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Attention and Olfactory Consciousness City University of New York (CUNY) CUNY Academic Works Publications and Research CUNY Graduate Center 2011 Attention and olfactory consciousness Andreas Keller CUNY Graduate Center How does access to this work benefit ou?y Let us know! More information about this work at: https://academicworks.cuny.edu/gc_pubs/357 Discover additional works at: https://academicworks.cuny.edu This work is made publicly available by the City University of New York (CUNY). Contact: [email protected] REVIEW ARTICLE published: 16 December 2011 doi: 10.3389/fpsyg.2011.00380 Attention and olfactory consciousness Andreas Keller* Department of Philosophy, Graduate Center, City University of New York, New York, NY, USA Edited by: Understanding the relation between attention and consciousness is an important part of Naotsugu Tsuchiya, RIKEN, Japan our understanding of consciousness. Attention, unlike consciousness, can be systemati- Reviewed by: cally manipulated in psychophysical experiments and a law-like relation between attention David Rosenthal, City University of New York, USA and consciousness is waiting to be discovered. Most attempts to discover the nature of Giorgio Marchetti, Mind, this relation are focused on a special type of attention: spatial visual attention. In this review Consciousness, and Language, Italy I want to introduce another type of attention to the discussion: attention to the olfactory *Correspondence: modality. I will first clarify the position of attention to smells in a general taxonomy of atten- Andreas Keller, Department of tion. I will then review the mechanisms and neuroanatomy of attention and consciousness Philosophy, Graduate Center, City University of New York, 365 Fifth in the olfactory system before using the newly introduced system to provide evidence that Avenue, New York, NY 10016, USA. attention is necessary for consciousness. e-mail: [email protected] Keywords: olfaction, attention, consciousness, odor, orbitofrontal cortex, piriform cortex INTRODUCTION A TAXONOMY OF OLFACTORY ATTENTION Knowledge about the relation between attention and conscious- The study of attention in the olfactory modality is in its infancy. ness is invaluable for the empirical study of consciousness because A search of literature databases will reveal that there are almost a attention can be varied experimentally and its effect on conscious thousand times more papers on visual attention than on olfactory perception can be measured. The discussion of how attention attention. Before discussing attention in the olfactory modality it relates to consciousness has so far been based primarily on empir- is therefore necessary to clarify what types of olfactory attention ical results from the study of spatial visual attention (Dehaene there are and how they relate to other types of attention. I will et al., 2006; De Brigard and Prinz, 2010; Prinz, 2010; Van Box- accomplish this by placing olfactory attentional processes into a tel et al., 2010). The goal of this paper is to introduce attentional recently introduced general taxonomy of attention (Chun et al., shifts toward the olfactory modality as a second system in which 2011). attention and consciousness interact. The advantage of opening The taxonomy proposed by Chun et al. (2011) is based on up the discussion to facts from a second type of attention is that it what type of information attention operates over. The most basic reduces the likelihood of mistaking special adaptations for general distinction is between external and internal attention. Internal principles. attention operates over internally generated information such as The main motivation to study attention in olfaction is the memories, thoughts, or task rules. External attention operates over computational and anatomical simplicity of the olfactory system sensory information. The types of olfactory attention discussed in (Haberly, 2001; Lledo et al., 2005; Isaacson, 2010; Sela and Sobel, this paper are types of external attention. External attention can 2010). The study of simple systems to reveal general principles has be further subdivided into attention to space, time, objects, or contributed significantly to our understanding of many biologi- features of objects. In addition, there is attention to information cal processes and the olfactory system is an ideal model system generated by a specific modality. I will now discuss these five types for consciousness research. It may even represent the minimal of external attention (spatial attention, temporal attention, atten- neuroanatomy that is required for conscious processing (Morsella tion to objects, attention to features, and attention to a modality) et al., 2010). in olfaction. Toward the goal of introducing attentional shifts toward olfac- tion as a system for the study of attention,this paper has three aims. SPATIAL OLFACTORY ATTENTION The first aim is to develop a taxonomy of olfactory attention that is The paradigmatic case of spatial attention is the allocation of visual integrated into a general taxonomy of attention (Chun et al.,2011). attention to positions in visual space. Visual spatial attention can The second aim is to review what is known about the brain struc- be shifted overtly by body, head, and eye movements or covertly tures that are involved in attentional shifts toward the olfactory by computational means while the fixation point is unchanged. modality and in the conscious processing of olfactory informa- In every-day experience overt shifts of spatial visual attention tion. These first two parts together introduce a system in which are more prominent but covert shifts are also significant (for questions about the relation between attention and consciousness example, Wojciulik et al., 1998). Other senses with spatially struc- can be studied. The third aim is to demonstrate the utility of the tured phenomenology, like passive touch, also have computational newly introduced system by answering one of these questions: mechanisms for covert spatial attention (Forster and Eimer, 2004). is attention to smells necessary for the conscious processing of Overt spatial shifts of attention are possible in olfaction. In smells? the same way in which visual attention can be shifted in space by www.frontiersin.org December 2011 | Volume 2 | Article 380 | 1 Keller Olfactory consciousness and attention turning the head, olfactory attention can be shifted in space by temporally unstructured. The experience in one sniff can be influ- placing the nose over different objects that are giving off odors. enced by the previous sniff, but these influences are generally not These overt shifts of olfactory spatial attention allow us to locate considered to be an olfactory version of the attentional blink but sources of odors and to track scents (Porter et al., 2006). The study rather effects of habituation or adaptation. of overt shifts of spatial attention to elucidate the relation between In summary, attention toward smells can be temporally struc- attention and consciousness is complicated by the fact that overtly tured. One can allocate attention toward smells during lunchtime shifting olfactory or visual attention changes the sensory input. but not for the rest of the day. However, olfaction is a “slower” Covert shifts, in which the sensory input remains the same and the sense than vision. Photons are faster than the odor molecules only difference is how attention is distributed over the visual field, diffusing through the olfactory mucus that covers the olfactory have been more informative for questions about consciousness sensory neurons in the nose. As a consequence many phenomena and attention. of fast temporal attention shifts that are studied in vision have no However, covert spatial shifts of attention are only possible in equivalent in olfaction. modalities in which the sensory experience has a spatial structure. Odor experiences are one example of spatially unstructured sen- ATTENTION TO OLFACTORY OBJECTS sory experiences (Radil and Wysocki, 1998; Frasnelli et al., 2008). Several different notions of “olfactory objects” have been intro- Some researchers have suggested that an olfactory experience has duced but none of them has become widely accepted. Olfactory a very simple spatial structure that consists of two locations: left objects could be clouds of molecules (Lycan, 2000). Alternatively, (nostril) and right (nostril; Porter et al., 2005, 2006). Even if this it has been suggested that “olfactory sources (objects that produce is the spatial structure of an olfactory experience, there is no evi- odors, such as a lion) and olfactory events (odors that emanate dence that attention can be shifted between the nostrils. There is from objects, such as a musky lion smell) can be thought of as therefore no evidence for covert spatial olfactory attention. olfactory objects”(Gottfried, 2010). A third notion has been intro- duced by Yeshurun and Sobel (2010) who propose that the odor TEMPORAL OLFACTORY ATTENTION object is the pleasantness of an odor. It has been shown that in vision attention can not only be allocated The relevant question for the possibility of attention to olfac- over space but also over time (Coull and Nobre, 1998). This type tory objects is if more than a single odor object can be experienced of attention can be tested in experiments which involve a cue that at the same time. If every odor experience consists of a single informs the subject at what time after the cue a stimulus can be object, there is nothing for olfactory object-based attention
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