Human olfaction: a constant state of change-blindness

Abstract

Paradoxically, although humans have a superb sense of smell, they don't trust their nose. Furthermore, although human odorant detection thresholds are very low, only unusually high odorant concentrations spontaneously shift our attention to olfaction. Here we suggest that this lack of olfactory awareness reflects the nature of olfactory attention that is shaped by the spatial and temporal envelopes of olfaction. Regarding the spatial envelope, selective attention is allocated in space. Humans direct an attentional spotlight within spatial coordinates in both vision and audition. Human olfactory spatial abilities are minimal. Thus, with no olfactory space, there is no arena for olfactory selective attention. Regarding the temporal envelope, whereas vision and audition consist of nearly continuous input, olfactory input is discreet, made of sniffs widely separated in time. If similar temporal breaks are artificially introduced to vision and audition, they induce "change blindness", a loss of attentional capture that results in a lack of awareness to change. Whereas "change blindness" is an aberration of vision and audition, the long inter-sniff-interval renders "change anosmia" the norm in human olfaction. Therefore, attentional capture in olfaction is minimal, as is human olfactory awareness. All this, however, does not diminish the role of olfaction through sub-attentive mechanisms allowing subliminal smells a profound influence on human behavior and perception.

Fig. 1

Schematic of the human olfactory system. Odorants are transduced at the olfactory epithelium (1). Different receptor types (three illustrated, 1,000 in mammals) converge via the olfactory nerve onto common glomeruli at the olfactory bulb (2). From here information is conveyed via the lateral olfactory tract to primary olfactory cortex (3). From here, information is further relayed throughout the brain, most notably to orbitofrontal cortex (5) via a direct and indirect route through the thalamus (4)

Fig. 2

No space for human olfactory attention. a Results from Porter et al. . Humans have good allocentric olfactory abilities, and can follow a scent trail. b Scent-trail tracking speed increases with each of 4 days of practice. c Results from Porter et al. . Humans have poor egocentric olfactory abilities, and are only marginally but significantly above chance at localizing the pure olfactant PEA to either the left or right of the nose. Note significantly better performance for propionic acid that has a significant trigeminal component. D. Brain mechanisms involved in extracting spatial information from smell, including the superior temporal gyrus

Fig. 3

No time for human olfactory attention. a, b. Results from Youngentob et al. . Two typical sniff-traces from rats. Note the time-scale bar is at 0.1 s. In other words, sniffing is portrayed at ~9 Hz within the sniffing bout. c A typical sniff-trace from a human subject in our lab. The subject generated 2 sniffs in 4 s, i.e. 0.5 Hz. The long delay between each sniff in the sniffing bout is sufficient in our view for change-anosmia

Fig. 4

Sniff 1. Carefully examine this picture, then look at a blank page, and then turn the page to look at Fig. 5

Fig. 5

Sniff 2 Do you see the change from sniff 1? Probably not. Such is human olfaction: discreet samples of sensory content separated by prolonged periods of no input. Now repeat rapidly without the inter-sniff-interval

Fig. 6

The influence of subliminal odors a Results from Li et al. . Increased odor awareness (x axis) was associated with a reduced influence on judgments (y axis). b Results from Epple and Herz (1999). Mean performance on a cognitive test by 5-year old children as a function of odor condition. Participants in the “same odor” condition (an odor previously associated with a frustrating task) performed worse than participants in the “different odor” or “no odor” groups (P < 0.05). c Results from Holland et al. (2005). Mean reaction times for cleaning related words and control words in odor and control conditions (without an odor) during a lexical decision task. Participants responded faster to cleaning-related words than to control words (P < 0.05), and excluding participants that have been aware of the odor, revealed a significant interaction between odor presence and word type (P < 0.05)