncular nucleus during SWS to mimick the action of the reticular activating system that is known to underlie the FWS. By this route they converted the cortical EEG from SWS to FWS and concurrently changed a weak odor response to a strong one. This suggested that the gating control originates in the brainstem ascending reticular formation and broadly affects all cortical areas, including the olfactory areas, in synchrony with thalamic gating of the other systems. Like any pioneering study, this report only scratches the surface. Other systems that may contribute to the synchronizing action with the rest of the brain are the various transmitter systems that project widely throughout the cortex, including serotonergic and noradrenergic projections from the brainstem, and cholinergic projections from the basal forebrain. The most pressing need now is to understand the processing step from olfactory cortex to orbitofrontal cortex at the neocortical level. We've arrived at the gate, but what lies beyond? The first functional study to address this problem was carried out many years ago by Mori's mentor, Sadayuki Takagi. In a tour de force, he and his colleagues (Tanabe et al., 1975Tanabe T. Iino M. Takagi S.F. J. Neurophysiol. 1975; 38: 1284-1296PubMed Google Scholar) made single-cell recordings in the monkey and showed that there is a progressive sharpening of the response spectrum from olfactory bulb through olfactory cortex to orbitofrontal cortex, reflecting a type of feature extraction at the highest cortical level. In awake behaving monkeys, most neurons in the olfactory region of the orbitofrontal cortex decrease their responses to an odor of a food to which the monkey is fed to satiety (Critchley and Rolls, 1996Critchley H.D. Rolls E.T. J. Neurophysiol. 1996; 75: 1673-1686PubMed Google Scholar), indicating that these neurons encode the reward value and relative pleasantness or unpleasantness of a stimulus within its behavioral context. This property, however, is not exclusive to orbitofrontal cortex; it has also been seen in recordings from mitral cells in the rat olfactory bulb (Pager, 1974Pager J. Physiol. Behav. 1974; 12: 189-195Crossref PubMed Scopus (48) Google Scholar) and in some neurons in olfactory cortex (Schoenbaum and Eichenbaum, 1995Schoenbaum G. Eichenbaum H. J. Neurophysiol. 1995; 74: 733-750PubMed Google Scholar). It appears that behavioral context is communicated to multiple levels of the olfactory pathway. These multiple levels apparently bridge across the gating between regions such as olfactory cortex and orbitofrontal cortex. The fact that olfactory processing begins in the olfactory bulb with “odor images” analogous to visual images (Haberly, 1985Haberly L.B. Chem. Senses. 1985; 10: 219-238Crossref Scopus (186) Google Scholar, Haberly, 2001Haberly L.B. Chem. Senses. 2001; 26: 551-576Crossref PubMed Scopus (481) Google Scholar, Shepherd, 2005Shepherd G.M. Chem. Senses. 2005; 30: i3-i5Crossref PubMed Scopus (27) Google Scholar, Shepherd, 1991Shepherd G.M. Eichenbaum H. Davis J. Olfaction: A Model for Computational Neuroscience. MIT Press, Cambridge, MA1991: 3-42Google Scholar, Wilson and Stevenson, 2003Wilson D.A. Stevenson R.J. Neurosci. Biobehav. Rev. 2003; 27: 307-328Crossref PubMed Scopus (145) Google Scholar) suggests possible parallels with central vision. It will be important to identify exactly what kind of higher level of processing of these images takes place in orbitofrontal cortex compared to olfactory cortex, and how it relates to specific psychophysical attributes of conscious smell perception. As these experiments are undertaken, the knowledge that the olfactory pathway is subject to gating of sensory inflow similar to that which occurs in other sensory systems will be critical to planning the strategy and interpreting the results." @default.
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• W2024939917 title "Perception without a Thalamus" @default.
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